Bernhard Schuldt

INTERVESSEL PIT MEMBRANE THICKNESS AS A KEY DETERMINANT OF EMBOLISM RESISTANCE IN ANGIOSPERM XYLEM

Pit membranes in bordered pits between neighbouring vessels play a major role in the entry of air-water menisci from an embolised vessel into a water-filled vessel (i.e., air-seeding). Here, we investigate intervessel pit membrane thickness (TPM) and embolism resistance (P50, i.e., the water potential corresponding to 50% loss of hydraulic conductivity) across a broad range of woody angiosperm species. Data on TPM and double intervessel wall thickness (TVW) were compiled based on electron and light microscopy. Fresh material that was directly fixated for transmission electron microscopy (TEM) was investigated for 71 species, while non-fresh samples were frozen, stored in alcohol, or air dried prior to TEM preparation for an additional 60 species. TPM and P50 were based on novel observations and literature. A strong correlation between TPM and P50 was found for measurements based on freshly fixated material (r = 0.78, P >0.01, n = 37), and between TPM and TVW (r = 0.79, P >0.01, n = 59), while a slightly weaker relationship occurred between TVW and P50 (r = 0.40, P >0.01, n = 34). However, non-fresh samples showed no correlation between TPM and P50, and between TPM and TVW. Intervessel pit membranes in non-fresh samples were c.28% thinner and more electron dense than fresh samples. Our findings demonstrate that TPM measured on freshly fixated material provides one of the strongest wood anatomical correlates of droughtinduced embolism resistance in angiosperms. Assuming that cellulose microfibrils show an equal spatial density, TPM is suggested to affect the length and the shape of intervessel pit membrane pores, but not the actual pore size. Moreover, the shrinking effect observed for TPM after dehydration and frost is associated with an increase in microfibril density and porosity, which may provide a functional explanation for embolism fatigue.

Changes in wood density, wood anatomy and hydraulic properties of the xylem along the root-to-shoot flow path in tropical rainforest trees

It is generally assumed that the largest vessels are occurring in the roots and that vessel diameters and the related hydraulic conductance in the xylem are decreasing acropetally from roots to leaves. With this study in five tree species of a perhumid tropical rainforest in Sulawesi (Indonesia), we searched for patterns in hydraulic architecture and axial conductivity along the flow path from small-diameter roots through strong roots and the trunk to distal sun-canopy twigs. Wood density differed by not more than 10% across the different flow path positions in a species, and branch and stem wood density were closely related in three of the five species. Other than wood density, the wood anatomical and xylem hydraulic traits varied in dependence on the position along the flow path, but were unrelated to wood density within a tree. In contrast to reports from conifers and certain dicotyledonous species, we found a hump-shaped variation in vessel diameter and sapwood area--specific conductivity along the flow path in all five species with a maximum in the trunk and strong roots and minima in both small roots and twigs; the vessel size depended on the diameter of the organ. This pattern might be an adaptation to the perhumid climate with a low risk of hydraulic failure. Despite a similar mean vessel diameter in small roots and twigs, the two distal organs, hydraulically weighted mean vessel diameters were on average 30% larger in small roots, resulting in ∼ 85% higher empirical and theoretical specific conductivities. Relative vessel lumen area in percent of sapwood area decreased linearly by 70% from roots to twigs, reflecting the increase in sclerenchymatic tissue and tracheids in acropetal direction in the xylem. Vessel size was more closely related to the organ diameter than to the distance along the root-to-shoot flow path. We conclude that (i) the five co-occurring tree species show convergent patterns in their hydraulic architecture despite different growth strategies, and (ii) the paradigm assuming continuous acropetal vessel tapering and decrease in specific conductance from fine roots towards distal twigs needs reconsideration.

A synthesis of tree functional traits related to drought‐induced mortality in forests across climatic zones

1. Forest dieback caused by drought-induced tree mortality has been observed world-wide. Forecasting which trees in which locations are vulnerable to drought-induced mortality is important to predict the consequences of drought on forest structure, biodiversity and ecosystem function. 2. In this paper, our central aim was to compile a synthesis of tree traits and associated abiotic variables that can be used to predict drought-induced mortality. We reviewed the literature that specifically links drought mortality to functional traits and site conditions (i.e. edaphic variables and biotic conditions), targeting studies that show clear use of tree traits in drought analysis. We separated the review into five climatic zones to determine global vs. regionally restricted relationships between traits and mortality. 3. Our synthesis identifies a number of traits that have clear relationships with drought-induced mortality (e.g. wood density at the species level and tree size and growth at the individual level). However, the lack of direct relationships between most traits and drought-induced mortality highlights areas where future research should focus to broaden our understanding. 5. Synthesis and applications. Our synthesis highlights established relationships between traits and drought-induced mortality, presents knowledge gaps for future research focus and suggests monitoring and research avenues for improving our understanding of drought-induced mortality. It is intended to assist ecologists and natural resource managers choose appropriate and measurable parameters for predicting local and regional scale tree mortality risk in different climatic zones within constraints of time and funding availability.

Intraspecific Variation in Wood Anatomical, Hydraulic, and Foliar Traits in Ten European Beech Provenances Differing in Growth Yield.

In angiosperms, many studies have described the inter-specific variability of hydraulic-related traits and little is known at the intra-specific level. This information is however mandatory to assess the adaptive capacities of tree populations in the context of increasing drought frequency and severity. Ten 20-year old European beech (Fagus sylvatica L.) provenances representing the entire distribution range throughout Europe and differing significantly in aboveground biomass increment (ABI) by a factor of up to four were investigated for branch wood anatomical, hydraulic, and foliar traits in a provenance trial located in Northern Europe. We quantified to which extend xylem hydraulic and leaf traits are under genetic control and tested whether the xylem hydraulic properties (hydraulic efficiency and safety) trades off with yield and wood anatomical and leaf traits. Our results showed that only three out of 22 investigated ecophysiological traits showed significant genetic differentiations between provenances, namely vessel density (VD), the xylem pressure causing 88% loss of hydraulic conductance and mean leaf size. Depending of the ecophysiological traits measured, genetic differentiation between populations explained 0–14% of total phenotypic variation, while intra-population variability was higher than inter-population variability. Most wood anatomical traits and some foliar traits were additionally related to the climate of provenance origin. The lumen to sapwood area ratio, vessel diameter, theoretical specific conductivity and theoretical leaf-specific conductivity as well as the C:N-ratio increased with climatic aridity at the place of origin while the carbon isotope signature (δ13C) decreased. Contrary to our assumption, none of the wood anatomical traits were related to embolism resistance but were strong determinants of hydraulic efficiency. Although ABI was associated with both VD and δ13C, both hydraulic efficiency and embolism resistance were unrelated, disproving the assumed trade-off between hydraulic efficiency and safety. European beech seems to compensate increasing water stress with growing size mainly by adjusting vessel number and not vessel diameter. In conclusion, European beech has a high potential capacity to cope with climate change due to the high degree of intra-population genetic variability.

Leaf gas exchange performance and the lethal water potential of five European species during drought

Establishing physiological thresholds to drought-induced mortality in a range of plant species is crucial in understanding how plants respond to severe drought. Here, five common European tree species were selected (Acer campestre L., Acer pseudoplatanus L., Carpinus betulus L., Corylus avellana L. and Fraxinus excelsior L.) to study their hydraulic thresholds to mortality. Photosynthetic parameters during desiccation and the recovery of leaf gas exchange after rewatering were measured. Stem vulnerability curves and leaf pressure-volume curves were investigated to understand the hydraulic coordination of stem and leaf tissue traits. Stem and root samples from well-watered and severely drought-stressed plants of two species were observed using transmission electron microscopy to visualize mortality of cambial cells. The lethal water potential (ψlethal) correlated with stem P99 (i.e., the xylem water potential at 99% loss of hydraulic conductivity, PLC). However, several plants that were stressed beyond the water potential at 100% PLC showed complete recovery during the next spring, which suggests that the ψlethal values were underestimated. Moreover, we observed a 1 : 1 relationship between the xylem water potential at the onset of embolism and stomatal closure, confirming hydraulic coordination between leaf and stem tissues. Finally, ultrastructural changes in the cytoplasm of cambium tissue and mortality of cambial cells are proposed to provide an alternative approach to investigate the point of no return associated with plant death.

Patterns in hydraulic architecture from roots to branches in six tropical tree species from cacao agroforestry and their relation to wood density and stem growth

For decades it has been assumed that the largest vessels are generally found in roots and that vessel size and corresponding sapwood area-specific hydraulic conductivity are acropetally decreasing toward the distal twigs. However, recent studies from the perhumid tropics revealed a hump-shaped vessel size distribution. Worldwide tropical perhumid forests are extensively replaced by agroforestry systems often using introduced species of various biogeographical and climatic origins. Nonetheless, it is unknown so far what kind of hydraulic architectural patterns are developed in those agroforestry tree species and which impact this exerts regarding important tree functional traits, such as stem growth, hydraulic efficiency and wood density (WD). We investigated wood anatomical and hydraulic properties of the root, stem and branch wood in Theobroma cacao and five common shade tree species in agroforestry systems on Sulawesi (Indonesia); three of these were strictly perhumid tree species, and the other three tree species are tolerating seasonal drought. The overall goal of our study was to relate these properties to stem growth and other tree functional traits such as foliar nitrogen content and sapwood to leaf area ratio. Our results confirmed a hump-shaped vessel size distribution in nearly all species. Drought-adapted species showed divergent patterns of hydraulic conductivity, vessel density, and relative vessel lumen area between root, stem and branch wood compared to wet forest species. Confirming findings from natural old-growth forests in the same region, WD showed no relationship to specific conductivity. Overall, aboveground growth performance was better predicted by specific hydraulic conductivity than by foliar traits and WD. Our study results suggest that future research on conceptual trade-offs of tree hydraulic architecture should consider biogeographical patterns underlining the importance of anatomical adaptation mechanisms to environment.

Species identity and neighbor size surpass the impact of tree species diversity on productivity in experimental broad-leaved tree sapling assemblages under dry and moist conditions.

Species diversity may increase the productivity of tree communities through complementarity (CE) and/or selection effects (SE), but it is not well known how this relationship changes under water limitation. We tested the stress-gradient hypothesis, which predicts that resource use complementarity and facilitation are more important under water-limited conditions. We conducted a growth experiment with saplings of five temperate broad-leaved tree species that were grown in assemblages of variable diversity (1, 3, or 5 species) and species composition under ample and limited water supply to examine effects of species richness and species identity on stand- and tree-level productivity. Special attention was paid to effects of neighbor identity on the growth of target trees in mixture as compared to growth in monoculture. Stand productivity was strongly influenced by species identity while a net biodiversity effect (NE) was significant in the moist treatment (mostly assignable to CE) but of minor importance. The growth performance of some of the species in the mixtures was affected by tree neighborhood characteristics with neighbor size likely being more important than neighbor species identity. Diversity and neighbor identity effects visible in the moist treatment mostly disappeared in the dry treatment, disproving the stress-gradient hypothesis. The mixtures were similarly sensitive to drought-induced growth reduction as the monocultures, which may relate to the decreased CE on growth upon drought in the mixtures.

Testing the plant pneumatic method to estimate xylem embolism resistance in stems of temperate trees

Abstract Methods to estimate xylem embolism resistance generally rely on hydraulic measurements, which can be far from straightforward. Recently, a pneumatic method based on air flow measurements of terminal branch ends was proposed to construct vulnerability curves by linking the amount of air extracted from a branch with the degree of embolism. We applied this novel technique for 10 temperate tree species, including six diffuse, two ring-porous and two gymnosperm species, and compared the pneumatic curves with hydraulic ones obtained from either the flow-centrifuge or the hydraulic-bench dehydration method. We found that the pneumatic method provides a good estimate of the degree of xylem embolism for all angiosperm species. The xylem pressure at 50% and 88% loss of hydraulic conductivity (i.e., Ψ50 and Ψ88) based on the methods applied showed a strongly significant correlation for all eight angiosperms. However, the pneumatic method showed significantly reduced Ψ50 values for the two conifers. Our findings suggest that the pneumatic method could provide a fast and accurate approach for angiosperms due to its convenience and feasibility, at least within the range of embolism resistances covered by our samples.

Monitoring global tree mortality patterns and trends. Report from the VW symposium 'Crossing scales and disciplines to identify global trends of tree mortality as indicators of forest health'

While global forest growth assessments have been carried out, no study has attempted to generate spatially explicit models of global tree mortality, which are necessary to generate a mechanistic understanding and to robustly quantify mortality at a global scale. The current initiative can build upon: (1)an increasing amount of data on forest ecosystems, including national forest inventories and monitoring, as well as an increasing number of research plot networks in all forested biomes; (2) a growing willingness of scientists and governmental agencies to openly share data; and (3) a greater availability of powerful tools for assessing and monitoring forests at broad spatial scales, such as remote-sensing products from satellites or airborne LIDAR. Despite this progress, current monitoring approaches are still incomplete in their spatial extent and data resolution is often inadequate for detecting scattered individual tree mortality and for identifying causal relationships between drivers of change in forest condition.

Acclimation of leaf water status and stem hydraulics to drought and tree neighbourhood: alternative strategies among the saplings of five temperate deciduous tree species

Adjustment in leaf water status parameters and modification in xylem structure and functioning can be important elements of a trees response to continued water limitation. In a growth trial with saplings of five co-occurring temperate broad-leaved tree species (genera Fraxinus, Acer, Carpinus, Tilia and Fagus) conducted in moist or dry soil, we compared the drought acclimation in several leaf water status and stem hydraulic parameters. Considering the extremes in the species responses, Fraxinus excelsior L. improved its leaf tissue hydration in the dry treatment through osmotic, elastic and apoplastic adjustment while Fagus sylvatica L. solely modified its xylem anatomy, which resulted in increased embolism resistance at the cost of hydraulic efficiency. Our results demonstrate the contrasting response strategies of coexisting tree species and how variable trait plasticity among species can be. The comparison of plants grown either in monoculture or in five-species mixture showed that the neighbouring species diversity can significantly influence a trees hydraulic architecture and leaf water status regulation. Droughted Carpinus betulus L. (and to a lesser extent, Acer pseudoplatanus L.) plants developed a more efficient stem hydraulic system in heterospecific neighbourhoods, while that of F. sylvatica was generally more efficient in conspecific than heterospecific neighbourhoods. We conclude that co-occurring tree species may develop a high diversity of drought-response strategies, and exploring the full diversity of trait characteristics requires synchronous study of acclimation at the leaf and stem (and possibly also the root) levels, and consideration of physiological as well as morphological and anatomical modifications.