Embolism resistance explains mortality and recovery of five subtropical evergreen broadleaf trees to persistent drought

Shao, Junjiong; Zhou, Xuhui; Zhang, Peipei; Zhai, Deping; Yuan, Tengfei; Li, Zhen; He, Yanghui; McDowell, Nate G.

doi:10.1002/ecy.3877

Embolism resistance explains mortality and recovery of five subtropical evergreen broadleaf trees to persistent drought

Journal Article · Fri Sep 30 00:00:00 EDT 2022 · Ecology

DOI:https://doi.org/10.1002/ecy.3877· OSTI ID:1922896

Shao, Junjiong ^[1]; ^[2]; Zhang, Peipei ^[3]; Zhai, Deping ^[4]; Yuan, Tengfei ^[5]; Li, Zhen ^[6]; He, Yanghui ^[2]; ^[7]

East China Normal Univ. (ECNU), Shanghai (China); Zhejiang A&F Univ., Hangzhou (China)
East China Normal Univ. (ECNU), Shanghai (China); Northeast Forestry Univ., Harbin (China)
East China Normal Univ. (ECNU), Shanghai (China); Chinese Academy of Sciences (CAS), Chengdu (China)
East China Normal Univ. (ECNU), Shanghai (China); Yunnan Univ., Kunming (China)
East China Normal Univ. (ECNU), Shanghai (China); Nanjing Univ. (China)
East China Normal Univ. (ECNU), Shanghai (China)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Washington State Univ., Pullman, WA (United States)

Subtropical evergreen broadleaf forest (SEBF) is experiencing and expected to suffer more frequent and severe drought events. However, how the hydraulic traits directly link to the mortality and recovery of SEBF trees remains unclear. In this study, we conducted a drought-rewatering experiment on tree seedlings of five dominant species to investigate how the hydraulic traits were related to tree mortality and the resistance and recovery of photosynthesis (A) and transpiration (E) under different drought severities. Species with greater embolism resistance (P₅₀) survived longer than those with the weaker P₅₀. However, there was no general hydraulic threshold associated with tree mortality, with the lethal hydraulic failure varying from 64% to 93% loss of conductance. Further, the photosynthesis and transpiration of tree species with greater P₅₀ were more resistant to and recovered faster from drought than those with lower P₅₀. Other plant traits could not explain the interspecific variation in tree mortality and drought resistance and recovery. These results highlight the unique importance of embolism resistance in driving carbon and water process under persistent drought across different trees in SEBF. The absence of multiple efficient drought strategies in SEBF seedlings implies the difficulty of natural seedling regeneration under future droughts, which often occurs after destructive disturbances (e.g., extreme drought events and typhoon), suggesting that this biome may be highly vulnerable to co-occurring climate extremes.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: National Key Research and Development Program of China; National Natural Science Foundation of China (NSFC); USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1922896

Report Number(s):: PNNL-SA-181482

Journal Information:: Ecology, Journal Name: Ecology Journal Issue: 2 Vol. 104; ISSN 0012-9658

Publisher:: Ecological Society of America (ESA)Copyright Statement

Country of Publication:: United States

Language:: English

References (61)

The role of isohydric and anisohydric species in determining ecosystem-scale response to severe drought Roman, D. T.; Novick, K. A.; Brzostek, E. R. Oecologia, Vol. 179, Issue 3 https://doi.org/10.1007/s00442-015-3380-9	journal	July 2015
Typhoon Disturbance and Forest Dynamics: Lessons from a Northwest Pacific Subtropical Forest Lin, Teng-Chiu; Hamburg, Steven P.; Lin, Kuo-Chuan Ecosystems, Vol. 14, Issue 1 https://doi.org/10.1007/s10021-010-9399-1	journal	November 2010
Drought Influences the Accuracy of Simulated Ecosystem Fluxes: A Model-Data Meta-analysis for Mediterranean Oak Woodlands Vargas, Rodrigo; Sonnentag, Oliver; Abramowitz, Gab Ecosystems, Vol. 16, Issue 5 https://doi.org/10.1007/s10021-013-9648-1	journal	February 2013
Fitting net photosynthetic light-response curves with Microsoft Excel — a critical look at the models Lobo, F. de A.; de Barros, M. P.; Dalmagro, H. J. Photosynthetica, Vol. 51, Issue 3 https://doi.org/10.1007/s11099-013-0045-y	journal	June 2013
Shifts in plant nutrient use strategies under secondary forest succession Yan, En-Rong; Wang, Xi-Hua; Huang, Jian-Jun Plant and Soil, Vol. 289, Issue 1-2 https://doi.org/10.1007/s11104-006-9128-x	journal	November 2006
Anisohydric behaviour in grapevines results in better performance under moderate water stress and recovery than isohydric behaviour Pou, Alícia; Medrano, Hipólito; Tomàs, Magdalena Plant and Soil, Vol. 359, Issue 1-2 https://doi.org/10.1007/s11104-012-1206-7	journal	March 2012
Xylem embolism refilling and resilience against drought-induced mortality in woody plants: processes and trade-offs Klein, Tamir; Zeppel, Melanie J. B.; Anderegg, William R. L. Ecological Research https://doi.org/10.1007/s11284-018-1588-y	journal	March 2018
Contrasting drought sensitivity and post-drought resilience among three co-occurring tree species in subtropical China Duan, Honglang; Li, Yiyong; Xu, Yue Agricultural and Forest Meteorology, Vol. 272-273 https://doi.org/10.1016/j.agrformet.2019.03.024	journal	July 2019
Recovery responses of photosynthesis, transpiration, and stomatal conductance in kidney bean following drought stress Miyashita, K.; Tanakamaru, S.; Maitani, T. Environmental and Experimental Botany, Vol. 53, Issue 2 https://doi.org/10.1016/j.envexpbot.2004.03.015	journal	April 2005
Responses of Chinese fir and Schima superba seedlings to light gradients: Implications for the restoration of mixed broadleaf-conifer forests from Chinese fir monocultures Liu, Bo; Liu, Qingqing; Daryanto, Stefani Forest Ecology and Management, Vol. 419-420 https://doi.org/10.1016/j.foreco.2018.03.033	journal	July 2018
What do you mean, ‘resilient’? Hodgson, Dave; McDonald, Jenni L.; Hosken, David J. Trends in Ecology & Evolution, Vol. 30, Issue 9 https://doi.org/10.1016/j.tree.2015.06.010	journal	September 2015
Increasing drought under global warming in observations and models Dai, Aiguo Nature Climate Change, Vol. 3, Issue 1 https://doi.org/10.1038/nclimate1633	journal	August 2012
A multi-species synthesis of physiological mechanisms in drought-induced tree mortality Adams, Henry D.; Zeppel, Melanie J. B.; Anderegg, William R. L. Nature Ecology & Evolution, Vol. 1, Issue 9 https://doi.org/10.1038/s41559-017-0248-x	journal	August 2017
Mechanisms of woody-plant mortality under rising drought, CO2 and vapour pressure deficit McDowell, Nate G.; Sapes, Gerard; Pivovaroff, Alexandria Nature Reviews Earth & Environment, Vol. 3, Issue 5 https://doi.org/10.1038/s43017-022-00272-1	journal	March 2022
Severe summer heatwave and drought strongly reduced carbon uptake in Southern China Yuan, Wenping; Cai, Wenwen; Chen, Yang Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep18813	journal	January 2016
New handbook for standardised measurement of plant functional traits worldwide Pérez-Harguindeguy, N.; Díaz, S.; Garnier, E. Australian Journal of Botany, Vol. 61, Issue 3 https://doi.org/10.1071/BT12225	journal	January 2013
High carbon dioxide uptake by subtropical forest ecosystems in the East Asian monsoon region Yu, Guirui; Chen, Zhi; Piao, Shilong Proceedings of the National Academy of Sciences, Vol. 111, Issue 13 https://doi.org/10.1073/pnas.1317065111	journal	March 2014
Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe Anderegg, William R. L.; Klein, Tamir; Bartlett, Megan Proceedings of the National Academy of Sciences, Vol. 113, Issue 18 https://doi.org/10.1073/pnas.1525678113	journal	April 2016
The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought Bartlett, Megan K.; Klein, Tamir; Jansen, Steven Proceedings of the National Academy of Sciences, Vol. 113, Issue 46 https://doi.org/10.1073/pnas.1604088113	journal	November 2016
Resistance of African tropical forests to an extreme climate anomaly Bennett, Amy C.; Dargie, Greta C.; Cuni-Sanchez, Aida Proceedings of the National Academy of Sciences, Vol. 118, Issue 21 https://doi.org/10.1073/pnas.2003169118	journal	May 2021
A Comparison of Pressure-Volume Curve Data Analysis Techniques Schulte, P. J.; Hinckley, T. M. Journal of Experimental Botany, Vol. 36, Issue 10 https://doi.org/10.1093/jxb/36.10.1590	journal	January 1985
Photosynthesis limitations during water stress acclimation and recovery in the drought-adapted Vitis hybrid Richter-110 (V. berlandieri×V. rupestris) Flexas, Jaume; Barón, Matilde; Bota, Josefina Journal of Experimental Botany, Vol. 60, Issue 8 https://doi.org/10.1093/jxb/erp069	journal	April 2009
Adaptive plasticity in plant traits increases time to hydraulic failure under drought in a foundation tree Challis, Anthea; Blackman, Chris; Ahrens, Collin Tree Physiology, Vol. 42, Issue 4 https://doi.org/10.1093/treephys/tpab096	journal	July 2021
Xylem recovery from drought-induced embolism: where is the hydraulic point of no return? Meinzer, F. C.; McCulloh, K. A. Tree Physiology, Vol. 33, Issue 4 https://doi.org/10.1093/treephys/tpt022	journal	April 2013
Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees Urli, M.; Porte, A. J.; Cochard, H. Tree Physiology, Vol. 33, Issue 7 https://doi.org/10.1093/treephys/tpt030	journal	May 2013
Leaf turgor loss point is correlated with drought tolerance and leaf carbon economics traits Zhu, Shi-Dan; Chen, Ya-Jun; Ye, Qing Tree Physiology, Vol. 38, Issue 5 https://doi.org/10.1093/treephys/tpy013	journal	February 2018
Large branch and leaf hydraulic safety margins in subtropical evergreen broadleaved forest Zhu, Shi-Dan; Li, Rong-Hua; He, Peng-Cheng Tree Physiology, Vol. 39, Issue 8 https://doi.org/10.1093/treephys/tpz028	journal	May 2019
Scaling of petiole anatomies, mechanics and vasculatures with leaf size in the widespread Neotropical pioneer tree species Cecropia obtusa Trécul (Urticaceae) Levionnois, Sébastien; Coste, Sabrina; Nicolini, Eric Tree Physiology, Vol. 40, Issue 2 https://doi.org/10.1093/treephys/tpz136	journal	January 2020
The Evolution of Mechanisms Driving the Stomatal Response to Vapor Pressure Deficit McAdam, Scott A. M.; Brodribb, Timothy J. Plant Physiology, Vol. 167, Issue 3 https://doi.org/10.1104/pp.114.252940	journal	January 2015
Experience of inundation or drought alters the responses of plants to subsequent water conditions Wang, Shu; Callaway, Ragan M.; Zhou, Dao‐Wei Journal of Ecology, Vol. 105, Issue 1 https://doi.org/10.1111/1365-2745.12649	journal	September 2016
Leaf economics and hydraulic traits are decoupled in five species-rich tropical-subtropical forests Li, Le; McCormack, M. Luke; Ma, Chengen Ecology Letters, Vol. 18, Issue 9 https://doi.org/10.1111/ele.12466	journal	June 2015
Plant resistance to drought depends on timely stomatal closure Martin-StPaul, Nicolas; Delzon, Sylvain; Cochard, Hervé Ecology Letters, Vol. 20, Issue 11 https://doi.org/10.1111/ele.12851	journal	September 2017
Global variations in ecosystem-scale isohydricity Konings, Alexandra G.; Gentine, Pierre Global Change Biology, Vol. 23, Issue 2 https://doi.org/10.1111/gcb.13389	journal	July 2016
Tolerance to low leaf water status of tropical tree seedlings is related to drought performance and distribution Kursar, Thomas A.; Engelbrecht, Bettina M. J.; Burke, Amy Functional Ecology, Vol. 23, Issue 1 https://doi.org/10.1111/j.1365-2435.2008.01483.x	journal	February 2009
A method for measuring hydraulic conductivity and embolism in xylem Sperry, J. S.; Donnelly, J. R.; Tyree, M. T. Plant, Cell and Environment, Vol. 11, Issue 1 https://doi.org/10.1111/j.1365-3040.1988.tb01774.x	journal	January 1988
Hierarchical statistical modeling of xylem vulnerability to cavitation Ogle, Kiona; Barber, Jarrett J.; Willson, Cynthia New Phytologist, Vol. 182, Issue 2 https://doi.org/10.1111/j.1469-8137.2008.02760.x	journal	February 2009
Xylem function and growth rate interact to determine recovery rates after exposure to extreme water deficit Brodribb, Tim J.; Bowman, David J. M. S.; Nichols, Scott New Phytologist, Vol. 188, Issue 2 https://doi.org/10.1111/j.1469-8137.2010.03393.x	journal	July 2010
Evaluating theories of drought-induced vegetation mortality using a multimodel-experiment framework McDowell, Nate G.; Fisher, Rosie A.; Xu, Chonggang New Phytologist, Vol. 200, Issue 2 https://doi.org/10.1111/nph.12465	journal	September 2013
A new look at water transport regulation in plants Martínez-Vilalta, Jordi; Poyatos, Rafael; Aguadé, David New Phytologist, Vol. 204, Issue 1 https://doi.org/10.1111/nph.12912	journal	July 2014
New developments in the effort to model ecosystems under water stress Medlyn, Belinda E.; De Kauwe, Martin G.; Duursma, Remko A. New Phytologist, Vol. 212, Issue 1 https://doi.org/10.1111/nph.14082	journal	August 2016
Research frontiers for improving our understanding of drought-induced tree and forest mortality Hartmann, Henrik; Moura, Catarina F.; Anderegg, William R. L. New Phytologist, Vol. 218, Issue 1 https://doi.org/10.1111/nph.15048	journal	February 2018
Anisohydric behavior linked to persistent hydraulic damage and delayed drought recovery across seven North American tree species Kannenberg, Steven A.; Novick, Kimberly A.; Phillips, Richard P. New Phytologist, Vol. 222, Issue 4 https://doi.org/10.1111/nph.15699	journal	February 2019
Thresholds for leaf damage due to dehydration: declines of hydraulic function, stomatal conductance and cellular integrity precede those for photochemistry Trueba, Santiago; Pan, Ruihua; Scoffoni, Christine New Phytologist, Vol. 223, Issue 1 https://doi.org/10.1111/nph.15779	journal	April 2019
Dead or dying? Quantifying the point of no return from hydraulic failure in drought‐induced tree mortality Hammond, William M.; Yu, Kailiang; Wilson, Luke A. New Phytologist, Vol. 223, Issue 4 https://doi.org/10.1111/nph.15922	journal	April 2019
Responses of two semiarid conifer tree species to reduced precipitation and warming reveal new perspectives for stomatal regulation: Stomatal regulation in piñon and juniper trees Garcia-Forner, NúRia; Adams, Henry D.; Sevanto, Sanna Plant, Cell & Environment, Vol. 39, Issue 1 https://doi.org/10.1111/pce.12588	journal	August 2015
Impacts of long-term precipitation manipulation on hydraulic architecture and xylem anatomy of piñon and juniper in Southwest USA: Xylem acclimation in piñon-juniper woodland Hudson, P. J.; Limousin, J. M.; Krofcheck, D. J. Plant, Cell & Environment, Vol. 41, Issue 2 https://doi.org/10.1111/pce.13109	journal	January 2018
Coordination between leaf, stem, and root hydraulics and gas exchange in three arid-zone angiosperms during severe drought and recovery: Coordination between hydraulics and gas exchange during drought and recovery Creek, Danielle; Blackman, Chris J.; Brodribb, Timothy J. Plant, Cell & Environment, Vol. 41, Issue 12 https://doi.org/10.1111/pce.13418	journal	September 2018
Testing the limits of plant drought stress and subsequent recovery in four provenances of a widely distributed subtropical tree species Duan, Honglang; Resco de Dios, Víctor; Wang, Defu Plant, Cell & Environment, Vol. 45, Issue 4 https://doi.org/10.1111/pce.14254	journal	January 2022
Mechanisms of xylem hydraulic recovery after drought in Eucalyptus saligna Gauthey, Alice; Peters, Jennifer M. R.; Lòpez, Rosana Plant, Cell & Environment, Vol. 45, Issue 4 https://doi.org/10.1111/pce.14265	journal	February 2022
The Structure, Distribution, and Biomass of the World's Forests Pan, Yude; Birdsey, Richard A.; Phillips, Oliver L. Annual Review of Ecology, Evolution, and Systematics, Vol. 44, Issue 1 https://doi.org/10.1146/annurev-ecolsys-110512-135914	journal	November 2013
Plantecophys - An R Package for Analysing and Modelling Leaf Gas Exchange Data Duursma, Remko A. PLOS ONE, Vol. 10, Issue 11 https://doi.org/10.1371/journal.pone.0143346	journal	November 2015
Antecedent Drought Condition Affects Responses of Plant Physiology and Growth to Drought and Post-drought Recovery Li, Ximeng; Bao, Jingting; Wang, Jin Frontiers in Forests and Global Change, Vol. 4 https://doi.org/10.3389/ffgc.2021.704470	journal	September 2021
Evolutionary Hotspots of Seed Plants in Subtropical China: A Comparison With Species Diversity Hotspots of Woody Seed Plants Fan, Dengmei; Huang, Jihong; Hu, Huili Frontiers in Genetics, Vol. 9 https://doi.org/10.3389/fgene.2018.00333	journal	August 2018
Cavitation Limits the Recovery of Gas Exchange after Severe Drought Stress in Holm Oak (Quercus ilex L.) Peguero-Pina, José; Mendoza-Herrer, Óscar; Gil-Pelegrín, Eustaquio Forests, Vol. 9, Issue 8 https://doi.org/10.3390/f9080443	journal	July 2018
Plant Hydraulic Trait Covariation: A Global Meta-Analysis to Reduce Degrees of Freedom in Trait-Based Hydrologic Models Mursinna, A.; McCormick, Erica; Van Horn, Katie Forests, Vol. 9, Issue 8 https://doi.org/10.3390/f9080446	journal	July 2018
A global analysis of xylem vessel length in woody plants Jacobsen, Anna L.; Pratt, R. Brandon; Tobin, Michael F. American Journal of Botany, Vol. 99, Issue 10 https://doi.org/10.3732/ajb.1200140	journal	October 2012
Responses of Taxus chinensis and Phoebe chekiangensis seedlings to controlled-release fertilizer in various formulations and application rates Chu, X.; Wang, X.; Zhang, D. iForest - Biogeosciences and Forestry, Vol. 12, Issue 3 https://doi.org/10.3832/ifor2714-012	journal	June 2019
Plant responses to drought and rewatering Xu, Zhenzhu; Zhou, Guangsheng; Shimizu, Hideyuki Plant Signaling & Behavior, Vol. 5, Issue 6 https://doi.org/10.4161/psb.5.6.11398	journal	June 2010
Does predictability of fluxes vary between FLUXNET sites? Haughton, Ned; Abramowitz, Gab; De Kauwe, Martin G. Biogeosciences, Vol. 15, Issue 14 https://doi.org/10.5194/bg-15-4495-2018	journal	January 2018
Dataset of drought-rewatering experiment on five subtropical tree species Shao, Junjiong figshare https://doi.org/10.6084/m9.figshare.20326380	dataset	January 2022
Dataset of drought-rewatering experiment on five subtropical tree species Shao, Junjiong figshare https://doi.org/10.6084/m9.figshare.20326380.v1	dataset	January 2022

Similar Records

Embolism recovery strategies and nocturnal water loss across species influenced by biogeographic origin

Journal Article · Fri Apr 12 20:00:00 EDT 2019 · Ecology and Evolution · OSTI ID:1508659

Related Subjects

54 ENVIRONMENTAL SCIENCES
PLC threshold
drought-rewatering
embolism resistance
recovery
subtropical forest
tree mortality

Embolism resistance explains mortality and recovery of five subtropical evergreen broadleaf trees to persistent drought

Citation Formats

References (61)

Similar Records

Related Subjects