Hydrological limits to leaf cooling during a record summer heat wave

Extreme heatwaves, that are increasing in intensity and duration around the globe, are causing many locally adapted plant populations to rapidly become maladapted to climate conditions in ways that are likely to impact forest carbon storage, biogeochemical cycling, and biodiversity. One species that may be of particular risk from excess heat exposure is Populus fremontii (Wats.): a dominant riparian tree species that occupies extremely arid riparian ecosystems in western North America. We used an experimental common garden of two-year old P. fremontii genotypes sourced across a broad climate gradient to evaluate leaf thermal regulation and thermal tolerance of trees exposed to daytime summer temperatures that regularly exceeded 45 °C. Traits were measured to evaluate patterns of hydraulic and thermal safety, including leaf temperature (T_leaf), stomatal conductance, leaf water potentials, leaf turgor loss point, stem xylem cavitation vulnerability and leaf thermal tolerance - defined as the critical temperature that triggers rapid reductions in electron transport capacity of Photosystem II (T_crit; °C). Three major results emerged. First, T_leaf of genotypes from the warmest locations were 4 to 5 °C cooler than air temperatures, even on days where air temperatures exceeded 48 °C. Second, short-term reductions in soil water availability - even reductions that were largely undetectable from predawn leaf water potentials - disrupted leaf cooling patterns in all genotypes, resulting in periods in which T_leaf exceeded T_crit. And third, during the warmest period of the summer, a clear tradeoff was detected between leaf thermal safety and hydraulic safety, with warm-adapted genotypes risking hydraulic safety to maximize leaf thermal safety. Results not only improves our understanding of tree thermal limits in the face of episodic heat exposure, but also advances our understanding of how short-term changes in soil moisture availability can alter plant thermal regulation and subsequent exposure to long-term heat stress.