Shifts in rainfall patterns and increasing temperatures associated with climate change are likely to cause widespread forest decline in regions where droughts are predicted to increase in duration and severity. One primary cause of productivity loss and plant mortality during drought is hydraulic failure. Drought stress creates trapped gas emboli in the water transport system, which reduces the ability of plants to supply water to leaves for photosynthetic gas exchange and can ultimately result in desiccation and mortality. At present we lack a clear picture of how thresholds to hydraulic failure vary across a broad range of species and environments, despite many individual experiments. Here we draw together published and unpublished data on the vulnerability of the transport system to drought-induced embolism for a large number of woody species, with a view to examining the likely consequences of climate change for forest biomes. We show that 70% of 226 forest species from 81 sites worldwide operate with narrow hydraulic safety margins against injurious levels of drought stress and therefore potentially face long-term reductions in productivity and survival if temperature and aridity increase as predicted for many regions across the globe. Safety margins are largely independent of mean annual precipitation, showing that there is global convergence in the vulnerability of forests to drought, with all forest biomes equally vulnerable to hydraulic failure regardless of their current rainfall environment. These findings provide insight into why drought-induced forest decline is occurring not only in arid regions but also in wet forests not normally considered at drought risk

SummaryThe evolution of lignified xylem allowed for the efficient transport of water under tension, but also exposed the vascular network to the risk of gas emboli and the spread of gas between xylem conduits, thus impeding sap transport to the leaves. A well-known hypothesis proposes that the safety of xylem (its ability to resist embolism formation and spread) should trade off against xylem efficiency (its capacity to transport water).We tested this safety-efficiency hypothesis in branch xylem across 335 angiosperm and 89 gymnosperm species. Safety was considered at three levels: the xylem water potentials where 12%, 50% and 88% of maximal conductivity are lost.Although correlations between safety and efficiency were weak (r 2 < 0.086), no species had high efficiency and high safety, supporting the idea for a safety-efficiency tradeoff. However, many species had low efficiency and low safety. Species with low efficiency and low safety were weakly associated (r 2 < 0.02 in most cases) with higher wood density, lower leaf-to sapwood-area and shorter stature. There appears to be no persuasive explanation for the considerable number of species with both low efficiency and low safety. These species represent a real challenge for understanding the evolution of xylem.

Tree mortality is a key factor influencing forest functions and dynamics, but our understanding of the mechanisms leading to mortality and the associated changes in tree growth rates are still limited. We compiled a new pan-continental tree-ring width database from sites where both dead and living trees were sampled (2970 dead and 4224 living trees from 190 sites, including 36 species), and compared early and recent growth rates between trees that died and those that survived a given mortality event. We observed a decrease in radial growth before death in ca. 84% of the mortality events. The extent and duration of these reductions were highly variable (1-100 years in 96% of events) due to the complex interactions among study species and the source(s) of mortality. Strong and long-lasting declines were found for gymnosperms, shade- and drought-tolerant species, and trees that died from competition. Angiosperms and trees that died due to biotic attacks (especially bark-beetles) typically showed relatively small and short-term growth reductions. Our analysis did not highlight any universal trade-off between early growth and tree longevity within a species, although this result may also reflect high variability in sampling design among sites. The intersite and interspecific variability in growth patterns before mortality provides valuable information on the nature of the mortality process, which is consistent with our understanding of the physiological mechanisms leading to mortality. Abrupt changes in growth immediately before death can be associated with generalized hydraulic failure and/or bark-beetle attack, while long-term decrease in growth may be associated with a gradual decline in hydraulic performance coupled with depletion in carbon reserves. Our results imply that growth-based mortality algorithms may be a powerful tool for predicting gymnosperm mortality induced by chronic stress, but not necessarily so for angiosperms and in case of intense drought or bark-beetle outbreaks.

Wall reinforcement in xylem conduits is thought to prevent wall implosion by negative pressures, but direct observations of xylem geometry during water stress are still largely lacking. In this study, we have analyzed the changes in xylem geometry during water stress in needles of four pine species (Pinus spp.). Dehydrated needles were frozen with liquid nitrogen, and xylem cross sections were observed, still frozen, with a cryo-scanning electron microscope and an epifluorescent microscope. Decrease in xylem pressure during drought provoked a progressive collapse of tracheids below a specific threshold pressure (P collapse ) that correlates with the onset of cavitation in the stems. P collapse was more negative for species with smaller tracheid diameter and thicker walls, suggesting a tradeoff between xylem efficiency, xylem vulnerability to collapse, and the cost of wall stiffening. Upon severe dehydration, tracheid walls were completely collapsed, but lumens still appeared filled with sap. When dehydration proceeded further, tracheids embolized and walls relaxed. Wall collapse in dehydrated needles was rapidly reversed upon rehydration. We discuss the implications of this novel hydraulic trait on the xylem function and on the understanding of pine water relations.In vascular plants, xylem sap is transported under negative pressure in lignified conduits (Pockman et al., 1995). From a physical point of view, such a transport is constrained by two major limitations: (a) a risk of collapse of the water columns; and (b) a risk of collapse of the conduit walls. The first constraint originates from the metastable state of water under negative pressures. Under such conditions, vapor nucleation can occur, disrupting the water columns in the xylem and therefore the sap flow. This phenomenon is referred to the risk of cavitation. The second physical limitation, wall collapse, is due to the centripetal forces exerted on conduit walls that may implode if wall mechanical reinforcement is deficient.Over the past decades, the risk of xylem cavitation in upper plants has received considerable attention. Significant advances were obtained after techniques for detecting cavitation events acoustically (Milburn, 1966;Tyree and Dixon, 1983) or hydraulically were introduced. These techniques confirmed that xylem transport can remarkably operate under large negative pressures for prolonged periods. Cavitation occurs when plants are exposed to severe drought and pressures exceed species-specific thresholds. These thresholds are determined by the structure of pit membranes in the xylem wall because cavitation is thought to be caused by the aspiration of an air bubble through these membranes (Zimmermann, 1983;. In the recent literature, results obtained with new techniques have suggested that the risk of xylem cavitation was much more pronounced than previously thought (Zimmermann et al., 1994; Canny, 1995). However, more recent studies (Wei et al., 1999; Cochard et al., 2000) have demonstrated that cavitation was overestimated in th...

Xylem embolism is a limiting factor for woody species worldwide. Conifers at the alpine timberline are exposed to drought and freeze-thaw stress during winter, which induce potentially lethal embolism. Previous studies indicated that timberline trees survive by xylem refilling. In this study on Picea abies, refilling was monitored during winter and spring seasons and analyzed in the laboratory and in situ experiments, based on hydraulic, anatomical, and histochemical methods. Refilling started in late winter, when the soil was frozen and soil water not available for the trees. Xylem embolism caused up to 86.2% ± 3.1% loss of conductivity and was correlated with the ratio of closed pits. Refilling of xylem as well as recovery in shoot conductance started in February and corresponded with starch accumulation in secondary phloem and in the mesophyll of needles, where we also observed increasing aquaporin densities in the phloem and endodermis. This indicates that active, cellular processes play a role for refilling even under winter conditions. As demonstrated by our experiments, water for refilling was thereby taken up via the branches, likely by foliar water uptake. Our results suggest that refilling is based on water shifts to embolized tracheids via intact xylem, phloem, and parenchyma, whereby aquaporins reduce resistances along the symplastic pathway and aspirated pits facilitate isolation of refilling tracheids. Refilling must be taken into account as a key process in plant hydraulics and in estimating future effects of climate change on forests and alpine tree ecosystems.