Drivers of drought-related physiological, morphological and anatomical trait expression in a temperate eucalypt

Abstract

Increasing drought-induced tree mortality is a global problem and current scientific efforts aim to understand why and how trees succumb to drought. Nevertheless, our current understanding of the mechanisms leading to drought-induced tree mortality is limited. Functional traits have emerged as useful indicators of drought susceptibility, but little research explores their underlying drivers. Traits expression can be under strong genetic control or phenotypically plastic. While traits under strong genetic control can only adapt through new generations, phenotypic plasticity facilitates adjustment within the lifetime of a tree which will be essential under rapid climate change. Hence, the ability to phenotypically adjust to drought is an important factor influencing drought resistance and therefore survival. However, differences in population genetics or phenotypic plasticity can result in diverse trait expressions even within a species. Hence, drought resistance may differ, even among populations of the same species. Furthermore, observations on drought mortality indicate that drought resistance likely differs between different developmental stages. However, we currently lack insights on how drought resistance in trees changes with developmental stage, which limits our understanding of species vulnerability under climate change. Therefore, this thesis analyses the expression of drought-related traits to determine which traits are phenotypically plastic as opposed to being under strong genetic control. To investigate phenotypic plasticity in detail, I conducted a set of experiments with different drought intensities and durations. These studies were performed on trees at different stages of development (i.e., seedlings, saplings, and mature trees) to also investigate how trait expression changes as trees develop. Eucalyptus obliqua L.Hér. was selected as the study species due to its ecological importance and wide distribution in south-eastern Australia, increasing the likelihood of trait plasticity.

Two experimental chapters of my thesis (Chapter II & IV) were conducted in young (~15 y.o.) E. obliqua forest stands in south-eastern Australia. The first study aimed to investigate whether key drought-related traits are phenotypically plastic or under strong genetic control for E. obliqua populations growing across a precipitation gradient (Chapter II). Phenotypic plasticity was investigated by measuring the drought-related trait expression in five E. obliqua populations once during the summer and winter seasons. Further, seeds were collected at the five sites and seedlings were grown under uniform conditions to assess which traits are under strong genetic control. In the field, drier populations had smaller leaves with thicker xylem vessel walls, a lower vulnerability to embolism and a lower water potential at turgor loss point, which likely confers greater hydraulic safety. Significant phenotypic adjustments in physiological and morphological traits were observed in all E. obliqua populations. The Huber Value (sapwood to leaf area ratio; HV) increased during dry summer conditions while the water potential at turgor loss point decreased, likely to increase the populations’ hydraulic safety in the short-term. Under uniform conditions, seedlings from dry-origin populations express smaller leaves, higher anatomical cavitation resistance and a lower vulnerability to embolism, indicating that these traits are under strong genetic control. Overall, the study indicates that the phenotypic plasticity in physiological and morphological traits may facilitate adjustment to future climatic conditions. In contrast, anatomical traits related to hydraulic vulnerability are under strong genetic control and increase the drought resistance of dry-origin populations.

A drought experiment was conducted on E. obliqua seedlings and saplings in a controlled glasshouse experiment (Chapter III). To investigate the potential of E. obliqua to acclimate to drier conditions, trees were first exposed to a mild long-term drought (drought conditioning). Following the mild drought, trees were subjected to a subsequent severe drought to induce mortality. Here, the aim was to investigate if drought conditioning can improve tree function and survival and if trait expression changes as trees transition from seedling into sapling stage. The results suggest that mild long-term drought stress induces mainly tree-level morphological trait adjustments, with drought conditioned trees having less leaf area and biomass compared to well-watered controls. Drought conditioning reduced total leaf area which reduced daily water demand, enabling trees to survive for longer during the severe drought event. However, no drought conditioning effect was observed on the water potential at turgor loss point, leaf xylem vulnerability to embolism, leaf size, maximum vessel diameter or wall thickness, indicating that leaf-level physiology, morphology or anatomy have a limited capacity to acclimate through long-term drought stress. Comparing seedling and sapling trait expression, most traits were observed to undergo substantial adjustments with developmental stages, suggesting that drought susceptibility likely changes significantly as trees develop. Seedlings likely confer drought resistance through a high anatomical cavitation resistance, smaller xylem vessel diameters and a lower vulnerability to embolism. In contrast, saplings express a lower water potential at turgor loss point and leaf mass fraction. Hence, drought resistance is likely to change during tree development. Further, depending on the developmental stage, drought resistance is likely to be conferred through different traits.

The second field study (Chapter IV) was designed to analyse seasonal plasticity in drought-related traits as well as adjustments to severe drought in the field. To initialise the prolonged drought, we installed rainfall exclusion gutters, which covered 50% of the surface area, in a E. obliqua forest stand. While no treatment effect between control and treatment sites was observed, the three-years of seasonal trait measurement allowed conclusions on the responses of young trees to different drought intensities in a natural forest stand. In addition to the seasonal observations along the gradient (Chapter II), the data suggest that seasonal morphological adjustments, in form of leaf shedding, occur only in years with more severe drought stress, while physiological traits adjusted also to mild drought stress. In consideration of the observations in Chapter III, the results also suggest that the trees in the field were not severely drought stressed as the full plastic capacity was not implemented. As the field site, with 1000 mm mean annual precipitation, represents nearly E. obliqua’s distribution centre (Fig. 1.2b), this result would further suggest that most E. obliqua trees are under no imminent risk of succumbing to drought-induced tree mortality.

In summary, my studies determined the contribution of physiological, morphological and leaf anatomical traits to the drought resistance of E. obliqua. The results highlight that leaf anatomy (i.e., cavitation resistance, xylem vessel walls) and vulnerability to embolism are under strong genetic control and confers a higher drought resistance for dry-origin populations. In contrast, most physiological and morphological traits demonstrated substantial potential to adjust towards drier conditions in all populations. As a general pattern, osmoregulation was observed under all drought durations and intensities, indicating that it is a main contributor to the drought response in E. obliqua. Intense droughts also induce morphological trait adjustments, in particular leaf shedding, which reduce the trees’ total leaf area and thus their water demand. Similarly, mild long-term droughts also induced leaf shedding as a key drought acclimation response. While the mild long-term drought exposure had only limited influence on the leaf physiology and no influence on leaf-level anatomy and morphology, the effectiveness of phenotypic adjustment in tree-level morphology became apparent during the subsequent severe drought. Trees that were previously exposed to the mild, long-term drought were able to delay canopy collapse and plant death during the subsequent severe drought from 27 to 39 days.

In conclusion, my studies confirm that most physiological and morphological traits are phenotypically plastic and provide fundamental survival benefit in various drought situations. Phenotypic trait adjustments during tree development were also apparent for most traits and suggested that drought resistance differs during tree development. Seedlings conferred their drought resistance mainly through a high anatomical drought resistance and a low vulnerability to embolism. In contrast, saplings likely use physiological and morphological traits and their phenotypic plasticity to provide drought resistance and mature trees use a high anatomical drought resistance as well as physiological and morphological traits.