A matter of leaf and death

As climatic changes enhance the likelihood of abrupt weather instability and the persistence of drought events, a critical challenge is to identify plant species that are most susceptible to these fast-changing conditions. The last decades have been characterised by alarming observations and reports of drought-induced forest diebacks, along with changes in species distribution and forest community composition. In particular, the phenomenon of canopy dieback is concerning at multiple scales, given that leaf damage is often a prelude to systemic failure in the whole plant. Drought not only has a direct impact on leaf mortality, but it can also induce lagged effects with consequences on plant recovery. Despite the gigantic efforts made to elucidate the drought effects on plants, we are still missing the physiological understanding of the drought mortality process, even at the leaf scale.
Water is transported in plants through an elegant, yet vulnerable hydraulic system called xylem, where it flows under a tension that connects the soil-plant-atmosphere continuum. The failure of this continuum has been correlated with plant damage and death during water stress, but the causal mechanism is still missing. During drought, xylem cavitation can occur and spread throughout the xylem causing a feedback that increases tension in the system leading to the complete blockage of the pipeline to a point of non-recovery, in a phenomenon known as hydraulic failure. Nevertheless, due to the complexities associated with detecting xylem cavitation, we still have imprecise knowledge about the effects of cavitation-induced air embolism in plant tissues, nor do we understand how it drives canopy damage and tree mortality.
This thesis links xylem vulnerability characteristics of leaves with the processes of drought-induced canopy dieback and canopy recovery after drought. I use the Optical Vulnerability Technique and a trait-based approach to study drought-induced cavitation spread at the leaf tissue level (Chapter 2), canopy level (Chapter 3), tree level (Chapter 4) and population level (Chapter 5).
In Chapter 1, I point out how current literature considers xylem cavitation as a process that is correlated but not yet linked to tree mortality. I discuss the knowledge gathered so far and the lack of a mechanistic understanding of the triggers of leaf tissue desiccation. Finally, I outline the objective of this thesis, and the specific aims of each chapter and explain the selection of Eucalyptus viminalis Labill. as a model tree species used throughout this work.
In Chapter 2, I follow the decline of photosynthetic activity and leaf width in juveniles of E. viminalis during whole-plant dehydration to find the triggers of lethal leaf desiccation. I causally associate the spread of cavitation into the terminal part of the leaf water transport system and the initiation of runaway cavitation feedback with the acceleration of tissue shrinkage, which causes damage to the photosynthetic machinery. These results reveal the importance of embolism spreading in high order veins (veins from 3^rd order above) as a triggering process driving tissue death, providing a causal explanation for canopy damage during drought.
By developing this further, in Chapter 3 I investigate the phenomenon of drought legacy and why assimilation recovery is impaired after water stress in tree canopies. I reveal that there is a clear cavitation threshold after which leaves cannot recover and rapidly die. However, this does not translate into instant canopy collapse, but, upon rewatering, into a gradual loss of assimilation recovery according to increasing water stress. I found that this is due to a significant variation in cavitation vulnerability within the canopy, which represents a possible mechanism allowing evergreen tree species to delay the desiccation time during drought and preserve a portion of leaves still functional.
In Chapter 4, I explore the source of canopy variation to predict the lethal desiccation time of branches. Determining which traits vary across canopies and which are constant, casts light on what is driving observed variation in leaf drought resistance found in Chapter 3. I use these findings to calculate the time to runaway cavitation utilising the new formulation introduced in Chapter 2 and dry-down data obtained from a natural population of trees, demonstrating how these variables can be used to predict canopy dieback. The results show the scale of variation hidden in tree canopies and how this affects the time to death, broadening the understanding of climate change impacts on plants with applications for plant conservation.
In Chapter 5, I measure the genetic variation to drought resistance among provenances of E. viminalis to select those more likely to survive future climatic conditions to determine whether local adaptation to climatic variation within species is occurring and could be used as a resource for forest restoration. I choose a suite of mechanistic and functional traits to compare provenances grown in a common garden. The results indicate that leaf and hydraulic traits are conserved among different provenances, but lignotuber traits differ, suggesting that they have been consistently selected to favour those populations growing in the most arid spectrum of distribution, where the selective pressure has acted in this direction.
Lastly, in Chapter 6 I discuss how the findings provided in this thesis contribute to elucidating the mechanistic role of cavitation in tissue damage and its consequence for canopy recovery. These results are discussed in the context of the variation present at leaf level that contributes to protecting canopies from drought stress, increasing the buffer time before tree death. Combined with the existing knowledge, these findings provide a model by which it should be possible to quantify the vulnerability of trees to drought-induced damage in forests across the world.