Adam D. Collins

A multi-species synthesis of physiological mechanisms in drought-induced tree mortality

Widespread tree mortality associated with drought has been observed on all forested continents and global change is expected to exacerbate vegetation vulnerability. Forest mortality has implications for future biosphere–atmosphere interactions of carbon, water and energy balance, and is poorly represented in dynamic vegetation models. Reducing uncertainty requires improved mortality projections founded on robust physiological processes. However, the proposed mechanisms of drought-induced mortality, including hydraulic failure and carbon starvation, are unresolved. A growing number of empirical studies have investigated these mechanisms, but data have not been consistently analysed across species and biomes using a standardized physiological framework. Here, we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought-induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves at mortality, indicating that evidence supporting carbon starvation was not universal. Reduced non-structural carbohydrates were more common for gymnosperms than angiosperms, associated with xylem hydraulic vulnerability, and may have a role in reducing hydraulic function. Our finding that hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling can be achieved using thresholds in hydraulic function.The mechanisms underlying drought-induced tree mortality are not fully resolved. Here, the authors show that, across multiple tree species, loss of xylem conductivity above 60% is associated with mortality, while carbon starvation is not universal.

Responses of two semiarid conifer tree species to reduced precipitation and warming reveal new perspectives for stomatal regulation

Relatively anisohydric species are predicted to be more predisposed to hydraulic failure than relatively isohydric species, as they operate with narrower hydraulic safety margins. We subjected co-occurring anisohydric Juniperus monosperma and isohydric Pinus edulis trees to warming, reduced precipitation, or both, and measured their gas exchange and hydraulic responses. We found that reductions in stomatal conductance and assimilation by heat and drought were more frequent during relatively moist periods, but these effects were not exacerbated in the combined heat and drought treatment. Counter to expectations, both species exhibited similar gs temporal dynamics in response to drought. Further, whereas P. edulis exhibited chronic embolism, J. monosperma showed very little embolism due to its conservative stomatal regulation and maintenance of xylem water potential above the embolism entry point. This tight stomatal control and low levels of embolism experienced by juniper refuted the notion that very low water potentials during drought are associated with loose stomatal control and with the hypothesis that anisohydric species are more prone to hydraulic failure than isohydric species. Because direct association of stomatal behaviour with embolism resistance can be misleading, we advocate consideration of stomatal behaviour relative to embolism resistance for classifying species drought response strategies.

Tree water dynamics in a drying and warming world

Disentangling the relative impacts of precipitation reduction and vapour pressure deficit (VPD) on plant water dynamics and determining whether acclimation may influence these patterns in the future is an important challenge. Here, we report sap flux density (FD ), stomatal conductance (Gs ), hydraulic conductivity (KL ) and xylem anatomy in piñon pine (Pinus edulis) and juniper (Juniperus monosperma) trees subjected to five years of precipitation reduction, atmospheric warming (elevated VPD) and their combined effects. No acclimation occurred under precipitation reduction: lower Gs and FD were found for both species compared to ambient conditions. Warming reduced the sensibility of stomata to VPD for both species but resulted in the maintenance of Gs and FD to ambient levels only for piñon. For juniper, reduced soil moisture under warming negated benefits of stomatal adjustments and resulted in reduced FD , Gs and KL . Although reduced stomatal sensitivity to VPD also occurred under combined stresses, reductions in Gs , FD and KL took place to similar levels as under single stresses for both species. Our results show that stomatal conductance adjustments to high VPD could minimize but not entirely prevent additive effects of warming and drying on water use and carbon acquisition of trees in semi-arid regions.

Lack of acclimation of leaf area:sapwood area ratios in piñon pine and juniper in response to precipitation reduction and warming

The leaf area to sapwood area ratios of trees (Al:AS) can shift to maintain homeostatic gas exchange per unit leaf area in response to climate variability. We tested the hypothesis that trees alter their Al:AS ratios in response to long-term warming and reduced precipitation in order to maintain leaf-specific gas exchange rates under more stressful conditions. Whole-tree Al:AS was measured on mature piñon pine (Pinus edulis Engelm.) and one-seed juniper (Juniperus monosperma (Engelm.) Sarg.) trees after 5 years (2012-16) of chronic exposure to increased temperature (+4.8 °C), precipitation reduction (-45%), or both simultaneously. No difference was found in Al:As among treatments for either species. Associated with this lack of shift in Al:As were large changes in pre-dawn leaf water potential and stomatal conductance, consistent with theoretical expectations of interactions between leaf and whole-tree hydraulic supply. Our results suggest that a lack of whole-tree acclimation in Al:As results in the reductions in plant gas exchange and water status associated with long-term warming and reduced precipitation in semi-arid woodlands.