Sylvain Delzon

Global convergence in the vulnerability of forests to drought.

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 Here we draw together published and unpublished data on the vulnerability of the transport system to drought-induced embolism for a large number of woody species, with a view to examining the likely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 (<1 megapascal) 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.

Climate change and European forests: What do we know, what are the uncertainties, and what are the implications for forest management?

The knowledge about potential climate change impacts on forests is continuously expanding and some changes in growth, drought induced mortality and species distribution have been observed. However despite a significant body of research, a knowledge and communication gap exists between scientists and non-scientists as to how climate change impact scenarios can be interpreted and what they imply for European forests. It is still challenging to advise forest decision makers on how best to plan for climate change as many uncertainties and unknowns remain and it is difficult to communicate these to practitioners and other decision makers while retaining emphasis on the importance of planning for adaptation. In this paper, recent developments in climate change observations and projections, observed and projected impacts on European forests and the associated uncertainties are reviewed and synthesised with a view to understanding the implications for forest management. Current impact assessments with simulation models contain several simplifications, which explain the discrepancy between results of many simulation studies and the rapidly increasing body of evidence about already observed changes in forest productivity and species distribution. In simulation models uncertainties tend to cascade onto one another; from estimating what future societies will be like and general circulation models (GCMs) at the global level, down to forest models and forest management at the local level. Individual climate change impact studies should not be uncritically used for decision-making without reflection on possible shortcomings in system understanding, model accuracy and other assumptions made. It is important for decision makers in forest management to realise that they have to take long-lasting management decisions while uncertainty about climate change impacts are still large. We discuss how to communicate about uncertainty - which is imperative for decision making - without diluting the overall message. Considering the range of possible trends and uncertainties in adaptive forest management requires expert knowledge and enhanced efforts for providing science-based decision support.

Xylem function and growth rate interact to determine recovery rates after exposure to extreme water deficit

• Motivated by the urgent need to understand how water stress-induced embolism limits the survival and recovery of plants during drought, the linkage between water-stress tolerance and xylem cavitation resistance was examined in one of the worlds most drought resistant conifer genera, Callitris. • Four species were subjected to drought treatments of -5, -8 and -10 MPa for a period of 3-4 wk, after which plants were rewatered. Transpiration, basal growth and leaf water potential were monitored during and after drought. • Lethal water potential was correlated with the tension producing a 50% loss of stem hydraulic conductivity. The most resilient species suffered minimal embolism and recovered gas exchange within days of rewatering from -10 MPa, while the most sensitive species suffered major embolism and recovered very slowly. The rate of repair of water transport in the latter case was equal to the rate of basal area growth, indicating xylem reiteration as the primary means of hydraulic repair. • The survival of, and recovery from, water stress in Callitris are accurately predicted by the physiology of the stem water-transport system. As the only apparent means of xylem repair after embolism, basal area growth is a critical part of this equation.

Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees.

Hydraulic failure is one of the main causes of tree mortality in conditions of severe drought. Resistance to cavitation is known to be strongly related to drought tolerance and species survival in conifers, but the threshold of water-stress-induced embolism leading to catastrophic xylem dysfunction in angiosperms has been little studied. We investigated the link between drought tolerance, survival and xylem cavitation resistance in five angiosperm tree species known to have contrasting desiccation resistance thresholds. We exposed seedlings in a greenhouse to severe drought to generate extreme water stress. We monitored leaf water potential, total plant water loss rate, leaf transpiration, stomatal conductance and CO2 assimilation rate during drought exposure and after rewatering (recovery phase). The time required for the recovery of 50% of the maximum value of a given ecophysiological variable after rewatering was used to determine the critical water potential corresponding to the threshold beyond which the plant failed to recover. We also investigated the relationship between this potential and stem xylem cavitation resistance, as assessed from vulnerability curves. This minimum recoverable water potential was consistent between ecophysiological variables and varied considerably between species, from -3.4 to -6.0 MPa. This minimum recoverable water potential was strongly correlated with P50 and P88, the pressures inducing 50 and 88% losses of stem hydraulic conductance, respectively. Moreover, the embolism threshold leading to irreversible drought damage was found to be close to 88%, rather than the 50% previously reported for conifers. Hydraulic failure leading to irreversible drought-induced global dysfunction in angiosperm tree species occurred at a very high level of xylem embolism, possibly reflecting the physiological characteristics of their stem water-transport system.

Altitudinal differentiation in growth and phenology among populations of temperate-zone tree species growing in a common garden

The aim of the study was to determine whether there are genetic variations in growth and leaf phenology (flushing and senescence) among populations of six woody species (Abies alba Mill., Acer pseudoplatanus L., Fagus sylvatica L., Fraxinus excelsior L., Ilex aquifolium L., and Quercus petraea (Matt.) Liebl.) along altitudinal gradients, using a common-garden experiment. We found (i) significant differences in phenology and growth among provenances for most species and (ii) evidence that these among-population differences in phenology were related to the annual temperature at the provenance sites for ash, beech, and oak. It is noteworthy that along the same climatic gradient, species can exhibit opposing genetic clines: beech populations from high elevations flushed earlier than those from low elevations, whereas we observed the opposite trend for ash and oak. For most species, significant altitudinal clines for growth were also revealed. Finally, we highlighted the fact that both phenology timing and gro...

Mechanism of water-stress induced cavitation in conifers: bordered pit structure and function support the hypothesis of seal capillary-seeding.

Resistance to water-stress induced cavitation is an important indicator of drought tolerance in woody species and is known to be intimately linked to the anatomy of the xylem. However, the actual mechanical properties of the pit membrane are not well known and the exact mode of air-seeding by which cavitation occurs is still uncertain. We examined the relationship between cavitation resistance and bordered pit structure and function in 40 coniferous species. Xylem pressure inducing 50% loss of hydraulic conductance (P50, a proxy for cavitation resistance) varied widely among species, from −2.9 to −11.3 MPa. The valve effect of the pit membrane, measured as a function of margo flexibility and torus overlap, explained more variation in cavitation-resistance than simple anatomical traits such as pit membrane, pit aperture or torus size. Highly cavitation resistant species exhibited both a high flexibility of the margo and a large overlap between the torus and the pit aperture, allowing the torus to tightly seal the pit aperture. Our results support the hypothesis of seal capillary-seeding as the most likely mode of air-seeding, and suggest that the adhesion of the torus to the pit border may be the main determinant of cavitation resistance in conifers.

Tree invasions: a comparative test of the dominant hypotheses and functional traits

Trees act as ecosystem engineers and invasions by exotic tree species profoundly impact recipient communities. Recently, research on invasive trees has dramatically increased, enabling the assessment of general trends in tree invasion. Analysing 90 studies dealing with 45 invasive tree species, we conducted a quantitative review and a meta-analysis to estimate the relevance of eight leading hypotheses for explaining tree invasions. We also tested whether species functional traits (growth rate, density/cover, germination, biomass and survival) equally promote tree invasiveness. Overall, our results suggest that several hypotheses, linked to invasibility or invasiveness, are pertinent to explain tree invasions. Furthermore, more than one hypothesis has been supported for a given species, which indicates that multiple factors lead to the success of invasive tree species. In addition, growth rate appears to be the most efficient predictor of invasiveness for invasive trees and could thus be used as a means to identify potential alien tree invasions. We conclude that further investigations are needed to test the consistency of some hypotheses across a broader pool of invasive tree species, whilst experimental studies with the same tree species across a larger range of sites would help to reveal the full suite of factors that affect tree invasions.

Uniform selection as a primary force reducing population genetic differentiation of cavitation resistance across a species range.

Background Cavitation resistance to water stress-induced embolism determines plant survival during drought. This adaptive trait has been described as highly variable in a wide range of tree species, but little is known about the extent of genetic and phenotypic variability within species. This information is essential to our understanding of the evolutionary forces that have shaped this trait, and for evaluation of its inclusion in breeding programs. Methodology We assessed cavitation resistance (P 50), growth and carbon isotope composition in six Pinus pinaster populations in a provenance and progeny trial. We estimated the heritability of cavitation resistance and compared the distribution of neutral markers (F ST) and quantitative genetic differentiation (Q ST), for retrospective identification of the evolutionary forces acting on these traits. Results/Discussion In contrast to growth and carbon isotope composition, no population differentiation was found for cavitation resistance. Heritability was higher than for the other traits, with a low additive genetic variance (h2 ns = 0.43±0.18, CVA = 4.4%). Q ST was significantly lower than F ST, indicating uniform selection for P 50, rather than genetic drift. Putative mechanisms underlying QST

Recent advances in tree hydraulics highlight the ecological significance of the hydraulic safety margin

Drought-induced cavitation resistance varies considerably between tree species and forest ecosystems (Maherali et al., 2004; Delzon et al., 2010) and is closely linked to survival under severe drought in both conifers (Brodribb & Cochard, 2009; Brodribb et al., 2010) and angiosperms (Kursar et al., 2009; Anderegg et al., 2012; Barigah et al., 2013; Urli et al., 2013). Choat et al. (2012) recently reported that most trees operate very close to their threshold of cavitation, leaving them potentially vulnerable to drought-induced mortality in a warmer/drier world (Engelbrecht, 2012). Indeed, species growing in dry environments are more resistant to droughtinduced cavitation (more negative water potential at 50% cavitation, P50) but experience a more negative minimumwater potential (Pmin) than those growing in wet environments. The so-called hydraulic safety margin, the difference between the level of water stress experienced by a species in the field (Pmin) and the level of water stress leading to hydraulic failure, is, therefore, remarkably narrow, whatever the forest species and biome considered (Choat et al., 2012). This pattern provides clues to the global droughtinduced mortality currently observed, even in very wet environments, such as tropical forests (Allen et al., 2010). Klein et al. (2014) play down the functional significance of the hydraulic safety margin in the vulnerability of forests to drought, pointing out the important role played by additional mechanisms, such as the ability of trees to repair embolism. While it is obvious that drought-induced forest dieback is a complex process involving a number of biotic and abiotic factors, we would like to draw the attention of scientists to the state of evidence for embolism repair, thereby guiding research on tree drought resistance into the most relevant and fruitful directions

To what extent is altitudinal variation of functional traits driven by genetic adaptation in European oak and beech

The phenotypic responses of functional traits in natural populations are driven by genetic diversity and phenotypic plasticity. These two mechanisms enable trees to cope with rapid climate change. We studied two European temperate tree species (sessile oak and European beech), focusing on (i) in situ variations of leaf functional traits (morphological and physiological) along two altitudinal gradients and (ii) the extent to which these variations were under environmental and/or genetic control using a common garden experiment. For all traits, altitudinal trends tended to be highly consistent between species and transects. For both species, leaf mass per area displayed a positive linear correlation with altitude, whereas leaf size was negatively correlated with altitude. We also observed a significant increase in leaf physiological performance with increasing altitude: populations at high altitudes had higher maximum rates of assimilation, stomatal conductance and leaf nitrogen content than those at low altitudes. In the common garden experiment, genetic differentiation between populations accounted for 0-28% of total phenotypic variation. However, only two traits (leaf mass per area and nitrogen content) exhibited a significant cline. The combination of in situ and common garden experiments used here made it possible to demonstrate, for both species, a weaker effect of genetic variation than of variations in natural conditions, suggesting a strong effect of the environment on leaf functional traits. Finally, we demonstrated that intrapopulation variability was systematically higher than interpopulation variability, whatever the functional trait considered, indicating a high potential capacity to adapt to climate change.