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Xylem cavitation during drought is proposed as a major driver of canopy collapse, but the mechanistic link between hydraulic failure and leaf damage in trees is still uncertain. Here, we used the tree species manna gum (Eucalyptus viminalis) to explore the connection between xylem dysfunction and lethal desiccation in leaves. Cavitation damage to leaf xylem could theoretically trigger lethal desiccation of tissues by severing water supply under scenarios such as runaway xylem cavitation, or the local failure of terminal parts of the leaf vein network. To investigate the role of xylem failure in leaf death, we compared the timing of damage to the photosynthetic machinery (Fv/Fm decline) with changes in plant hydration and xylem cavitation during imposed water stress. The water potential at which Fv/Fm was observed to decline corresponded to the water potential marking a transition from slow to very rapid tissue dehydration. Both events also occurred simultaneously with the initiation of cavitation in leaf high-order veins (HOV, veins from the third order above) and the analytically derived point of leaf runaway hydraulic failure. The close synchrony between xylem dysfunction and the photosynthetic damage strongly points to water supply disruption as the trigger for desiccation of leaves in this hardy evergreen tree. These results indicate that runaway cavitation, possibly triggered by HOV network failure, is the tipping agent determining the vulnerability of E. viminalis leaves to damage during drought and suggest that HOV cavitation and runaway hydraulic failure may play a general role in determining canopy damage in plants.

12 págs.- 5 figuras.- referencias, Global warming is expected to dramatically accelerate forest mortality as temperature and drought intensity increase. Predicting the magnitude of this impact urgently requires an understanding of the process connecting atmospheric drying to plant tissue damage. Recent episodes of forest mortality worldwide have been widely attributed to dry conditions causing acute damage to plant vascular systems. Under this scenario vascular embolisms produced by water stress are thought to cause plant death, yet this hypothetical trajectory has never been empirically demonstrated. Here we provide foundational evidence connecting failure in the vascular network of leaves with tissue damage caused during water stress. We observe a catastrophic sequence initiated by water column breakage under tension in leaf veins which severs local leaf tissue water supply, immediately causing acute cellular dehydration and irreversible damage. By highlighting the primacy of vascular network failure in the death of leaves exposed to drought or evaporative stress our results provide a strong mechanistic foundation upon which models of plant damage in response to dehydration can be confidently structured., This study was supported by funds from the Australian Research Council (DP190101552) to TB; a visiting research fellowship from University of Tasmania (UTAS) to CRB; Individual Fellowship from the European Union’sHorizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement no. 751918 -AgroPHYS to CRD.

Plant invasive alien species (IAS) are a serious threat to biodiversity. Several studies have compared the functional features of IAS and native species to identify the functional traits, or set of traits, favouring the process of invasion. However, most of these studies analysed traits only related to carbon and nutrients, and the inclusion of traits related to water use and acquisition might be useful to describe the functions underlying plant invasion. Here we present an analysis of cost-related, hydraulic and leaf vein traits measured on a large assemblage of woody and herbaceous native and invasive species (93 species in total, 78 natives and 15 IAS), that co-occur in site types in the Mediterranean area with different water availability (i.e. xeric, mesic and hydric sites). IAS shared lower leaf construction costs and drought resistance, but potential higher efficiency in water transport (i.e. higher values of vein length per unit area/mass) than native species. Moreover, IAS and native species separated along the trade-offs drawn by the measured traits, suggesting that hydraulic and vein traits could set an important axis of variation between IAS and native species. At last, IAS tended to occupy the fast-growth region of the functional space, independently of growth form and site type. Hydraulic and vein traits provide stronger mechanistic linkages between construction costs and photosynthetic and growth rates, thus possibly playing a central role in determining the invasive potential of IAS. IAS could reduce costs associated with leaf construction and resistance to drought stress having, at the same time, high efficiency of water transport and photosynthetic rates by developing a denser venation network, translating to higher growth rates than native and more conservative species.

Invasion of natural habitats by alien trees is a threat to forest conservation. Our understanding of fundamental ecophysiological mechanisms promoting plant invasions is still limited, and hydraulic and water relation traits have been only seldom included in studies comparing native and invasive trees. We compared several leaf and wood functional and mechanistic traits in co-occurring Ailanthus altissima (Mill.) Swingle (Aa) and Fraxinus ornus L. (Fo). Aa is one of the most invasive woody species in Europe and North America, currently outcompeting several native trees including Fo. We aimed at quantifying inter-specific differences in terms of: (i) performance in resource use and acquisition; (ii) hydraulic efficiency and safety; (iii) carbon costs associated to leaf and wood construction; and (iv) plasticity of functional and mechanistic traits in response to light availability. Traits related to leaf and wood construction and drought resistance significantly differed between the two species. Fo sustained higher structural costs than Aa, but was more resistant to drought. The lower resistance to drought stress of Aa was counterbalanced by higher water transport efficiency, but possibly required mechanisms of resilience to drought-induced hydraulic damage. Larger phenotypic plasticity of Aa in response to light availability could also promote the invasive potential of the species.

Novel features related to turgor loss adjustment and higher ability to modulate leaf-construction costs could improve A. altissima fitness in its invaded range. Phenotypic plasticity has been recently proposed to play an important role in invasion process. More precisely, phenotypic plasticity of alien invasive species could be higher in their exotic rather than native habitat, probably because of the release from biotic or abiotic constraints. In this paper, several plant functional traits were analysed on Ailanthus altissima (Mill.) Swingle, a highly invasive species in Europe, aiming at providing a comparison among key functional traits measured on individuals growing in their native habitat and to test if values of functional traits and their related plasticity are higher in exotic habitats. Our analysis pinpointed that variability of functional traits in the native habitat was mainly driven by different irradiance, temperature and evaporative demand of the studied sites, in accordance to the traits trade-offs in the Leaf Economic Spectrum. Physiological traits related to drought tolerance were different between native and exotic habitats. In the native one, A. altissima relied on osmoregulation processes to adjust leaf turgor loss point (Ψtlp), as the osmotic potential at full turgor (π0) were lower in drier sites. In the exotic habitat, individuals in drier sites had similar π0 but lower wall elasticity (e), suggesting that leaves had thinner cell walls. Moreover, plasticity in specific leaf area and e were higher in the exotic habitat. The novel features related to Ψtlp adjustment and the higher plasticity in traits related to leaf-construction costs could increase A. altissima fitness in response to different environmental conditions in its invasive range.