Catastrophic Hydraulic Failure and Tipping Points in Plants

Water inside plants forms a continuous chain from water in soils to the water evaporating from leaf surfaces. Failures in this chain result in reduced transpiration and photosynthesis and these failures are caused by soil drying and/or cavitation-induced xylem embolism. Xylem embolism and plant hydraulic failure share a number of analogies to “catastrophe theory” in dynamical systems. These catastrophes are often represented in the physiological and ecological literature as tipping points or alternative stable states when control variables exogenous (e.g. soil water potential) or endogenous (e.g. leaf water potential) to the plant are allowed to slowly vary. Here, plant hydraulics viewed from the perspective of catastrophes at multiple spatial scales is considered with attention to bubble expansion (i.e. cavitation), organ-scale vulnerability to embolism, and whole-plant biomass as a proxy for transpiration and hydraulic function. The hydraulic safety-efficiency tradeoff, hydraulic segmentation and maximum plant transpiration are examined using this framework. Underlying mechanisms for hydraulic failure at very fine scales such as pit membranes, intermediate scales such as xylem network properties and at larger scales such as soil-tree hydraulic pathways are discussed. Lacunarity areas in plant hydraulics are also flagged where progress is urgently needed.

The xylem of anisohydric Quercus alba L. is more vulnerable to embolism than isohydric co-dominants

The coordination of plant leaf water potential (Ψ) regulation and xylem vulnerability to embolism is fundamental for understanding the tradeoffs between carbon uptake and risk of hydraulic damage. There is a general consensus that trees with vulnerable xylem regulate Ψ more conservatively than plants with resistant xylem. We evaluated if this paradigm applied to three important eastern US temperate tree species, Quercus alba L., Acer saccharum Marsh., and Liriodendron tulipifera L., by synthesizing 1600 Ψ observations, 122 xylem embolism curves, and xylem anatomical measurements across ten forests spanning pronounced hydroclimatological gradients and ages. We found that, unexpectedly, the species with the most vulnerable xylem (Q. alba) regulated Ψ less strictly than the other species. This relationship was found across all sites, such that coordination among traits was largely unaffected by climate and stand age. Quercus species are perceived to be among the most drought tolerant temperate US forest species; however, our results suggest their relatively loose Ψ regulation in response to hydrologic stress occurs with a substantial hydraulic cost that may expose them to novel risks in a more drought-prone future. We end by discussing mechanisms that allow these species to tolerate and/or recover from hydraulic damage.

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

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.

Xylem embolism spread is largely prevented by interconduit pit membranes until the majority of conduits are gas-filled

Xylem embolism resistance varies across species influencing drought tolerance, yet little is known about the determinants of the embolism resistance of an individual conduit. Here we conducted an experiment using the optical vulnerability method to test whether individual conduits have a specific water potential threshold for embolism formation and whether pre-existing embolism in neighbouring conduits alters this threshold. Observations were made on a diverse sample of angiosperm and conifer species through a cycle of dehydration, rehydration and subsequent dehydration to death. Upon rehydration after the formation of embolism, no refilling was observed. When little pre-existing embolism was present, xylem conduits had a conserved, individual, embolism resistance threshold that varied across the population of conduits. The consequence of a variable conduit-specific embolism threshold is that a small degree of pre-existing embolism in the xylem results in an apparently more resistant xylem in a subsequent dehydration, particularly in angiosperms with vessels. While our results suggest that pit membranes separating xylem conduits are critical for maintaining a conserved individual embolism threshold for given conduit when little pre-exisiting embolism is present, as the percentage of embolized conduits increases, gas movement, local pressure differences, and connectivity between conduits increasingly contribute to embolism spread.

Acoustic Vulnerability, Hydraulic Capacitance, and Xylem Anatomy Determine Drought Response of Small Grain Cereals

Selection of high-yielding traits in cereal plants led to a continuous increase in productivity. However, less effort was made to select on adaptive traits, favorable in adverse and harsh environments. Under current climate change conditions and the knowledge that cereals are staple foods for people worldwide, it is highly important to shift focus to the selection of traits related to drought tolerance, and to evaluate new tools for efficient selection. Here, we explore the possibility to use vulnerability to drought-induced xylem embolism of wheat cultivars Excalibur and Hartog (Triticum aestivum L.), rye cultivar Duiker Max (Secale cereale L.), and triticale cultivars Dublet and US2014 (x Triticosecale Wittmack) as a proxy for their drought tolerance. Multiple techniques were combined to underpin this hypothesis. During bench-top dehydration experiments, acoustic emissions (AEs) produced by formation of air emboli were detected, and hydraulic capacitances quantified. By only looking at the AE50 values, one would classify wheat cultivar Excalibur as most tolerant and triticale cultivar Dublet as most vulnerable to drought-induced xylem embolism, though Dublet had significantly higher hydraulic capacitances, which are essential in terms of internal water storage to temporarily buffer or delay water shortage. In addition, xylem anatomical traits revealed that both cultivars have a contrasting trade-off between hydraulic safety and efficiency. This paper emphasizes the importance of including a cultivar’s hydraulic capacitance when evaluating its drought response and vulnerability to drought-induced xylem embolism, instead of relying on the AE50 as the one parameter.