Heat tolerance metrics, their relations, and identifying large-scale patterns
Tiwari et al . (2020) recently showed that the higher TCrit was among seven Amazonian tree species, the steeper the decrease in Fv/Fm above TCrit. We found the same pattern across the 147 species in our study. As TCrit increased in our study, the b parameter became more negative (r2=0.29). T50 of lowland tropical species appears to be close to a hard, upper limit, as suggested by the fact that growth at elevated temperature does not significantly increase T50 (Krauseet al . 2010, 2013). Indeed, T50 of tropical plants tends to be less variable than TCrit (Tiwariet al. 2020; Perez & Feeley 2020a; current study). This suggests that when plants can prevent irreversible damage up to a higher temperature (i.e., have a higher TCrit) the decrease in Fv/Fm is necessarily steeper. This also means that across a temperature gradient, TCritincreases more steeply with temperature than T50. Interspecific variation in b also explains why T50 and TCrit, although correlated, did not scale equally with other leaf traits. For example, we found a significant relationship between T50 and LMA among lowland plants, but not between TCrit and LMA, because b correlated with LMA in such a way that the slope of the TCrit–LMA relationship was reduced relative to the T50–LMA slope.
In 1935, Sapper (1935) wrote that since the pioneering work by Sachs (1864) various studies had been conducted to investigate plant heat tolerance, but that systematic comparisons are complicated by the all-too-different methodologies used. This remains true 85 years later (Geange et al. 2020). A recent study (Lancaster & Humpreys 2020) compiled heat tolerance data from across the plant kingdom, but combined metrics with fundamentally different meanings, such as T50 of Fv/Fm as defined in the current study (using data from e.g., Slot et al . 2018), T50 of F0 rise (e.g., Zhu et al . 2018), TCrit of F0 rise (Marias et al . 2016), TMax of dark respiration (e.g., O’Sullivanet al . 2017), and heat tolerance based on electrolyte leakage (e.g., Nobel & Smith 1983). Identifying reliable, general patterns of thermal tolerance across environmental gradients thus remains challenging, and more studies are needed using consistent methodology (Geange et al. 2020). Here we used >110 lowland species—the largest dataset on heat tolerance of lowland tropical forest plants to date—and almost 40 mid-elevation to pre-montane species, measured with a now commonly used protocol (Krause et al. 2010). We show that 30% of the heat tolerance variation across a phylogenetically and functionally diverse range of species could be explained by elevation and LMA alone. Site elevation is readily available, and LMA is one of the best represented traits in the TRY database (Kattge et al . 2020), making this a useful predictor, at least for the species-rich and understudied lowland tropics—at higher elevation neither LMA, nor indeed any of the tested traits was a strong predictor of heat tolerance. Remaining variation is likely explained in part by variation in microclimate, which has been shown to have strong effects on maximum leaf temperatures (Fauset et al. 2018), and heat tolerance (Curtis et al. 2016; Perez & Feeley 2020a); differences in preconditioning to mild stressors that caused upregulation in antioxidant activity; and variation in other aspects that may protect leaves against heat damage, such as the capacity for isoprene emission, which is associated with higher maximum temperature for carbon fixation among tropical forest species (Taylor et al . 2019).
Tropical forests are sensitive to rising temperatures. Warming decreases net carbon uptake (Clark et al . 2003; Sullivan et al . 2020), results in shifts in species composition (e.g., Fadrique et al . 2018; Feeley et al . 2020b), and exacerbates climate extremes (Rifai et al . 2019) and the risk of associated mortality. Due to the increased frequency of extreme events TCrit may already be exceeded occasionally in forests in the southern Amazon (Tiwari et al . 2020). We showed that lowland forests in Panama are operating closer to their critical upper temperature thresholds than pre-montane forests, but that in both ecosystems species differ considerably in their proximity to critical thresholds. To properly determine thermal safety margins detailed information is needed on variation in leaf temperature dynamics among co-occurring species, and predicting future safety margins further requires understanding of the plasticity of heat tolerance; upregulation of heat tolerance appears limited, but this needs to be tested for more tropical forest species.