Seasonal acclimation of photosynthetic thermal tolerances in six woody tropical species along a thermal gradient

1 INTRODUCTION

Anthropogenic climate change in the Amazon has led to a significant rise in mean air temperatures as well as the frequency, intensity and duration of heatwaves (Costa et al., 2022; de Barros Soares et al., 2017). These changes are concerning, as tropical plants are particularly sensitive to heatwaves (Doughty et al., 2023; Kitudom et al., 2022). This vulnerability may arise from tropical plants having evolved under relatively stable climate conditions that have promoted the evolution of thermal specialists (Cunningham & Read, 2003; Janzen, 1967; Kullberg & Feeley, 2022; Perez et al., 2016). Moreover, given their long lifespans and generation times, it is highly unlikely that most tropical tree species will be able to respond to climate change through evolutionary adaptation or migration to more suitable habitats (Feeley et al., 2023; Wang et al., 2023). It is therefore imperative to investigate the ability of individual tropical trees to acclimate to rapid changes in temperature through acclimation.

Photosynthetic thermal tolerance may be especially pertinent for understanding the rapid acclimation of plants to extreme temperature events and is defined as a high-temperature threshold beyond which the functioning of Photosystem II—one of the more thermally sensitive components of the photosynthetic apparatus—is impaired (Berry & Björkman, 1980). In addition, thermal tolerance has recently been associated, albeit weakly, with permanent leaf damage (Zhang et al., 2024) and thus is a potential mechanism through which rising temperatures may lead to increased tree mortality and cause forest dieback (Doughty et al., 2023). Importantly, photosynthetic thermal tolerance tends to be more plastic than many other leaf traits that are related to leaf temperature (e.g. morphoanatomical traits) because it is related to leaf biochemistry and gene regulation and can therefore change in response to abiotic conditions within the lifespan of a single leaf (Perez & Feeley, 2021; Zhu et al., 2018). Indeed, there are various mechanisms governing photosynthetic thermal tolerance (Geange et al., 2020), including membrane content of saturated fatty acids (Zhu et al., 2018), heat shock protein expression and content (Barua & Heckathorn, 2006; Chen et al., 2018), production of zeaxanthin (Demmig et al., 1987; Demmig-Adams, 1998), synthesis of antioxidants (Gill & Tuteja, 2010), and content of plant hormones such as abscisic acid and brassinosteroid (Li et al., 2021). This polygenic trait plays a critical role in conferring resistance in plants to increasingly frequent and intense heatwaves (Doughty et al., 2023; Feeley et al., 2023).

Previous studies have shown that acclimation of thermal tolerance in tropical trees to rapid changes in temperature (over days to months) is generally possible but is often insufficient to fully offset increases in leaf temperatures (Kitudom et al., 2022). For example, O'Sullivan et al. (2017) and Zhu et al. (2018) found seasonal acclimation in all 3 and 10 of their tropical rainforest study species, respectively. Drake et al. (2018) found that growth temperature had no impact on the ability of Eucalyptus parramattensis to acclimate its thermal tolerance in response to a heatwave. In contrast, other studies have found weak or no seasonal acclimation of thermal tolerance in tropical trees and consequently narrowing leaf thermal safety margins during extreme heat events (Tiwari et al., 2021) and a negative relationship between deciduousness and acclimation response (Sastry & Barua, 2017), signalling a trade-off between leaf longevity and resource investment.

In this study, we tested whether six common, woody Amazonian species acclimate their photosynthetic thermal tolerances to differences in maximum air temperatures between the end of the local wet (cool) season and the end of the local dry (hot) season along the Boiling River thermal gradient in the Peruvian Amazon. We measured photosynthetic thermal tolerances in both the dry and wet season, remeasuring the same individuals between seasons. In a parallel study on the same species, Kullberg et al. (2024) found limited signs of acclimation to overall growing temperatures in terms of leaf thermoregulatory traits (i.e. traits that are directly or indirectly related to regulation of leaf temperature) as well as limited acclimation of thermal tolerance when measured only once at the end of the dry season. These findings suggested limited phenotypic plasticity and/or decoupling of leaf and air temperatures unrelated to variation in thermoregulatory traits. The current study builds on these results and expands our understanding of the thermal ecology of woody Amazon species by investigating the responsiveness of their thermal tolerances to seasonal temperature changes.

Our specific research questions were: (1) Do individual plants of the six focal species acclimate their thermal tolerances between seasons? Based on the varied intraspecific responses of thermoregulatory traits and thermal tolerances to overall growing temperatures previously observed at the Boiling River (Kullberg et al., 2024), we hypothesized that the more plastic species in terms of thermoregulation would also show a greater ability to increase their thermal tolerances. (2) Is the magnitude of thermal tolerance acclimation associated with the magnitude of microsite-level seasonal differences in maximum air temperature (ΔT_max)? We expect that species with leaf temperatures closely related to air temperatures should show acclimation responses dependent on the magnitude of ΔT_max, whereas species whose leaf temperatures are more strongly governed by other factors, such as solar radiation, should show little or no relationship between acclimation response and magnitude of ΔT_max. Understanding the ability of Amazonian plant species to acclimate to changes in temperature will increase our ability to predict the effects of climate change on tropical forests.