Daytime stomatal regulation in mature temperate trees prioritizes stem rehydration at night.

European forests; canopy conductance; dendrometer; hydraulic traits; leaf water potential; sap flow; stomatal control; wood anatomy; Water; Xylem/physiology; Water/physiology; Droughts; Fluid Therapy; Trees/physiology; Plant Leaves/physiology; Plant Leaves; Trees; Xylem; Physiology; Plant Science

Abstract :

[en] Trees remain sufficiently hydrated during drought by closing stomata and reducing canopy conductance (Gc ) in response to variations in atmospheric water demand and soil water availability. Thresholds that control the reduction of Gc are proposed to optimize hydraulic safety against carbon assimilation efficiency. However, the link between Gc and the ability of stem tissues to rehydrate at night remains unclear. We investigated whether species-specific Gc responses aim to prevent branch embolisms, or enable night-time stem rehydration, which is critical for turgor-dependent growth. For this, we used a unique combination of concurrent dendrometer, sap flow and leaf water potential measurements and collected branch-vulnerability curves of six common European tree species. Species-specific Gc reduction was weakly related to the water potentials at which 50% of branch xylem conductivity is lost (P50 ). Instead, we found a stronger relationship with stem rehydration. Species with a stronger Gc control were less effective at refilling stem-water storage as the soil dries, which appeared related to their xylem architecture. Our findings highlight the importance of stem rehydration for water-use regulation in mature trees, which likely relates to the maintenance of adequate stem turgor. We thus conclude that stem rehydration must complement the widely accepted safety-efficiency stomatal control paradigm.

Disciplines :

Environmental sciences & ecology

Author, co-author :

Peters, Richard ; Université de Liège - ULiège > TERRA Research Centre > Gestion durable des bio-agresseurs ; Laboratory of Plant Ecology, Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Coupure links 653, B-9000, Ghent, Belgium ; Forest Dynamics, Swiss Federal Research Institute for Forest, Snow and Landscape Research (WSL), Zürcherstrasse 111, CH-8903, Birmensdorf, Switzerland

Steppe, Kathy ; Laboratory of Plant Ecology, Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Coupure links 653, B-9000, Ghent, Belgium

Pappas, Christoforos ; Department of Civil Engineering, University of Patras, Rio, Patras, 26504, Greece

Zweifel, Roman ; Forest Dynamics, Swiss Federal Research Institute for Forest, Snow and Landscape Research (WSL), Zürcherstrasse 111, CH-8903, Birmensdorf, Switzerland

Babst, Flurin ; School of Natural Resources and the Environment, University of Arizona, East Lowell Street 1064, Tucson, AZ, 85721, USA ; Laboratory of Tree-Ring Research, University of Arizona, East Lowell Street 1215, Tucson, AZ, 857121, USA

Dietrich, Lars ; Department of Environmental Sciences - Botany, University of Basel, Schönbeinstrasse 6, CH-4056, Basel, Switzerland

von Arx, Georg ; Forest Dynamics, Swiss Federal Research Institute for Forest, Snow and Landscape Research (WSL), Zürcherstrasse 111, CH-8903, Birmensdorf, Switzerland ; Oeschger Centre for Climate Change Research, University of Bern, 3012, Bern, Switzerland

Poyatos, Rafael ; CREAF, E08193 Bellaterra (Cerdanyola del Vallès), Catalonia, Spain ; Universitat Autònoma de Barcelona, E08193 Bellaterra (Cerdanyola del Vallès), Catalonia, Spain

Fonti, Marina ; Forest Dynamics, Swiss Federal Research Institute for Forest, Snow and Landscape Research (WSL), Zürcherstrasse 111, CH-8903, Birmensdorf, Switzerland

Fonti, Patrick ; Forest Dynamics, Swiss Federal Research Institute for Forest, Snow and Landscape Research (WSL), Zürcherstrasse 111, CH-8903, Birmensdorf, Switzerland

More authors (5 more)

Language :

English

Title :

Daytime stomatal regulation in mature temperate trees prioritizes stem rehydration at night.

Publication date :

July 2023

Journal title :

New Phytologist

ISSN :

0028-646X

eISSN :

1469-8137

Publisher :

John Wiley and Sons Inc, England

Volume :

239

Issue :

Pages :

533 - 546

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/nph.18964

Funders :

SNF - Schweizerischer Nationalfonds zur Förderung der wissenschaftlichen Forschung

Funding text :

RLP acknowledges the support of the Swiss National Science Foundation (SNSF), Grant P2BSP3_184475. MG acknowledges funding by Swiss National Science Foundation Project ICOS-CH Phase 3 20FI20_198227. FB acknowledges funding from the project ‘Inside out’ (#POIR.04.04.00-00-5F85/18-00) funded by the HOMING programme of the Foundation for Polish Science co-financed by the European Union under the European Regional Development Fund. LD acknowledges the support provided by the Department of Environmental Sciences at the University of Basel and the Swiss Federal Office for the Environment (FOEN). RP acknowledges support by the grant RTI2018-095297-J-I00 (Spain). CG acknowledges funding by the Swiss National Science Foundation (310030_204697). We would also like to thank three anonymous reviewers for their generous time in providing detailed comments and suggestions, which helped us to improve the presented research.RLP acknowledges the support of the Swiss National Science Foundation (SNSF), Grant P2BSP3_184475. MG acknowledges funding by Swiss National Science Foundation Project ICOS‐CH Phase 3 20FI20_198227. FB acknowledges funding from the project ‘Inside out’ (#POIR.04.04.00‐00‐5F85/18‐00) funded by the HOMING programme of the Foundation for Polish Science co‐financed by the European Union under the European Regional Development Fund. LD acknowledges the support provided by the Department of Environmental Sciences at the University of Basel and the Swiss Federal Office for the Environment (FOEN). RP acknowledges support by the grant RTI2018‐095297‐J‐I00 (Spain). CG acknowledges funding by the Swiss National Science Foundation (310030_204697). We would also like to thank three anonymous reviewers for their generous time in providing detailed comments and suggestions, which helped us to improve the presented research.

Available on ORBi :

since 05 March 2024

Statistics

Number of views

13 (0 by ULiège)

Number of downloads

53 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Abdalla M, Carminati A, Cai G, Javaux M, Ahmed MA. 2021. Stomatal closure of tomato under drought is driven by an increase in soil–root hydraulic resistance. Plant, Cell & Environment 44: 425–431.
Anderegg WRL, Tamir K, Megan B, Lawren S, Pellegrini AFA, Brendan C, Steven J. 2016. Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe. Proceedings of the National Academy of Sciences, USA 113: 5024–5029.
Anderegg WRL, Wolf A, Arango-Velez A, Choat B, Chmura DJ, Jansen S, Kolb T, Li S, Meinzer F, Pita P et al. 2017. Plant water potential improves prediction of empirical stomatal models. PLoS ONE 12: e0185481.
Anderegg WRL, Wolf A, Arango-Velez A, Choat B, Chmura DJ, Jansen S, Kolb T, Li S, Meinzer FC, Pita P et al. 2018. Woody plants optimise stomatal behaviour relative to hydraulic risk. Ecology Letters 21: 968–977.
Aranda I, Gil L, Pardos JA. 2005. Seasonal changes in apparent hydraulic conductance and their implications for water use of European beech (Fagus sylvatica L.) and sessile oak [Quercus petraea (Matt.) Liebl] in South Europe. Plant Ecology 179: 155–167.
Arend M, Link RM, Patthey R, Hoch G, Schuldt B, Kahmen A. 2021. Rapid hydraulic collapse as cause of drought-induced mortality in conifers. Proceedings of the National Academy of Sciences, USA 118: e2025251118.
Arend M, Link RM, Zahnd C, Hoch G, Schuldt B, Kahmen A. 2022. Lack of hydraulic recovery as a cause of post-drought foliage reduction and canopy decline in European beech. New Phytologist 234: 1195–1205.
von Arx G, Carrer M. 2014. roxas: a new tool to build centuries-long tracheid-lumen chronologies in conifers. Dendrochronologia 32: 290–293.
Babst F, Bouriaud O, Poulter B, Trouet V, Girardin MP, Frank DC. 2019. Twentieth century redistribution in climatic drivers of global tree growth. Science Advances 5: eaat4313.
Babst F, Poulter B, Trouet V, Tan K, Neuwirth B, Wilson R, Carrer M, Grabner M, Tegel W, Levanic T et al. 2013. Site- and species-specific responses of forest growth to climate across the European continent. Global Ecology and Biogeography 22: 706–717.
Bachofen C, Poyatos R, Flo V, Martínez-Vilalta J, Mencuccini M, Granda V, Grossiord C. 2023. Stand structure of Central European forests matters more than climate for transpiration sensitivity to VPD. Journal of Applied Ecology 60: 886–897.
Bartlett MK, Klein T, Jansen S, Choat B, Sack L. 2016. The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought. Proceedings of the National Academy of Sciences, USA 113: 13098–13103.
Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 1–48.
Brinkmann N, Eugster W, Buchmann N, Kahmen A. 2018. Species-specific differences in water uptake depth of mature temperate trees vary with water availability in the soil. Plant Biology 21: 71–81.
Brodribb TJ, Holbrook NM. 2004. Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms. New Phytologist 162: 663–670.
Brodribb TJ, McAdam SAM, Jordan GJ, Martins SCV. 2014. Conifer species adapt to low-rainfall climates by following one of two divergent pathways. Proceedings of the National Academy of Sciences, USA 111: 14489–14493.
Buckley TN. 2019. How do stomata respond to water status? New Phytologist 224: 21–36.
Buras A, Rammig A, Zang CS. 2020. Quantifying impacts of the 2018 drought on European ecosystems in comparison to 2003. Biogeosciences 17: 1655–1672.
Cabon A, Kannenberg SA, Arain A, Babst F, Baldocchi D, Belmecheri S, Delpierre N, Guerrieri R, Maxwell JT, McKenzie S et al. 2022. Cross-biome synthesis of source versus sink limits to tree growth. Science 376: 758–761.
Carminati A, Ahmed MA, Zarebanadkouki M, Cai G, Lovric G, Javaux M. 2020. Stomatal closure prevents the drop in soil water potential around roots. New Phytologist 226: 1541–1543.
Carminati A, Javaux M. 2020. Soil rather than xylem vulnerability controls stomatal response to drought. Trends in Plant Science 25: 868–880.
Choat B, Brodribb TJ, Brodersen CR, Duursma RA, López R, Medlyn BE. 2018. Triggers of tree mortality under drought. Nature 558: 531–539.
Cochard H, Damour G, Bodet C, Tharwat I, Poirier M, Améglio T. 2005. Evaluation of a new centrifuge technique for rapid generation of xylem vulnerability curves. Physiologia Plantarum 124: 410–418.
Comstock J, Mencuccini M. 1998. Control of stomatal conductance by leaf water potential in Hymenoclea salsola (T. & G.), a desert subshrub. Plant, Cell & Environment 21: 1029–1038.
Coussement JR, Villers SLY, Nelissen H, Inzé D, Steppe K. 2021. Turgor-time controls grass leaf elongation rate and duration under drought stress. Plant, Cell & Environment 44: 1361–1378.
Cowan IR, Farquhar GD. 1977. Stomatal function in relation to leaf metabolism and environment. Symposia of the Society for Experimental Biology 31: 471–505.
Damour G, Simonneau T, Cochard H, Urban L. 2010. An overview of models of stomatal conductance at the leaf level. Plant, Cell & Environment 33: 1419–1438.
Darwin F. 1898. Observations on stomata. Proceedings of the Royal Society of London 63: 413–417.
De Schepper V, Steppe K. 2010. Development and verification of a water and sugar transport model using measured stem diameter variations. Journal of Experimental Botany 61: 2083–2099.
Delzon S, Cochard H. 2014. Recent advances in tree hydraulics highlight the ecological significance of the hydraulic safety margin. New Phytologist 203: 355–358.
Dietrich L, Delzon S, Hoch G, Kahmen A. 2019. No role for xylem embolism or carbohydrate shortage in temperate trees during the severe 2015 drought. Journal of Ecology 107: 334–349.
Dietrich L, Kahmen A. 2019. Water relations of drought-stressed temperate trees benefit from short drought-intermitting rainfall events. Agricultural and Forest Meteorology 265: 70–77.
Domec JC, Gartner BL. 2003. Relationship between growth rates and xylem hydraulic characteristics in young, mature and old-growth ponderosa pine trees. Plant, Cell & Environment 26: 471–483.
Domec JC, Schäfer K, Oren R, Kim HS, McCarthy HR. 2010. Variable conductivity and embolism in roots and branches of four contrasting tree species and their impacts on whole-plant hydraulic performance under future atmospheric CO2 concentration. Tree Physiology 30: 1001–1015.
Domec JC, Warren JM, Meinzer FC, Lachenbruch B. 2009. Safety factors for xylem failure by implosion and air-seeding within roots, trunks and branches of young and old conifer trees. IAWA Journal 30: 101–120.
Edwards D, Kerp H, Hass H. 1998. Stomata in early land plants: an anatomical and ecophysiological approach. Journal of Experimental Botany 49: 255–278.
Etzold S, Sterck F, Bose AK, Braun S, Buchmann N, Eugster W, Gessler A, Kahmen A, Peters RL, Vitasse Y et al. 2022. Number of growth days and not length of the growth period determines radial stem growth of temperate trees. Ecology Letters 25: 427–439.
Fatichi S, Pappas C, Ivanov VY. 2016. Modeling plant–water interactions: an ecohydrological overview from the cell to the global scale. Wiley Interdisciplinary Reviews: Water 3: 327–368.
Fatichi S, Pappas C, Zscheischler J, Leuzinger S. 2019. Modelling carbon sources and sinks in terrestrial vegetation. New Phytologist 221: 652–668.
Feng X, Ackerly DD, Dawson TE, Manzoni S, Skelton RP, Vico G, Thompson SE. 2018. The ecohydrological context of drought and classification of plant responses. Ecology Letters 21: 1723–1736.
Flo V, Martínez-Vilalta J, Mencuccini M, Granda V, Anderegg WRL, Poyatos R. 2021. Climate and functional traits jointly mediate tree water-use strategies. New Phytologist 231: 617–630.
Fonti P, Jansen S. 2012. Xylem plasticity in response to climate. New Phytologist 195: 734–736.
Forrester DI, Tachauer IHH, Annighoefer P, Barbeito I, Pretzsch H, Ruiz-Peinado R, Stark H, Vacchiano G, Zlatanov T, Chakraborty T et al. 2017. Generalized biomass and leaf area allometric equations for European tree species incorporating stand structure, tree age and climate. Forest Ecology and Management 396: 160–175.
Gagne MA, Smith DD, McCulloh KA. 2020. Limited physiological acclimation to recurrent heatwaves in two boreal tree species. Tree Physiology 40: 1680–1696.
Gelman A, Su YS. 2021. arm: data analysis using regression and multilevel/hierarchical models. R Package v.1.12-2. [WWW document] URL https://CRAN.R-project.org/package=arm [accessed 15 October 2021].
Gharun M, Hörtnagl L, Paul-Limoges E, Ghiasi S, Feigenwinter I, Burri S, Marquardt K, Etzold S, Zweifel R, Eugster W et al. 2020. Physiological response of Swiss ecosystems to 2018 drought across plant types and elevation. Philosophical Transactions of the Royal Society B: Biological Sciences 375: 20190521.
Granier A. 1985. Une nouvelle méthode pour la mesure du flux de sève brute dans le tronc des arbres. Annals of Forest Science 42: 193–200.
Greenwood S, Ruiz-Benito P, Martínez-Vilalta J, Lloret F, Kitzberger T, Allen CD, Fensham R, Laughlin DC, Kattge J, Bönisch G et al. 2017. Tree mortality across biomes is promoted by drought intensity, lower wood density and higher specific leaf area. Ecology Letters 20: 539–553.
Grossiord C, Buckley TN, Cernusak LA, Novick KA, Poulter B, Siegwolf RTW, Sperry JS, McDowell NG. 2020. Plant responses to rising vapor pressure deficit. New Phytologist 226: 1550–1566.
Grossiord C, Sevanto S, Borrego I, Chan AM, Collins AD, Dickman LT, Hudson PJ, McBranch N, Michaletz ST, Pockman WT et al. 2017. Tree water dynamics in a drying and warming world. Plant, Cell & Environment 40: 1861–1873.
Hammond WM, Williams AP, Abatzoglou JT, Adams HD, Klein T, López R, Sáenz-Romero C, Hartmann H, Breshears DD, Allen CD. 2022. Global field observations of tree die-off reveal hotter-drought fingerprint for Earth's forests. Nature Communications 13: 1761.
Harris I, Osborn TJ, Jones P, Lister D. 2020. Version 4 of the CRU TS monthly high-resolution gridded multivariate climate dataset. Scientific Data 7: 109.
Henry C, John GP, Pan R, Bartlett MK, Fletcher LR, Scoffoni C, Sack L. 2019. A stomatal safety-efficiency trade-off constrains responses to leaf dehydration. Nature Communications 10: 3398.
Hochberg U, Rockwell FE, Holbrook NM, Cochard H. 2018. Iso/anisohydry: a plant–environment interaction rather than a simple hydraulic trait. Trends in Plant Science 23: 112–120.
Hubau W, Lewis SL, Phillips OL, Affum-Baffoe K, Beeckman H, Cuní-Sanchez A, Daniels AK, Ewango CEN, Fauset S, Mukinzi JM et al. 2020. Asynchronous carbon sink saturation in African and Amazonian tropical forests. Nature 579: 80–87.
Hurley AG, Peters RL, Pappas C, Steger DN, Heinrich I. 2022. Addressing the need for interactive, efficient, and reproducible data processing in ecology with the datacleanr R package. PLoS ONE 17: e0268426.
Jarvis PG, Monteith JL, Weatherley PE. 1976. The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 273: 593–610.
Joshi J, Stocker BD, Hofhansl F, Zhou S, Dieckmann U, Prentice IC. 2022. Towards a unified theory of plant photosynthesis and hydraulics. Nature Plants 8: 1304–1316.
Kahmen A, Basler D, Hoch G, Link RM, Schuldt B, Zahnd C, Arend M. 2022. Root water uptake depth determines the hydraulic vulnerability of temperate European tree species during the extreme 2018 drought. Plant Biology 24: 1224–1239.
Kahmen A, Buser T, Hoch G, Grun G, Dietrich L. 2021. Dynamic 2H irrigation pulse labelling reveals rapid infiltration and mixing of precipitation in the soil and species-specific water uptake depths of trees in a temperate forest. Ecohydrology 14: e2322.
Kannenberg SA, Novick KA, Alexander MR, Maxwell JT, Moore DJP, Phillips RP, Anderegg WRL. 2019. Linking drought legacy effects across scales: from leaves to tree rings to ecosystems. Global Change Biology 25: 2978–2992.
Katul G, Manzoni S, Palmroth S, Oren R. 2010. A stomatal optimization theory to describe the effects of atmospheric CO2 on leaf photosynthesis and transpiration. Annals of Botany 105: 431–442.
Klein T. 2014. The variability of stomatal sensitivity to leaf water potential across tree species indicates a continuum between isohydric and anisohydric behaviours. Functional Ecology 28: 1313–1320.
Knüsel S, Peters RL, Haeni M, Wilhelm M, Zweifel R. 2021. Processing and extraction of seasonal tree physiological parameters from stem radius time series. Forests 12: 765.
Koch GW, Sillett SC, Jennings GM, Davis SD. 2004. The limits to tree height. Nature 428: 851–854.
Krejza J, Haeni M, Darenova E, Foltýnová L, Fajstavr M, Světlík J, Nezval O, Bednář P, Šigut L, Horáček P et al. 2022. Disentangling carbon uptake and allocation in the stems of a spruce forest. Environmental and Experimental Botany 196: 104787.
Lemoine R, La Camera S, Atanassova R, Dédaldéchamp F, Allario T, Pourtau N, Bonnemain J-L, Laloi M, Coutos-Thévenot P, Maurousset L et al. 2013. Source-to-sink transport of sugar and regulation by environmental factors. Frontiers in Plant Science 4: 00272.
Lenth RV. 2022. emmeans: estimated marginal means, aka least-squares means. R Package v.1.7.4-1. [WWW document] URL https://CRAN.R-project.org/package=emmeans [accessed 15 May 2022].
Lu P, Urban L, Ping Z. 2004. Granier's Thermal Dissipation Probre (TDP) method for measuring sap flow in trees: theory and practice. Acta Botanica Sinica 46: 631–646.
Mantova M, Menezes-Silva PE, Badel E, Cochard H, Torres-Ruiz JM. 2021. The interplay of hydraulic failure and cell vitality explains tree capacity to recover from drought. Physiologia Plantarum 172: 247–257.
Martínez-Sancho E, Dorado-Liñán I, Hacke UG, Seidel H, Menzel A. 2017a. Contrasting hydraulic architectures of scots pine and sessile oak at their southernmost distribution limits. Frontiers in Plant Science 8: 1–12.
Martínez-Sancho E, Dorado-Liñán I, Heinrich I, Helle G, Menzel A. 2017b. Xylem adjustment of sessile oak at its southern distribution limits. Tree Physiology 37: 903–914.
Martinez-Vilalta J, Anderegg WRL, Sapes G, Sala A. 2019. Greater focus on water pools may improve our ability to understand and anticipate drought-induced mortality in plants. New Phytologist 223: 22–32.
Martínez-Vilalta J, Cochard H, Mencuccini M, Sterck F, Herrero A, Korhonen JFJ, Llorens P, Nikinmaa E, Nolè A, Poyatos R et al. 2009. Hydraulic adjustment of Scots pine across Europe. New Phytologist 184: 353–364.
Martínez-Vilalta J, Garcia-Forner N. 2017. Water potential regulation, stomatal behaviour and hydraulic transport under drought: deconstructing the iso/anisohydric concept. Plant, Cell & Environment 40: 962–976.
Martin-StPaul N, Delzon S, Cochard H. 2017. Plant resistance to drought depends on timely stomatal closure. Ecology Letters 20: 1437–1447.
Mastrotheodoros T, Pappas C, Molnar P, Burlando P, Manoli G, Parajka J, Rigon R, Szeles B, Bottazzi M, Hadjidoukas P et al. 2020. More green and less blue water in the Alps during warmer summers. Nature Climate Change 10: 155–161.
McAdam SAM, Brodribb TJ. 2014. Separating active and passive influences on stomatal control of transpiration. Plant Physiology 164: 1578–1586.
McAdam SAM, Manzi M, Ross JJ, Brodribb TJ, Gómez-Cadenas A. 2016. Uprooting an abscisic acid paradigm: Shoots are the primary source. Plant Signaling & Behavior 11: e1169359.
McCulloh KA, Domec J-C, Johnson DM, Smith DD, Meinzer FC. 2019. A dynamic yet vulnerable pipeline: Integration and coordination of hydraulic traits across whole plants. Plant, Cell & Environment 42: 2789–2807.
McCulloh KA, Johnson DM, Meinzer FC, Woodruff DR. 2014. The dynamic pipeline: hydraulic capacitance and xylem hydraulic safety in four tall conifer species. Plant, Cell & Environment 37: 1171–1183.
McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG et al. 2008. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytologist 178: 719–739.
Medlyn BE, Duursma RA, Eamus D, Ellsworth DS, Prentice IC, Barton CVM, Crous KY, De Angelis P, Freeman M, Wingate L. 2011. Reconciling the optimal and empirical approaches to modelling stomatal conductance. Global Change Biology 17: 2134–2144.
Mencuccini M, Manzoni S, Christoffersen B. 2019a. Modelling water fluxes in plants: from tissues to biosphere. New Phytologist 222: 1207–1222.
Mencuccini M, Rosas T, Rowland L, Choat B, Cornelissen H, Jansen S, Kramer K, Lapenis A, Manzoni S, Niinemets Ü et al. 2019b. Leaf economics and plant hydraulics drive leaf: wood area ratios. New Phytologist 224: 1544–1556.
Novick KA, Ficklin DL, Stoy PC, Williams CA, Bohrer G, Oishi AC, Papuga SA, Blanken PD, Noormets A, Sulman BN et al. 2016. The increasing importance of atmospheric demand for ecosystem water and carbon fluxes. Nature Climate Change 6: 1023–1027.
Novick KA, Konings AG, Gentine P. 2019. Beyond soil water potential: An expanded view on isohydricity including land–atmosphere interactions and phenology. Plant, Cell & Environment 42: 1802–1815.
Oren R, Sperry JS, Katul GG, Pataki DE, Ewers BE, Phillips N, Schäfer KVR. 1999. Survey and synthesis of intra- and interspecific variation in stomatal sensitivity to vapour pressure deficit. Plant, Cell & Environment 22: 1515–1526.
Pappas C, Matheny AM, Baltzer JL, Barr AG, Black TA, Bohrer G, Detto M, Maillet J, Roy A, Sonnentag O et al. 2018. Boreal tree hydrodynamics: asynchronous, diverging, yet complementary. Tree Physiology 38: 953–964.
Peters JMR, Gauthey A, Lopez R, Carins-Murphy MR, Brodribb TJ, Choat B. 2020. Non-invasive imaging reveals convergence in root and stem vulnerability to cavitation across five tree species. Journal of Experimental Botany 71: 6623–6637.
Peters RL, Balanzategui D, Hurley AG, von Arx G, Prendin AL, Cuny HE, Björklund J, Frank DC, Fonti P. 2018. raptor: row and position tracheid organizer in R. Dendrochronologia 47: 10–16.
Peters RL, Klesse S, Fonti P, Frank DC. 2017. Contribution of climate vs larch budmoth outbreaks in regulating biomass accumulation in high-elevation forests. Forest Ecology and Management 401: 147–158.
Peters RL, Pappas C, Hurley AG, Poyatos R, Flo V, Zweifel R, Goossens W, Steppe K. 2021a. Assimilate, process and analyse thermal dissipation sap flow data using the trex R package. Methods in Ecology and Evolution 12: 342–350.
Peters RL, Speich M, Pappas C, Kahmen A, von Arx G, Graf Pannatier E, Steppe K, Treydte K, Stritih A, Fonti P. 2019. Contrasting stomatal sensitivity to temperature and soil drought in mature alpine conifers. Plant, Cell & Environment 42: 1674–1689.
Peters RL, Steppe K, Cuny HE, De Pauw DJW, Frank DC, Schaub M, Rathgeber CBK, Cabon A, Fonti P. 2021b. Turgor – a limiting factor for radial growth in mature conifers along an elevational gradient. New Phytologist 229: 213–229.
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team. 2016. nlme: linear and nonlinear mixed effects models. R Package v.3.1-126. [WWW document] URL http://CRAN.R-project.org/package=nlme [accessed 7 September 2021].
Potkay A, Feng X. 2022. Do stomata optimize turgor-driven growth? A new framework for integrating stomata response with whole-plant hydraulics and carbon balance. New Phytologist 238: 506–528.
Poyatos R, Martínez-Vilalta J, Čermák J, Ceulemans R, Granier A, Irvine J, Köstner B, Lagergren F, Meiresonne L, Nadezhdina N et al. 2007. Plasticity in hydraulic architecture of Scots pine across Eurasia. Oecologia 153: 245–259.
Prendin AL, Petit G, Fonti P, Rixen C, Dawes MA, von Arx G. 2018. Axial xylem architecture of Larix decidua exposed to CO2 enrichment and soil warming at the tree line. Functional Ecology 32: 273–287.
R Core Team. 2017. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. [WWW document] URL https://www.R-project.org/ [accessed 1 April 2023].
Rodriguez-Dominguez CM, Brodribb TJ. 2020. Declining root water transport drives stomatal closure in olive under moderate water stress. New Phytologist 225: 126–134.
Rosas T, Mencuccini M, Barba J, Cochard H, Saura-Mas S, Martínez-Vilalta J. 2019. Adjustments and coordination of hydraulic, leaf and stem traits along a water availability gradient. New Phytologist 223: 632–646.
Salmon Y, Dietrich L, Sevanto S, Hölttä T, Dannoura M, Epron D. 2019. Drought impacts on tree phloem: from cell-level responses to ecological significance. Tree Physiology 39: 173–191.
Salomón RL, Limousin J-M, Ourcival J-M, Rodríguez-Calcerrada J, Steppe K. 2017. Stem hydraulic capacitance decreases with drought stress: implications for modelling tree hydraulics in the Mediterranean oak Quercus ilex. Plant, Cell & Environment 40: 1379–1391.
Salomón RL, Peters RL, Zweifel R, Sass-Klaassen UGW, Stegehuis AI, Smiljanic M, Poyatos R, Babst F, Cienciala E, Fonti P et al. 2022. The 2018 European heatwave led to stem dehydration but not to consistent growth reductions in forests. Nature Communications 13: 28.
Schlesinger WH, Jasechko S. 2014. Transpiration in the global water cycle. Agricultural and Forest Meteorology 189–190: 115–117.
Schuldt B, Buras A, Arend M, Vitasse Y, Beierkuhnlein C, Damm A, Gharun M, Grams TEE, Hauck M, Hajek P et al. 2020. A first assessment of the impact of the extreme 2018 summer drought on Central European forests. Basic and Applied Ecology 45: 86–103.
Schulze E-D, Kelliher FM, Körner C, Lloyd J, Leuning R. 1994. Relationships among maximum stomatal conductance, ecosystem surface conductance, carbon assimilation rate, and plant nitrogen nutrition: a global ecology scaling exercise. Annual Review of Ecology and Systematics 25: 629–662.
Sperry JS, Venturas MD, Anderegg WRL, Mencuccini M, Mackay DS, Wang Y, Love DM. 2017. Predicting stomatal responses to the environment from the optimization of photosynthetic gain and hydraulic cost. Plant, Cell & Environment 40: 816–830.
Steppe K, De Pauw DJW, Lemeur R, Vanrolleghem PA. 2006. A mathematical model linking tree sap flow dynamics to daily stem diameter fluctuations and radial stem growth. Tree Physiology 26: 257–273.
Steppe K, Lemeur R. 2007. Effects of ring-porous and diffuse-porous stem wood anatomy on the hydraulic parameters used in a water flow and storage model. Tree Physiology 27: 43–52.
Steppe K, Sterck F, Deslauriers A. 2015. Diel growth dynamics in tree stems: linking anatomy and ecophysiology. Trends in Plant Science 20: 335–343.
Trotsiuk V, Hartig F, Cailleret M, Babst F, Forrester DI, Baltensweiler A, Buchmann N, Bugmann H, Gessler A, Gharun M et al. 2020. Assessing the response of forest productivity to climate extremes in Switzerland using model–data fusion. Global Change Biology 26: 2463–2476.
Tyree MT, Zimmermann MH. 2002. Hydraulic architecture of whole plants and plant performance. In: Tyree MT, Zimmermann MH, eds. Xylem structure and the ascent of sap. Berlin, Heidelberg, Germany: Springer, 175–214.
Walthert L, Ganthaler A, Mayr S, Saurer M, Waldner P, Walser M, Zweifel R, von Arx G. 2021. From the comfort zone to crown dieback: sequence of physiological stress thresholds in mature European beech trees across progressive drought. Science of the Total Environment 753: 141792.
Wang Y, Sperry JS, Anderegg WRL, Venturas MD, Trugman AT. 2020. A theoretical and empirical assessment of stomatal optimization modeling. New Phytologist 227: 311–325.
Wenping Y, Yi Z, Shilong P, Philippe C, Danica L, Yingping W, Youngryel R, Guixing C, Wenjie D, Zhongming H et al. 2019. Increased atmospheric vapor pressure deficit reduces global vegetation growth. Science Advances 5: eaax1396.
Wolf A, Anderegg WRL, Pacala SW. 2016. Optimal stomatal behavior with competition for water and risk of hydraulic impairment. Proceedings of the National Academy of Sciences, USA 113: E7222–E7230.
Zuur AF, Ieno EN, Elphick CS. 2010. A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1: 3–14.
Zweifel R, Etzold S, Sterck F, Gessler A, Anfodillo T, Mencuccini M, von Arx G, Lazzarin M, Haeni M, Feichtinger L et al. 2020. Determinants of legacy effects in pine trees – implications from an irrigation-stop experiment. New Phytologist 227: 1081–1096.
Zweifel R, Haeni M, Buchmann N, Eugster W. 2016. Are trees able to grow in periods of stem shrinkage? New Phytologist 211: 839–849.
Zweifel R, Steppe K, Sterck FJ. 2007. Stomatal regulation by microclimate and tree water relations: interpreting ecophysiological field data with a hydraulic plant model. Journal of Experimental Botany 58: 2113–2131.
Zweifel R, Sterck F, Braun S, Buchmann N, Eugster W, Gessler A, Häni M, Peters RL, Walthert L, Wilhelm M et al. 2021. Why trees grow at night. New Phytologist 231: 2174–2185.
Zweifel R, Zimmermann L, Zeugin F, Newbery DM. 2006. Intra-annual radial growth and water relations of trees: implications towards a growth mechanism. Journal of Experimental Botany 57: 1445–1459.