On the importance of vapor pressure deficit for the determination of the photosynthetic temperature optimum in tropical trees

Abstract

Temperature can stimulate photosynthesis until a maximum rate is reached. This temperature point is referred to as the photosynthetic temperature optimum (i.e. T_opt). However, when T_opt is exceeded, plants must close their stomata to maintain the integrity of the xylem water column to avoid embolism-induced mortality (McDowell et al., 2022). This mechanism leads to a significant reduction in carbon uptake through the inhibition of photosynthesis, resulting in a sharp decline in carbon sequestration. Moreover, stomatal closure can also reduce transpiration rate, which in turn reduces the potential for evaporative cooling at the leaf surface, consequently leading to elevated leaf temperatures (T_leaf). Although T_leaf typically closely tracks air temperature (Still et al., 2021), variations in biological and environmental conditions, such as leaf thickness and light availability, respectively, can result in large deviations of T_leaf, above or below T_air, by altering latent or sensible heat losses. Furthermore, when species-specific leaf thermal thresholds (T_crit) are exceeded, elevated leaf temperatures can lead to severe leaf scorching and tissue mortality (Still et al., 2023). Although this effect has yet to be observed in tropical forests, the gradual rise in T_air and VPD recorded in the tropics implies that widespread canopy mortality could occur under future climatic conditions (Lancaster & Humphreys, 2020). Despite these predictions, there is a growing literature documenting the acclimation of T_opt to different environmental conditions (Wittemann et al., 2022), suggesting that trees may exhibit enhanced photosynthetic performance under elevated temperature due to the increase in T_opt with increasing growth temperatures. While this may be positive news for the trees, understanding whether this long-term acclimation is associated with an adjusted stomatal sensitivity to VPD or a change in temperature-induced biochemical thresholds remains a challenge to unravel. For instance, in a previous study, the acclimation of T_opt was found to be strongly downregulated by factors affecting stomatal behavior (such as VPD), although forests with higher air temperatures (such as tropical forests) exhibited higher T_opt, indicating an adaptive strategy which increases the resilience of tropical forests (Tan et al., 2017).

Nevertheless, one of the main challenges in accurately measuring T_opt is the way temperature response curves (i.e. photosynthesis vs temperature) are computed. Indeed, in many studies, temperature response curves do not take into account the effects of VPD, even though increasing temperature inherently means increasing VPD. Thus, to assess how VPD and temperature independently affect T_opt, Slot et al. used different functions, a nonlinear parabolic temperature optimum and a generalized additive model (GAM), to fit their extended dataset. Through this process, they created VPD-dependent and VPD-independent temperature response curves by removing the ‘VPD’ factor from temperature-only models. With these curves, the authors demonstrated for the first time that, in tropical forests, the impact of VPD is greater than the impact of temperature on photosynthesis. They showed a clear increase in T_opt in response to the combined influence of temperature and VPD, compared with temperature alone, in trees growing in the wet forest of San Lorenzo. Results from this study further reveal that VPD-dependent temperature response curves more accurately predict ‘true’ T_opt compared with estimating T_opt without considering VPD. Failure to account for VPD during these measurements could underestimate ‘apparent’ T_opt by over 3°C in trees, thus potentially underestimating carbon uptake and storage in tropical forests. In lianas, this discrepancy was not even discernible as T_opt exceeded the measured temperature range. This indicates that the temperature response of photosynthesis in tropical trees is primarily driven by the indirect effect of temperature, resulting from VPD changes, and highlights how VPD confounds the temperature response of photosynthesis. Stomatal conductance exhibited a similar response, thus emphasizing the role of VPD as the primary factor explaining the dynamics of gas exchange. Moreover, the VPD-dependent T_opt corresponded to the T_opt of photosynthetic parameters such as the maximum velocity of carboxylation and maximum rate of photosynthetic electron transport (measured in a previous study), highlighting the importance of indirect temperature effects on the net photosynthetic rate.

These results have major implications regarding the future dynamic of tropical forests under climate change. Understanding the relative contributions of the two mechanisms of high-temperature photosynthetic declines (i.e. VPD-induced stomatal restrictions and temperature-driven biochemical limitations) is essential to accurately predict future carbon cycling in tropical forests. Mild VPD increases can have a positive effect on photosynthesis, through the acclimation of T_opt or by increasing stomatal sensitivity to VPD (Marchin et al., 2016). However, growing under high VPD comes with major costs, especially regarding changes in nitrogen plant status or reduction in primary productivity (López et al., 2021). Increased VPD due to higher temperature also leads to reduced transpiration rate and gas exchange, and to higher tree mortality rate through VPD-enhanced soil drought (Will et al., 2013). Similarly, with temperature alone, photosynthesis may be reduced due to the high sensitivity of the Rubisco and the electron transport chain to elevated temperatures. Yet, several studies have observed an increase in stomatal conductance with rising temperatures which was attributed to the lower water viscosity and increasing plant membrane permeability under warming, thus increasing water availability to guard cells (Diao et al., 2024). In their study, Slot et al. highlighted that VPD overrides the impacts of temperature alone on the temperature response of photosynthesis in tropical trees. They suggested that temperature-induced biochemical damage was not the main driver of photosynthesis limitation restricting A_opt. Instead, VPD-induced stomatal closure was proposed as the main driver of photosynthesis reduction under increased temperatures. Although the mechanisms driving stomatal closure in response to high VPD remain to be clarified, they are thought to involve an active sensing of the water status in cells, probably mediated by abscisic acid (Grossiord et al., 2020). Nevertheless, the VPD-corrected ‘true’ T_opt is the result of complex interactions between VPD-dependent stomatal limitation, but also VPD-independent direct temperature effects on photorespiration and Rubisco deactivation. Thus, despite VPD being the main limitation of photosynthesis and carbon uptake in tropical trees, the effect of temperature alone should not be underestimated.

In conclusion, the authors provided compelling evidence that the stomatal response to VPD is the primary mechanism reducing photosynthetic capacity in tropical trees, and this mechanism is likely to predominate over the direct effect of temperature in the short term. The results from Slot et al. suggest that, in tropical forests, photosynthesis is limited by the indirect effect of temperature through VPD changes. Furthermore, it is suggested that not taking VPD into account could alter the accuracy of predictions of carbon stock and forest growth under future climates. Finally, while this study highlights the importance of VPD on the short-term responses of tropical trees, the long-term dynamic may differ as T_opt acclimation may occur.