Introduction
The conservation of existing forests and active reforestation are
pivotal to mitigating the worst impacts of climate change (Girardin et
al., 2021; Griscom et al., 2017). However, periodic heat stress induced
by rapid climate change (IPCC, 2022) threatens forest function and
thereby the future success of these conservation efforts (Jordan et al.,
2023). Increased frequency of hot, dry conditions has driven declines in
forest tree populations (Hammond et al., 2022) and associated carbon
accumulation in biomass (Anderegg et al., 2016; Brienen et al., 2015).
Tropical rainforests may be particularly susceptible, given their
canopies already experience temperatures in excess of their thermal
limits for maximum photosynthesis (Mau et al., 2018). With the frequency
of lethal temperatures predicted to increase with future global warming
(Doughty et al., 2023), it is essential to understand the capacity of
species to tolerate or avoid heat stress.
The leaf thermal safety margin describes the difference between observed
maximum leaf temperatures and thermal tolerance of photosynthesis, and
as such is a useful proxy to determine vulnerability of ecosystems,
species, or populations to climate warming. Photosynthetic heat
tolerance is often determined by assessing irreversible damage to leaf
photosystem II using chlorophyll fluorescence (Maxwell & Johnson,
2000). Two commonly used metrics are Tcrit and
T50, representing the temperatures at which there is a
5% and 50% irreversible decline in photosystem II functioning. Higher
photosynthetic heat tolerance is a common adaptation to warmer leaf
temperatures (Perez & Feeley, 2020), with higher values generally found
in leaves exposed to higher ambient temperatures (Geange et al., 2021;
O’Sullivan et al., 2017), lower soil moisture (Cook et al., 2021), and
higher radiation (Slot et al., 2019). While species originating from
warmer habitats exhibit higher Tcrit, the increase
observed across an increase in growth temperature is modest, ranging
from 0.24 to 0.60 °C increase per 1 °C increase in mean annual
temperature (O’Sullivan et al., 2017; Slot et al., 2021; Zhu et al.,
2018). Consequently, higher observed leaf temperatures in warmer
climates such as lowland tropical forests result in them having a
narrower thermal safety margin, which has been observed across species
in contrasting biomes (Kitudom et al., 2022; Perez & Feeley, 2020) and
within species (Kullberg et al., 2023).
Forest canopy leaf temperatures can be substantially different from
ambient air temperatures (Blonder & Michaletz, 2018; Crous et al.,
2023; Doughty et al., 2023; Mau et al., 2018; Rey-Sanchez et al., 2017;
Song et al., 2017; Still et al., 2022). Leaf temperature is a result of
the balance of sensible and latent heat fluxes, along with net incoming
radiation, and is impacted by a broad suite of morphological and
physiological traits that interact with the microclimate of the leaf
(Campbell & Norman, 1998; Jones, 2013). Fully illuminated sunlit leaves
are typically warmer than ambient air temperatures (Zhou et al., 2023),
with the magnitude of this offset (∆T) varying due to differences in
leaf thermal traits (Blonder & Michaletz, 2018), such as effective leaf
width, solar absorptance profile, inclination angle and orientation, and
dynamic stomatal conductance (g s) (Fauset et al.,
2018; Guo et al., 2022; Perez & Feeley, 2020). Trait variation
resulting in enhanced leaf cooling is an important strategy to avoid
heat stress (Deva et al., 2020; Drake et al., 2018). Indeed, there is
growing evidence that communities of plant species grown under warmer
conditions preferentially express leaf trait combinations that decrease
leaf warming compared to those grown under cooler conditions (Kitudom et
al., 2022; Kullberg et al., 2023; Leigh et al., 2012; Middleby et al.,
2024a; Posch et al., 2022; Wright et al., 2017), providing some support
to the idea of plant thermoregulation and limited homeothermy (Blonder
& Michaletz, 2018; Michaletz et al., 2016).
However, it is unclear to what extent intra-specific genetic variation
may also show similar patterns of limited homeothermy. A recent study in
sagebrush reported lower canopy temperatures of warm origin populations,
attributing this to differences in plant height altering canopy
microclimate (Olsoy et al., 2023). Similarly, warm origin genotypes ofPopulus fremontii exhibited higher transpiration rates and
consequently lower leaf temperatures compared to cool origin genotypes
(Hultine et al., 2020). In addition, enhanced leaf cooling has been
associated with more heat tolerant genotypes in common bean (Deva et
al., 2020). On the other hand, evidence for increased thermal tolerance
of warm-origin genotypes is mixed (Chen et al., 2016; Coast et al.,
2022; Gimeno et al., 2008; Marias et al., 2016). If tropical trees do
exhibit a simultaneous increase in thermal tolerance and decrease in
leaf temperatures of warm origin provenances, there is a potential for
warm origin genotypes to have greater thermal safety margins when
planted under common conditions, such as in restoration plantings.
However, if Tcrit acclimates to Tleafacross populations as it does across species and biomes (Perez &
Feeley, 2020), this may ultimately lead to a convergence of thermal
safety margins. Therefore, understanding how these two variables covary
across provenances is important for the conservation and management of
tropical rainforests.
Here we tested whether upland and lowland provenances of four tropical
tree species differed in their thermal safety margins when grown in a
lowland common garden. This was achieved by measuring photosynthetic
heat tolerance, leaf, and canopy temperatures, as well as leaf thermal
traits which were then used to paramaterise a leaf energy balance model.
We hypothesised that provenances from the warmer lowlands would have a
lower ΔT compared to provenances from the cooler uplands (H1), and that
this provenance variation could be explained by variation in both leaf
thermal traits, and differences in microclimate in plants of differing
canopy heights (H2). We also expected thermal tolerance to acclimate to
Tleaf, such that Tcrit and
T50 would show similar patterns of
provenance-differentiation as ΔT, leading to a convergence of thermal
safety margins across provenances (H3).