The role of height-driven constraints and compensations on tree vulnerability to drought.

Frequent observations of higher mortality in larger trees than in smaller ones during droughts have sparked an increasing interest in size-dependent drought-induced mortality. However, the underlying physiological mechanisms are not well understood, with height-associated hydraulic constraints often being implied as the potential mechanism driving increased drought vulnerability. We performed a quantitative synthesis on how key traits that drive plant water and carbon economy change with tree height within species and assessed the implications that the different constraints and compensations may have on the interacting mechanisms (hydraulic failure, carbon starvation and/or biotic-agent attacks) affecting tree vulnerability to drought. While xylem tension increases with tree height, taller trees present a range of structural and functional adjustments, including more efficient water use and transport and greater water uptake and storage capacity, that mitigate the path-length-associated drop in water potential. These adaptations allow taller trees to withstand episodic water stress. Conclusive evidence for height-dependent increased vulnerability to hydraulic failure and carbon starvation, and their coupling to defence mechanisms and pest and pathogen dynamics, is still lacking. Further research is needed, particularly at the intraspecific level, to ascertain the specific conditions and thresholds above which height hinders tree survival under drought.

Cutting tree rings into time slices: how intra-annual dynamics of wood formation help decipher the space-for-time conversion.

Tree-ring anatomy, microdensity and isotope records provide valuable intra-annual information. However, extracting signals at that scale is challenged by the complexity of xylogenesis, where two major processes - cell enlargement and wall thickening - occur at different times and rates. We characterized the space-for-time association in the tree rings of three conifer species by examining the duration, overlapping, inter-tree synchronicity and interannual stability during cell enlargement and wall thickening across regular tree-ring sectors (portions of equal tangential width). The number of cells and cell differentiation rates determined the duration of sector formation, which augmented more rapidly throughout the ring for wall thickening than for enlargement. Increasing the number of sectors above c. 15 had a limited effect on improving time resolution because consecutive sector formation overlapped greatly in time, especially in narrow rings and during wall thickening. Increasing the number of sectors also resulted in lower synchronicity and stability of intermediate-sector enlargement, whereas all sectors showed high synchronicity and stability during wall thickening. Increasing the number of sectors had a stronger effect on enhancing time-series resolution for enlargement- than for wall-thickening-related traits, which would nevertheless produce more reliable intra-annual chronologies as a result of the more similar calendars across trees and years in wall thickening.

Water potential control of turgor-driven tracheid enlargement in Scots pine at its xeric distribution edge.

The extent to which water availability can be used to predict the enlargement and final dimensions of xylem conduits remains an open issue. We reconstructed the time course of tracheid enlargement in Pinus sylvestris trees in central Spain by repeated measurements of tracheid diameter on microcores sampled weekly during a 2 yr period. We analyzed the role of water availability in these dynamics empirically through time-series correlation analysis and mechanistically by building a model that simulates daily tracheid enlargement rate and duration based on Lockhart's equation and water potential as the sole input. Tracheid enlargement followed a sigmoid-like time course, which varied intra- and interannually. Our empirical analysis showed that final tracheid diameter was strongly related to water availability during tracheid enlargement. The mechanistic model was calibrated and successfully validated (R2  = 0.92) against the observed tracheid enlargement time course. The model was also able to reproduce the seasonal variations of tracheid enlargement rate, duration and final diameter (R2  = 0.84-0.99). Our results support the hypothesis that tracheid enlargement and final dimensions can be modeled based on the direct effect of water potential on turgor-driven cell expansion. We argue that such a mechanism is consistent with other reported patterns of tracheid dimension variation.

Geographical adaptation prevails over species-specific determinism in trees' vulnerability to climate change at Mediterranean rear-edge forests.

Climate change may reduce forest growth and increase forest mortality, which is connected to high carbon costs through reductions in gross primary production and net ecosystem exchange. Yet, the spatiotemporal patterns of vulnerability to both short-term extreme events and gradual environmental changes are quite uncertain across the species' limits of tolerance to dryness. Such information is fundamental for defining ecologically relevant upper limits of species tolerance to drought and, hence, to predict the risk of increased forest mortality and shifts in species composition. We investigate here to what extent the impact of short- and long-term environmental changes determines vulnerability to climate change of three evergreen conifers (Scots pine, silver fir, Norway spruce) and two deciduous hardwoods (European beech, sessile oak) tree species at their southernmost limits of distribution in the Mediterranean Basin. Finally, we simulated future forest growth under RCP 2.6 and 8.5 emission scenarios using a multispecies generalized linear mixed model. Our analysis provides four key insights into the patterns of species' vulnerability to climate change. First, site climatic marginality was significantly linked to the growth trends: increasing growth was related to less climatically limited sites. Second, estimated species-specific vulnerability did not match their a priori rank in drought tolerance: Scots pine and beech seem to be the most vulnerable species among those studied despite their contrasting physiologies. Third, adaptation to site conditions prevails over species-specific determinism in forest response to climate change. And fourth, regional differences in forests vulnerability to climate change across the Mediterranean Basin are linked to the influence of summer atmospheric circulation patterns, which are not correctly represented in global climate models. Thus, projections of forest performance should reconsider the traditional classification of tree species in functional types and critically evaluate the fine-scale limitations of the climate data generated by global climate models.

Divergent phenological and leaf gas exchange strategies of two competing tree species drive contrasting responses to drought at their altitudinal boundary.

In Mediterranean mountains, Pinus sylvestris L. is expected to be displaced under a warming climate by more drought-tolerant species such as the sub-Mediterranean Quercus pyrenaica Willd. Understanding how environmental factors drive tree physiology and phenology is, therefore, essential to assess the effect of changing climatic conditions on the performance of these species and, ultimately, their distribution. We compared the cambial and leaf phenology and leaf gas exchange of Q. pyrenaica and P. sylvestris at their altitudinal boundary in Central Spain and assessed the environmental variables involved. Results indicate that P. sylvestris cambial phenology was more sensitive to weather conditions (temperature at the onset and water deficit at the end of the growing season) than Q. pyrenaica. On the other hand, Q. pyrenaica cambial and leaf phenology were synchronized and driven by photoperiod and temperatures. Pinus sylvestris showed lower photosynthetic nitrogen-use efficiency and higher intrinsic water-use efficiency than Q. pyrenaica as a result of a tighter stomatal control in response to summer dry conditions, despite its less negative midday leaf water potentials. These phenological and leaf gas exchange responses evidence a stronger sensitivity to drought of P. sylvestris than that of Q. pyrenaica, which may therefore hold a competitive advantage over P. sylvestris under the predicted increase in recurrence and intensity of drought events. On the other hand, both species could benefit from warmer springs through an advanced phenology, although this effect could be limited in Q. pyrenaica if it maintains a photoperiod control over the onset of xylogenesis.

Xylem and Leaf Functional Adjustments to Drought in Pinus sylvestris and Quercus pyrenaica at Their Elevational Boundary.

Climatic scenarios for the Mediterranean region forecast increasing frequency and intensity of drought events. Consequently, a reduction in Pinus sylvestris L. distribution range is projected within the region, with this species being outcompeted at lower elevations by more drought-tolerant taxa such as Quercus pyrenaica Willd. The functional response of these species to the projected shifts in water availability will partially determine their performance and, thus, their competitive success under these changing climatic conditions. We studied how the cambial and leaf phenology and xylem anatomy of these two species responded to a 3-year rainfall exclusion experiment set at their elevational boundary in Central Spain. Additionally, P. sylvestris leaf gas exchange, water potential and carbon isotope content response to the treatment were measured. Likewise, we assessed inter-annual variability in the studied functional traits under control and rainfall exclusion conditions. Prolonged exposure to drier conditions did not affect the onset of xylogenesis in either of the studied species, whereas xylem formation ceased 1-3 weeks earlier in P. sylvestris. The rainfall exclusion had, however, no effect on leaf phenology on either species, which suggests that cambial phenology is more sensitive to drought than leaf phenology. P. sylvestris formed fewer, but larger tracheids under dry conditions and reduced the proportion of latewood in the tree ring. On the other hand, Q. pyrenaica did not suffer earlywood hydraulic diameter changes under rainfall exclusion, but experienced a cumulative reduction in latewood width, which could ultimately challenge its hydraulic performance. The phenological and anatomical response of the studied species to drought is consistent with a shift in resource allocation under drought stress from xylem to other sinks. Additionally, the tighter stomatal control and higher intrinsic water use efficiency observed in drought-stressed P. sylvestris may eventually limit carbon uptake in this species. Our results suggest that both species are potentially vulnerable to the forecasted increase in drought stress, although P. sylvestris might experience a higher risk of drought-induced decline at its low elevational limit.

Stand competition determines how different tree species will cope with a warming climate.

Plant-plant interactions influence how forests cope with climate and contribute to modulate species response to future climate scenarios. We analysed the functional relationships between growth, climate and competition for Pinus sylvestris, Quercus pyrenaica and Quercus faginea to investigate how stand competition modifies forest sensitivity to climate and simulated how annual growth rates of these species with different drought tolerance would change throughout the 21st century. Dendroecological data from stands subjected to thinning were modelled using a novel multiplicative nonlinear approach to overcome biases related to the general assumption of a linear relationship between covariates and to better mimic the biological relationships involved. Growth always decreased exponentially with increasing competition, which explained more growth variability than climate in Q. faginea and P. sylvestris. The effect of precipitation was asymptotic in all cases, while the relationship between growth and temperature reached an optimum after which growth declined with warmer temperatures. Our growth projections indicate that the less drought-tolerant P. sylvestris would be more negatively affected by climate change than the studied sub-Mediterranean oaks. Q. faginea and P. sylvestris mean growth would decrease under all the climate change scenarios assessed. However, P. sylvestris growth would decline regardless of the competition level, whereas this decrease would be offset by reduced competition in Q. faginea. Conversely, Q. pyrenaica growth would remain similar to current rates, except for the warmest scenario. Our models shed light on the nature of the species-specific interaction between climate and competition and yield important implications for management. Assuming that individual growth is directly related to tree performance, trees under low competition would better withstand the warmer conditions predicted under climate change scenarios but in a variable manner depending on the species. Thinning following an exponential rule may be desirable to ensure long-term conservation of high-density Mediterranean woodlands, particularly in drought-limited sites.