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.