Prediction of temperate broadleaf tree species mortality in arid limestone habitats with stomatal safety margins

Abstract A growing body of evidence highlights the occurrence of increased widespread tree mortality during climate change-associated severe droughts; however, in situ long-term drought experiments with multispecies communities for the prediction of tree mortality and exploration of related mechanisms are rather limited in natural environments. We conducted a 7-year afforestation trial with 20 drought-resistant broadleaf tree species in an arid limestone habitat in northern China, where the species displayed a broad range of survival rates. The stomatal and xylem hydraulic traits of all the species were measured. We found that species’ stomatal closure points were strongly related to their xylem embolism resistance and xylem minimum water potential but not to their survival rates. Hydraulic failure of the vascular system appeared to be the main cause of tree mortality, and the stomatal safety margin was a better predictor of tree mortality than the traditionally considered xylem embolism resistance and hydraulic safety margin. We recommend the stomatal safety margin as the indicator for predicting drought-induced tree mortality and for selecting tree species in future forest restorations in arid regions.

Download Full-text

Xylem embolism in leaves does not occur with open stomata: evidence from direct observations using the optical visualization technique

Journal of Experimental Botany ◽

10.1093/jxb/erz474 ◽

2019 ◽

Vol 71 (3) ◽

pp. 1151-1159 ◽

Cited By ~ 9

Author(s):

Danielle Creek ◽

Laurent J Lamarque ◽

José M Torres-Ruiz ◽

Camille Parise ◽

Regis Burlett ◽

...

Keyword(s):

Water Stress ◽

Stomatal Closure ◽

Safety Margin ◽

Carbon Assimilation ◽

Xylem Embolism ◽

Growth And Survival ◽

Direct Observations ◽

Optical Visualization ◽

Embolism Resistance ◽

The One

Abstract Drought represents a major abiotic constraint to plant growth and survival. On the one hand, plants keep stomata open for efficient carbon assimilation while, on the other hand, they close them to prevent permanent hydraulic impairment from xylem embolism. The order of occurrence of these two processes (stomatal closure and the onset of leaf embolism) during plant dehydration has remained controversial, largely due to methodological limitations. However, the newly developed optical visualization method now allows concurrent monitoring of stomatal behaviour and leaf embolism formation in intact plants. We used this new approach directly by dehydrating intact saplings of three contrasting tree species and indirectly by conducting a literature survey across a greater range of plant taxa. Our results indicate that increasing water stress generates the onset of leaf embolism consistently after stomatal closure, and that the lag time between these processes (i.e. the safety margin) rises with increasing embolism resistance. This suggests that during water stress, embolism-mediated declines in leaf hydraulic conductivity are unlikely to act as a signal for stomatal down-regulation. Instead, these species converge towards a strategy of closing stomata early to prevent water loss and delay catastrophic xylem dysfunction.

Download Full-text

Differential drought resistance strategies of co-existing woodland species enduring the long rainless Eastern Mediterranean summer

Tree Physiology ◽

10.1093/treephys/tpz130 ◽

2019 ◽

Vol 40 (3) ◽

pp. 305-320 ◽

Cited By ~ 1

Author(s):

Päivi J Väänänen ◽

Yagil Osem ◽

Shabtai Cohen ◽

José M Grünzweig

Keyword(s):

Drought Resistance ◽

Tree Mortality ◽

Eastern Mediterranean ◽

Stomatal Closure ◽

Woody Species ◽

The Other ◽

Severe Drought ◽

Resistance Strategies ◽

Safety Margins ◽

Species Specific

Abstract In anticipation of a drier climate and to project future changes in forest dynamics, it is imperative to understand species-specific differences in drought resistance. The objectives of this study were to form a comprehensive understanding of the drought resistance strategies adopted by Eastern Mediterranean woodland species, and to elaborate specific ecophysiological traits that can explain the observed variation in survival among these species. We examined leaf water potential (𝛹), gas exchange and stem hydraulics during 2–3 years in mature individuals of the key woody species Phillyrea latifolia L., Pistacia lentiscus L. and Quercus calliprinos Webb that co-exist in a dry woodland experiencing ~ 6 rainless summer months. As compared with the other two similarly functioning species, Phillyrea displayed considerably lower 𝛹 (minimum 𝛹 of −8.7 MPa in Phillyrea vs −4.2 MPa in Pistacia and Quercus), lower 𝛹 at stomatal closure and lower leaf turgor loss point (𝛹TLP ), but reduced hydraulic vulnerability and wider safety margins. Notably, Phillyrea allowed 𝛹 to drop below 𝛹TLP under severe drought, whereas the other two species maintained positive turgor. These results indicate that Phillyrea adopted a more anisohydric drought resistance strategy, while Pistacia and Quercus exhibited a more isohydric strategy and probably relied on deeper water reserves. Unlike the two relatively isohydric species, Phillyrea reached complete stomatal closure at the end of the dry summer. Despite assessing a large number of physiological traits, none of them could be directly related to tree mortality. Higher mortality was observed for Quercus than for the other two species, which may result from higher water consumption due to its 2.5–10 times larger crown volume. The observed patterns suggest that similar levels of drought resistance in terms of survival can be achieved via different drought resistance strategies. Conversely, similar resistance strategies in terms of isohydricity can lead to different levels of vulnerability to extreme drought.

Download Full-text

Climatic limits of temperate rainforest tree species are explained by xylem embolism resistance among angiosperms but not among conifers

New Phytologist ◽

10.1111/nph.16448 ◽

2020 ◽

Vol 226 (3) ◽

pp. 727-740 ◽

Cited By ~ 1

Author(s):

Daniel C. Laughlin ◽

Sylvain Delzon ◽

Michael J. Clearwater ◽

Peter J. Bellingham ◽

Matthew S. McGlone ◽

...

Keyword(s):

Tree Species ◽

Xylem Embolism ◽

Temperate Rainforest ◽

Embolism Resistance

Download Full-text

Evolutionary relationships between drought-related traits and climate shape large hydraulic safety margins in western North American oaks

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2008987118 ◽

2021 ◽

Vol 118 (10) ◽

pp. e2008987118

Author(s):

Robert P. Skelton ◽

Leander D. L. Anderegg ◽

Jessica Diaz ◽

Matthew M. Kling ◽

Prahlad Papper ◽

...

Keyword(s):

North American ◽

Related Species ◽

Vascular System ◽

Xylem Embolism ◽

Closely Related Species ◽

Geographic Ranges ◽

Resistant Species ◽

Optical Visualization ◽

Safety Margins ◽

Dated Phylogeny

Quantitative knowledge of xylem physical tolerance limits to dehydration is essential to understanding plant drought tolerance but is lacking in many long-vessel angiosperms. We examine the hypothesis that a fundamental association between sustained xylem water transport and downstream tissue function should select for xylem that avoids embolism in long-vessel trees by quantifying xylem capacity to withstand air entry of western North American oaks (Quercus spp.). Optical visualization showed that 50% of embolism occurs at water potentials below −2.7 MPa in all 19 species, and −6.6 MPa in the most resistant species. By mapping the evolution of xylem vulnerability to embolism onto a fossil-dated phylogeny of the western North American oaks, we found large differences between clades (sections) while closely related species within each clade vary little in their capacity to withstand air entry. Phylogenetic conservatism in xylem physical tolerance, together with a significant correlation between species distributions along rainfall gradients and their dehydration tolerance, suggests that closely related species occupy similar climatic niches and that species' geographic ranges may have shifted along aridity gradients in accordance with their physical tolerance. Such trends, coupled with evolutionary associations between capacity to withstand xylem embolism and other hydraulic-related traits, yield wide margins of safety against embolism in oaks from diverse habitats. Evolved responses of the vascular system to aridity support the embolism avoidance hypothesis and reveal the importance of quantifying plant capacity to withstand xylem embolism for understanding function and biogeography of some of the Northern Hemisphere’s most ecologically and economically important plants.

Download Full-text

Interaction of stomatal behaviour and vulnerability to xylem cavitation determines the drought response of three temperate tree species

AoB Plants ◽

10.1093/aobpla/plz058 ◽

2019 ◽

Vol 11 (5) ◽

Cited By ~ 1

Author(s):

Zhicheng Chen ◽

Shirong Liu ◽

Haibo Lu ◽

Xianchong Wan

Keyword(s):

Water Potential ◽

Tree Species ◽

Stomatal Closure ◽

Safety Margin ◽

Xylem Cavitation ◽

Stomatal Behaviour ◽

Xylem Vulnerability ◽

Humid Region ◽

Rainfall Reduction ◽

Lindera Obtusiloba

Abstract How the mortality and growth of tree species vary with the iso-anisohydric continuum and xylem vulnerability is still being debated. We conducted a precipitation reduction experiment to create a mild drought condition in a forest in the Baotianman Mountains, China, a sub-humid region. Three main sub-canopy tree species in this region were examined. After rainfall reduction, Lindera obtusiloba showed severe dieback, but two other co-occurring species did not show dieback. The water potential at stomatal closure of Dendrobenthamia japonica, L. obtusiloba and Sorbus alnifolia was −1.70, −2.54 and −3.41 MPa, respectively, whereas the water potential at 88 % loss in hydraulic conductivity of the three species was −2.31, −2.11 and −7.01 MPa, respectively. Taken together, near-anisohydric L. obtusiloba with vulnerable xylem was highly susceptible to drought dieback. Anisohydric S. alnifolia had the most negative minimum water potential, and its xylem was the most resistant to cavitation. Isohydric D. japonica conserved water by rapidly closing its stomata. Ultimately, the hydraulic safety margin (HSM) of L. obtusiloba was the smallest among the three species, especially in precipitation-reduced plots. In terms of the stomatal safety margin (SSM), L. obtusiloba was negative, while S. alnifolia and D. japonica were positive. Of the two species without dieback, rainfall reduction decreased growth of D. japonica, but did not influence growth of S. Alnifolia; meanwhile, rainfall reduction led to a decrease of non-structural carbohydrates (NSCs) in D. japonica, but an increase in S. alnifolia. It is concluded that HSM as well as SSM allow interpreting the sensitivity of the three sub-canopy species to drought. The drought-induced dieback of L. obtusiloba is determined by the interaction of stomatal behaviour and xylem vulnerability, and the species could be sensitive to climate change-caused drought although still in sub-humid areas. The isohydric/anisohydric degree is associated with NSCs status and growth of plants.

Download Full-text

Drought response strategies and hydraulic traits contribute to mechanistic understanding of plant dry-down to hydraulic failure

Tree Physiology ◽

10.1093/treephys/tpz016 ◽

2019 ◽

Vol 39 (6) ◽

pp. 910-924 ◽

Cited By ~ 15

Author(s):

Chris J Blackman ◽

Danielle Creek ◽

Chelsea Maier ◽

Michael J Aspinwall ◽

John E Drake ◽

...

Keyword(s):

Drought Tolerance ◽

Tree Mortality ◽

Stomatal Closure ◽

Safety Margin ◽

Critical Levels ◽

Response Strategies ◽

Hydraulic Failure ◽

Dry Down ◽

Leaf Succulence ◽

And Function

Abstract Drought-induced tree mortality alters forest structure and function, yet our ability to predict when and how different species die during drought remains limited. Here, we explore how stomatal control and drought tolerance traits influence the duration of drought stress leading to critical levels of hydraulic failure. We examined the growth and physiological responses of four woody plant species (three angiosperms and one conifer) representing a range of water-use and drought tolerance traits over the course of two controlled drought–recovery cycles followed by an extended dry-down. At the end of the final dry-down phase, we measured changes in biomass ratios and leaf carbohydrates. During the first and second drought phases, plants of all species closed their stomata in response to decreasing water potential, but only the conifer species avoided water potentials associated with xylem embolism as a result of early stomatal closure relative to thresholds of hydraulic dysfunction. The time it took plants to reach critical levels of water stress during the final dry-down was similar among the angiosperms (ranging from 39 to 57 days to stemP88) and longer in the conifer (156 days to stemP50). Plant dry-down time was influenced by a number of factors including species stomatal-hydraulic safety margin (gsP90 – stemP50), as well as leaf succulence and minimum stomatal conductance. Leaf carbohydrate reserves (starch) were not depleted at the end of the final dry-down in any species, irrespective of the duration of drought. These findings highlight the need to consider multiple structural and functional traits when predicting the timing of hydraulic failure in plants.

Download Full-text

Large hydraulic safety margins protect Neotropical canopy rainforest tree species against hydraulic failure during drought

Annals of Forest Science ◽

10.1007/s13595-019-0905-0 ◽

2019 ◽

Vol 76 (4) ◽

Cited By ~ 7

Author(s):

Camille Ziegler ◽

Sabrina Coste ◽

Clément Stahl ◽

Sylvain Delzon ◽

Sébastien Levionnois ◽

...

Keyword(s):

Tree Species ◽

Turgor Loss Point ◽

Canopy Tree ◽

Hydraulic Failure ◽

Xylem Vulnerability ◽

Safety Margins ◽

Hydraulic Safety ◽

Dry Seasons ◽

Canopy Tree Species ◽

Embolism Resistance

Abstract Key message Abundant Neotropical canopy-tree species are more resistant to drought-induced branch embolism than what is currently admitted. Large hydraulic safety margins protect them from hydraulic failure under actual drought conditions. Context Xylem vulnerability to embolism, which is associated to survival under extreme drought conditions, is being increasingly studied in the tropics, but data on the risk of hydraulic failure for lowland Neotropical rainforest canopy-tree species, thought to be highly vulnerable, are lacking. Aims The purpose of this study was to gain more knowledge on species drought-resistance characteristics in branches and leaves and the risk of hydraulic failure of abundant rainforest canopy-tree species during the dry season. Methods We first assessed the range of branch xylem vulnerability to embolism using the flow-centrifuge technique on 1-m-long sun-exposed branches and evaluated hydraulic safety margins with leaf turgor loss point and midday water potential during normal- and severe-intensity dry seasons for a large set of Amazonian rainforest canopy-tree species. Results Tree species exhibited a broad range of embolism resistance, with the pressure threshold inducing 50% loss of branch hydraulic conductivity varying from − 1.86 to − 7.63 MPa. Conversely, we found low variability in leaf turgor loss point and dry season midday leaf water potential, and mostly large, positive hydraulic safety margins. Conclusions Rainforest canopy-tree species growing under elevated mean annual precipitation can have high resistance to embolism and are more resistant than what was previously thought. Thanks to early leaf turgor loss and high embolism resistance, most species have a low risk of hydraulic failure and are well able to withstand normal and even severe dry seasons.

Download Full-text

Is vulnerability segmentation at the leaf-stem transition a drought resistance mechanism? A theoretical test with a trait-based model for Neotropical canopy tree species

Annals of Forest Science ◽

10.1007/s13595-021-01094-9 ◽

2021 ◽

Vol 78 (4) ◽

Author(s):

Sébastien Levionnois ◽

Camille Ziegler ◽

Patrick Heuret ◽

Steven Jansen ◽

Clément Stahl ◽

...

Keyword(s):

Drought Resistance ◽

Tree Species ◽

Resistance Mechanism ◽

Severe Drought ◽

Xylem Embolism ◽

Empirical Measures ◽

Canopy Tree ◽

Neotropical Tree ◽

Canopy Tree Species ◽

Embolism Resistance

Abstract Key message Leaf-stem vulnerability segmentation predicts lower xylem embolism resistance in leaves than stem. However, although it has been intensively investigated these past decades, the extent to which vulnerability segmentation promotes drought resistance is not well understood. Based on a trait-based model, this study theoretically supports that vulnerability segmentation enhances shoot desiccation time across 18 Neotropical tree species. Context Leaf-stem vulnerability segmentation predicts lower xylem embolism resistance in leaves than stems thereby preserving expensive organs such as branches or the trunk. Although vulnerability segmentation has been intensively investigated these past decades to test its consistency across species, the extent to which vulnerability segmentation promotes drought resistance is not well understood. Aims We investigated the theoretical impact of the degree of vulnerability segmentation on shoot desiccation time estimated with a simple trait-based model. Methods We combined data from 18 tropical rainforest canopy tree species on embolism resistance of stem xylem (flow-centrifugation technique) and leaves (optical visualisation method). Measured water loss under minimum leaf and bark conductance, leaf and stem capacitance, and leaf-to-bark area ratio allowed us to calculate a theoretical shoot desiccation time (tcrit). Results Large degrees of vulnerability segmentation strongly enhanced the theoretical shoot desiccation time, suggesting vulnerability segmentation to be an efficient drought resistance mechanism for half of the studied species. The difference between leaf and bark area, rather than the minimum leaf and bark conductance, determined the drastic reduction of total transpiration by segmentation during severe drought. Conclusion Our study strongly suggests that vulnerability segmentation is an important drought resistance mechanism that should be better taken into account when investigating plant drought resistance and modelling vegetation. We discuss future directions for improving model assumptions with empirical measures, such as changes in total shoot transpiration after leaf xylem embolism.

Download Full-text

Bootstrap and Order Statistics for Quantifying Thermal-Hydraulic Code Uncertainties in the Estimation of Safety Margins

Science and Technology of Nuclear Installations ◽

10.1155/2008/340164 ◽

2008 ◽

Vol 2008 ◽

pp. 1-9 ◽

Cited By ~ 14

Author(s):

Enrico Zio ◽

Francesco Di Maio

Keyword(s):

Confidence Interval ◽

Order Statistics ◽

Nuclear Reactor ◽

Safety Margin ◽

Fuel Cladding ◽

Complete Group ◽

Bootstrap Technique ◽

Safety Margins ◽

Group Distribution

In the present work, the uncertainties affecting the safety margins estimated from thermal-hydraulic code calculations are captured quantitatively by resorting to the order statistics and the bootstrap technique. The proposed framework of analysis is applied to the estimation of the safety margin, with its confidence interval, of the maximum fuel cladding temperature reached during a complete group distribution blockage scenario in a RBMK-1500 nuclear reactor.

Download Full-text