Fiber-parenchyma trade-off underlies changes in tropical forest structure and xylem architecture across a soil water gradient

Wood anatomical traits can underpin tropical forest structural and functional changes across soil water gradients and therefore could improve our mechanistic understanding of how plants adapt to environmental change. We assessed how the variation in the forest maximum height (Hmax), stem diameter, and wood density (WD) is associated with variation in xylem traits (area of fibers and parenchyma, conductive area [CondA, sum of all vessels lumens], vessel lumen area [VLA], vessel density [VD], and vessel wall reinforcement [VWR]) across 42 plots of a Brazilian Atlantic Forest habitat that span strong soil water gradients. We found that in wetter communities, greater height and lower WD were associated with greater parenchyma area (capacitance), and lower fibers, VD, VWR. Contrastingly, in drier communities, lower height was associated with higher fiber area (xylem reinforcement), WD, VD, and VWR, while parenchyma area and vessels are reduced. Tree communities vary from conservative resource-use and structurally dependent hydraulic safety (Fibers) to acquisitive resource-use and capacitance dependent hydraulic safety (parenchyma). Such a fiber-parenchyma trade-off (FPT) underlies the variation in tree height across a soil water gradient. Wood anatomy is fundamental to understanding and predicting the impacts of environmental change on forest structure.

Pit and tracheid anatomy explain the hydraulic safety- but not the hydraulic efficiency of 28 conifer species

Conifers face increased drought mortality risks because of drought-induced embolism in their vascular system. Variation in embolism resistance may result from species differences in pit structure and function, as pits control the air seeding between water transporting conduits. This study quantifies variation in embolism resistance and hydraulic conductivity for 28 conifer species grown in a 50-year-old common garden experiment and assesses the underlying mechanisms. Conifer species with a small pit aperture, high pit aperture resistance and large valve effect were more resistant to embolism, as they all may reduce air seeding. Surprisingly, hydraulic conductivity was only negatively correlated with tracheid cell wall thickness. Embolism resistance and its underlying pit traits related to pit size and sealing were stronger phylogenetically controlled than hydraulic conductivity and anatomical tracheid traits. Conifers differed in hydraulic safety and hydraulic efficiency, but there was no trade-off between safety and efficiency because they are driven by different xylem anatomical traits that are under different phylogenetic control.

Coordination between leaf biomechanical resistance and hydraulic safety across 30 subtropical woody species

Background and Aims Leaf biomechanical resistance protects leaves from biotic and abiotic damage. Previous studies have revealed that enhancing leaf biomechanical resistance is costly for plant species and leads to an increase in leaf drought tolerance. We thus predicted that there is a functional correlation between leaf hydraulic safety and biomechanical characteristics. Methods We measured leaf morphological and anatomical traits, pressure–volume parameters, maximum leaf hydraulic conductance (Kleaf-max), leaf water potential at 50% loss of hydraulic conductance (P50leaf), leaf hydraulic safety margin (SMleaf), and leaf force to tear (Ft) and punch (Fp) of 30 co-occurring woody species in a subtropical evergreen broadleaved forest. Linear regression analysis was performed to examine the relationships between biomechanical resistance and other leaf hydraulic traits. Key Results We found that higher Ft and Fp values were significantly associated with a lower (more negative) P50leaf and a larger SMleaf, thereby confirming the correlation between leaf biomechanical resistance and hydraulic safety. However, leaf biomechanical resistance showed no correlation with Kleaf-max, although it was significantly and negatively correlated with leaf outside-xylem hydraulic conductance. In addition, we also found that there was a significant correlation between biomechanical resistance and the modulus of elasticity by excluding an outlier. Conclusions The findings of this study reveal leaf biomechanical-hydraulic safety correlation in subtropical woody species.

Rapid hydraulic collapse as cause of drought-induced mortality in conifers

Understanding the vulnerability of trees to drought-induced mortality is key to predicting the fate of forests in a future climate with more frequent and intense droughts, although the underlying mechanisms are difficult to study in adult trees. Here, we explored the dynamic changes of water relations and limits of hydraulic function in dying adults of Norway spruce (Picea abies L.) during the progression of the record-breaking 2018 Central European drought. In trees on the trajectory to drought-induced mortality, we observed rapid, nonlinear declines of xylem pressure that commenced at the early onset of xylem cavitation and caused a complete loss of xylem hydraulic conductance within a very short time. We also observed severe depletions of nonstructural carbohydrates, though carbon starvation could be ruled out as the cause of the observed tree death, as both dying and surviving trees showed these metabolic limitations. Our observations provide striking field-based evidence for fast dehydration and hydraulic collapse as the cause of drought-induced mortality in adult Norway spruce. The nonlinear decline of tree water relations suggests that considering the temporal dynamics of dehydration is critical for predicting tree death. The collapse of the hydraulic system within a short time demonstrates that trees can rapidly be pushed out of the zone of hydraulic safety during the progression of a severe drought. In summary, our findings point toward a higher mortality risk for Norway spruce than previously assumed, which is in line with current reports of unprecedented levels of drought-induced mortality in this major European tree species.

Large scale assessment of post-drought climate sensitivity of tree-growth

<p>Hotter droughts will have an increasingly influential role in shaping forest ecosystems in the future. Risks include decreases in species richness, altered species distributions, forest dieback and changed function as carbon sink. A common method to study the impacts of droughts on forests is the quantification of reductions in biomass productivity via secondary growth – approximated by ring-width measurements –, including duration until growth rates return to pre-drought levels, so-called legacy periods. However, while these metrics are practical and relatively easy to measure, the underlying governing mechanisms are not, and thus poorly understood. Consequently, it is uncertain if drought-induced reductions in secondary growth are due to corresponding decreases in total physiological function or high plasticity, and if recovery times are due to lasting damage or adaptation with more carbon allocated to drought-mitigating structures.</p><p>The principle of the most limiting factor for tree-growth can be used to track temporal variations in climate-growth relationships. Similarly, the considerable strain hotter drought constitutes for tree-growth, and the need to repair damaged structures or alter carbon allocation, may imply temporary climate sensitivity deviations during legacy periods. Identifying their existence and quantifying subsequent differences in these deviations can help to shed light on strategies used by trees to respond to droughts.</p><p>Here, we detect and quantify deviations in climate-growth relationships during hotter drought legacy periods and assess how they differ according to clade (angiosperms – gymnosperms), site aridity and hydraulic safety margin. We do this by applying a linear mixed model on all ring-width indices (RWI) in the global-scale International Tree-Ring Data Bank (ITRDB) which exhibit a positive correlation with Standardized Precipitation-Evapotranspiration Index (SPEI). We apply a combined climatological and ecological definition for drought events and use site-dependent SPEI time-scales to allow for specific climate dependencies.</p><p>Results show heterogeneous post-drought climate sensitivity deviations, which are broadly categorized in three groups: 1) angiosperms growing in arid sites become increasingly sensitive to climate for 2 – 4 years; 2) angiosperms in mesic sites and or with high hydraulic safety margin show abrupt and complete disruption of the climate-growth relationship for the first year after droughts, which turn into a decrease in climate sensitivity for an additional 1 – 3 years; 3) gymnosperms in arid sites become less sensitive to climate for 2 – 4 years, although without the abrupt disruption seen in group 2. We discuss these results and their implications in an ecophysiological context, including future research avenues.</p><p>In conclusion, the results clearly show a functional legacy effect that is not detected through measurements of reductions in biomass accumulation alone, hinting at differential strategies employed by trees to cope with hotter droughts. This is a first step towards a better understanding of the mechanisms underlying hotter drought legacies which may help to improve ecosystem models and better predict how trees will respond to drought in a warming future climate.</p>

Mediterranean trees vulnerability to climate change will not be minimized through hydraulic safety traits adjustments.

<p><span>Climate change in the Mediterranean region leads to an intensification of summer droughts. These episodes of extreme water stress threaten the survival of tree species and, by the same token, would affect the structure and ecosystem services of woodlands. Indeed, in conditions of prolonged and intense drought, one of the major risks for trees is the hydraulic failure due to high embolism level. Xylem embolism risk depends essentially on various leaf and hydraulic traits including (i) the vulnerability of their xylem to cavitation, (ii) the turgor loss point (a surrogate for stomatal control) and (iii) their cuticular transpiration (gmin). The two former traits can be used to compute hydraulic safety margins (HSM). </span></p><p><span>In order to assess whether trees will survive future climatic conditions, it is necessary to quantify and assess the plasticity of these traits to intensified drought. In this study, we used three rainfall exclusion experiments established in mature forests in south-eastern France (Font-blanche, Puéchabon and O3HP experimental sites) to measure these traits and evaluate their ability to adjust to aggravated drought conditions for three Mediterranean widespread species: </span><span><em>Quercus ilex</em></span><span>, </span><span><em>Quercus Pubescens</em></span><span>, and </span><span><em>Pinus halepensis</em></span><span>. We performed pressure-volume curves of trees from rainfall exclusion and control plots to see if adjustments of gmin and leaf hydraulic traits involved in stomatal regulation occurred in these three species. Using the optical method and cavitron, we also quantified the plasticity of xylem vulnerability to cavitation by comparing the values of water potential leading to a 50% reduction in plant hydraulic conductance (P50). </span></p><p><span>Our results show that </span><span><em>Quercus pubescens</em></span><span> has the lowest HSM while </span><span><em>Quercus ilex</em></span><span> has the highest. In addition, gmin is higher for </span><span><em>Quercus pubescens</em></span><span> than for the other two species. All together these results suggest that </span><span><em>Quercus pubescens</em></span><span> is the most vulnerable to drought among the three studied. Globally, for most traits and species no significant difference was found between treatments. The only exception was for </span><span><em>Quercus ilex</em></span><span> that exhibited lower turgor loss point (Ψtlp) in the dry treatment. Drought acclimation for these species may rather depend on other traits, such as leaf area reduction or rooting depth. To integrate the role of these traits to estimate the historic and future mortality risk for these species, the use of hydraulic based models will be of interest. </span></p>

Leaf hydraulic safety margin and safety–efficiency trade-off across angiosperm woody species

Leaf hydraulic conductance and the vulnerability to water deficits have profound effects on plant distribution and mortality. In this study, we compiled a leaf hydraulic trait dataset with 311 species-at-site combinations from biomes worldwide. These traits included maximum leaf hydraulic conductance ( K leaf ), water potential at 50% loss of K leaf (P50 leaf ), and minimum leaf water potential ( Ψ min ). Leaf hydraulic safety margin (HSM leaf ) was calculated as the difference between Ψ min and P50 leaf . Our results indicated that 70% of the studied species had a narrow HSM leaf (less than 1 MPa), which was consistent with the global pattern of stem hydraulic safety margin. There was a positive relationship between HSM leaf and aridity index (the ratio of mean annual precipitation to potential evapotranspiration), as species from humid sites tended to have larger HSM leaf . We found a significant relationship between K leaf and P50 leaf across global angiosperm woody species and within each of the different plant groups. This global analysis of leaf hydraulic traits improves our understanding of plant hydraulic response to environmental change.