High heat tolerance, evaporative cooling, and stomatal decoupling regulate canopy temperature and their safety...

Heatwaves and soil droughts are increasing in frequency and intensity, leading many tree species to exceed their thermal thresholds, and driving wide-scale forest mortality. Therefore, investigating heat tolerance and canopy temperature regulation mechanisms is essential to understanding and predicting tree vulnerability to hot droughts. We measured the diurnal and seasonal variation in leaf water potential (Ψ), gas exchange (photosynthesis A_net and stomatal conductance g_s), canopy temperature (T_can), and heat tolerance (leaf critical temperature T_crit and thermal safety margins TSM, i.e., the difference between maximum T_can and T_crit) in three oak species in forests along a latitudinal gradient (Quercus petraea in Switzerland, Quercus ilex in France, and Quercus coccifera in Spain) throughout the growing season. Gas exchange and Ψ of all species were strongly reduced by increased air temperature (T_air) and soil drying, resulting in stomatal closure and inhibition of photosynthesis in Q. ilex and Q. coccifera when T_air surpassed 30°C and soil moisture dropped below 14%. Across all seasons, T_can was mainly above T_air but increased strongly (up to 10°C > T_air) when A_net was null or negative. Although trees endured extreme T_air (up to 42°C), positive TSM were maintained during the growing season due to high T_crit in all species (average T_crit of 54.7°C) and possibly stomatal decoupling (i.e., A_net ≤0 while g_s >0). Indeed, Q. ilex and Q. coccifera trees maintained low but positive g_s (despite null A_net), decreasing Ψ passed embolism thresholds. This may have prevented T_can from rising above T_crit during extreme heat. Overall, our work highlighted that the mechanisms behind heat tolerance and leaf temperature regulation in oak trees include a combination of high evaporative cooling, large heat tolerance limits, and stomatal decoupling. These processes must be considered to accurately predict plant damages, survival, and mortality during extreme heatwaves.