Stomatal decoupling: New insights into environmental drivers and underlying physiological mechanisms during simulated heatwaves in temperate and tropical tree species

By 2024, anthropogenic greenhouse gas emissions have increased global average surface temperatures 1.55 °C above pre-industrial levels. This has led to an increase in both the intensity and frequency of heat waves. In recent years, it has been shown that the strong relationship (e.g., the coupling) between net photosynthetic CO2 assimilation (Anet) and stomatal conductance (gs) is decreased or even lost at high temperatures (Diao et al., 2024; Marchin et al., 2023). However, the isolated effect of environmental drivers (e.g. air temperature, vapour pressure deficit; VPDair) and the underlying plant physiological mechanisms are not yet fully understood (Mills et al., 2024). To improve our understanding why at high temperatures gs continues to increase while Anet decreases, we conducted a climate chamber experiment with 3 temperate (Alnus cordata, Acer platanoides, Phillyrea angustifolia) and 3 tropical (Terminalia microcarpa, Terma tomentosa, Syzygium jambos) tree species. In one chamber, we increased the air temperature (Tair) from 20 to 40 °C in 5 °C steps (2 days at every temperature) while keeping the VPDair at 1.2 kPa. In the second chamber, we increased Tair the same way, but simultaneously increased VPDair every step from 1.2 to 6 kPa. One subset per chamber was kept well-watered (e.g. at capacity; ~35 vol-%), while in the other subset the trees were exposed to soil drought (~8 vol-%). Every second day, we conducted leaf gas exchange measurements. Across all species, we observed gs to continue to increase while Anet decreased (but never reached 0 or negative values) at high temperatures above 35 °C under constant VPD, while increasing VPD maintained the coupling between the two by decreasing gs. However, the transpiration rate (E) showed the same pattern of decoupling under both VPD regimes. Since E is directly driven by gs and VPD, plants need to upregulate gs in order to upregulate E if VPD is too low. While E is important for the regulation of leaf temperature, it is also crucial for other plant physiological processes. We speculate that another reason for increasing E may be that E drives sap flow, which is important for the internal transport and distribution of nutrients, O2 and CO2 in plants. Thus, an increased sap flow might be crucial to sustain tree functioning during high-temperature driven periods of accelerated metabolic activity. Future specifically designed experiments are needed to simultaneously investigate plant physiological responses in different tissues as well as at the whole plant level.