Introduction
The effect of global environmental change on life on earth often
exhibits threshold dynamics in which performance steeply and
irreversibly drops off above or below a critical threshold (Scheffer
2009). One example is the heat tolerance of ectotherms: beyond a
critical temperature threshold (TCrit) performance
rapidly declines, eventually resulting in irreversible damage typically
only a few degrees above TCrit, as shown in e.g.
arthropods (García-Robledo et al . 2016; Franken et al .
2018), amphibians and reptiles (e.g., Duarte et al . 2012), as
well as in primary producers such as phytoplankton (Padfield et
al . 2016) and terrestrial plants (e.g., Sachs 1864; Sapper 1935; Knight
& Ackerly 2003; Krause et al . 2010). To better anticipate the
consequences of rising temperatures for ectotherms it will be important
to understand variation in thermal thresholds among co-occurring species
within a community and among different communities. Because of the
dependence of virtually all organisms on primary producers,
understanding thermal thresholds of photosynthesizing organisms is
particularly important.
More than 150 years ago, Sachs (1864) reported that plants in his
university’s botanical garden could withstand exposure to air
temperatures up to 50°C without leaf damage, but that 51°C or higher
temperatures killed the leaves. Later studies reported more variation in
heat tolerance, with both lower and higher values being observed in the
early 20th century (Sapper 1935), but it remained
challenging to identify general patterns underlying this variation. In
recent years leaf heat tolerance has received renewed interest as
ongoing global warming and more frequent and intense heatwaves may push
ecosystems past their critical thermal thresholds (Feeley et al. 2020a;
Lancaster & Humphreys 2020; Perez & Feeley 2020a,b; Geange et al.
2021). Recent studies have shown that heat tolerance increases from the
poles towards the tropics (O’Sullivan et al . 2017) and from high
elevation to low elevation (Feeley et al . 2020a), in parallel
with increasing temperatures under which plants develop. While
consistent, the increase in thermal thresholds along these gradients is
moderate: 0.38°C per °C increase in mean maximum temperature of the
warmest month from poles to the tropics, and < 0.1°C
°C–1 mean annual temperature from high to low
elevation. Furthermore, at each latitude and elevation heat tolerance
varies considerably among species, and the mechanisms underlying this
variation have not been explored in detail.
Variation in heat tolerance among co-occurring species may represent
functional or ecological differences in micro-climate adaptation among
species. For example, Sapper (1935) already showed that sun species have
higher heat tolerance than shade species, and Slot et al . (2018)
showed that even within species, heat tolerance tends to be moderately
higher in sun leaves than in shade leaves. Within site variation may
also reflect different evolutionary histories of plants. Dick et
al . (2013) reported that many common Neotropical tree species have
emerged long enough ago to have previously experienced climatological
conditions not unlike those predicted for the end of the current
century. As such, Dick et al . (2013) proposed, these survivors of
past extreme climates may be more likely to tolerate high temperatures
than species in contemporary Neotropical forests that have emerged more
recently under relatively cooler conditions. Neotropical forests have
existed for at least ~58 million years (Wing et
al . 2009) and are characterized not only by high species diversity, but
also by great diversity at higher taxonomic levels. For example, on 50
hectares of forest in central Panama > 300 species of woody
plants with >1 cm stem diameter have been identified,
belonging to >60 families, including ancient families such
as Fabaceae and Lecythidaceae and families of more recent origins such
as Chrysobalanaceae and Apocynaceae. Within site variation of
temperature sensitivity may thus also be related to the evolutionary
history of species.
Tropical forest trees routinely experience high temperatures when
exposed to direct irradiance, especially during moments of low wind
speed, with leaf temperatures exceeding air temperature by as much as
10–18°C (Doughty & Goulden 2008; Rey-Sanchez et al . 2016;
Fauset et al . 2018). Leaf traits can influence both the magnitude
and rate of leaf heating (Jones 2013). For example, greater leaf width
and leaf size are generally associated with a larger leaf boundary layer
and greater decoupling of leaf and air temperatures (Jones 2013).
Indeed, Fauset et al . (2018) parameterized a leaf energy balance
model for tropical montane species and found that leaf width was the
most important leaf morphological driver of species differences in the
leaf-to-air temperature differential. Multiple leaf traits can also be
combined into composite traits that characterize the dynamics of leaf
temperatures. For example, the thermal time constant (τ; s) quantifies
the thermal stability of a leaf, i.e. how rapidly leaf temperature
responds to temporal variation in microclimate (Michaletz et al .
2015, 2016). The low τ of relatively small and thin leaves indicates
that they heat up and cool down quickly, so that leaf temperatures
essentially track changes in microclimate variables, including very high
temperatures when in full sun. By contrast, leaves with a comparatively
large thermal mass and a high τ are buffered against fluctuations in
microclimate, so that leaf temperatures lag behind changes in
microclimate variables (Michaletz et al . 2015, 2016). Leaf
temperature can also be affected by transpirational cooling, especially
in hot and dry environments (Lin et al. 2017), and thus stomatal
conductance is another potentially relevant leaf trait. However, because
of the prevalence of mid-day stomatal depression (Zotz et al. 1995;
Goulden et al. 2004; Kosugi et al. 2008), the highest leaf temperatures
are experienced when stomata are closed, and maximum stomatal
conductance is therefore unlikely to distinguish maximum temperatures
across species. Furthermore, a sensitivity analysis revealed that
variation in stomatal conductance had virtually no effect on the thermal
time constant τ (Michaletz et al. 2016)
One would expect a strong selective advantage of high heat tolerance in
species that have traits that cause them to experience high maximum
temperatures. Indeed, heat tolerance scaled with maximum recorded leaf
temperatures in a botanical garden in Florida (Perez & Feeley 2020a).
High heat tolerance would likewise seem advantageous for species with
traits that result in high temperatures being maintained for long
periods of time. The rapid response to warming of low τ species should
predispose them to experiencing higher maximum temperatures, whereas the
slow cooling high τ species maintain high temperatures longer once they
are reached. The photosynthetic capacity of species with low τ peaks at
higher ambient temperatures than for species with high τ, suggesting
that species with low τ are better acclimated to higher temperatures
than high τ species (Michaletz et al . 2016). Whether low τ
species also have higher heat tolerances under field conditions has not
yet been tested.
Leaves that are structurally relatively costly to produce need to last
long enough for the plant to offset the investment, and therefore tend
to be better protected against biotic (Coley 1987) and abiotic stressors
(Nardini et al . 2012). Correspondingly, high heat tolerance of
such leaves would be expected. This has indeed been observed for plants
experiencing distinct temperature seasonality (e.g., Knight & Ackerly
2003; Sastry & Barua 2017), but whether this pattern is maintained in
more thermally stable ecosystems such as tropical forests remains to be
tested.
We measured leaf heat tolerance for 147 tropical species from lowland
and pre-montane forest sites in Panama and tested the following
hypotheses:
1) Heat tolerance will be greater in species growing in lowland than in
pre-montane sites, consistent with previously observed relationships
between heat tolerance and growth temperature. Based on previous
observations we expect this difference to be smaller than the difference
in growth temperature. Over a 20°C growing season temperature range from
the arctic to the tropics, mean heat tolerance increased by only 9°C
(O’Sullivan et al . 2017), and over a 17°C mean annual temperature
range across a tropical elevation gradient, Feeley et al . (2020a)
reported an increase in heat tolerance of less than 2°C. These
observations suggest that upper temperature thresholds are relatively
high in cool conditions and increase only moderately with growth
temperature.
2) Heat tolerance will be phylogenetically structured and lineages that
can be considered survivors of past hot epochs will have higher heat
tolerance than species or lineages that emerged later and are naïve to
such conditions.
3) Heat tolerance will increase with traits that enable leaves to reach
high temperature extremes, such that species that quickly heat up will
have higher heat tolerance than species that are more buffered against
high temperatures. This would be consistent with Perez & Feeley (2020a)
and with the higher temperature optimum for photosynthesis of low τ
species (Michaletz et al . 2016). Alternatively, heat tolerance
may be greater in thermally buffered species because they cool down more
slowly and thus maintain stable temperatures for longer. Heat tolerance
may differ with duration of exposure; when individual leaves are warmed
gradually over a wide temperature range (commonly by 1°C per minute)
heat tolerance is often relatively low, suggesting a negative effect of
the cumulative heat exposure (Krause et al. 2010). If the
negative impact of sustained high temperatures is greater than that of
higher, but shorter peak temperatures, heat tolerance might correlate
positively with τ across species.
4) Species that produce structurally expensive leaves will have higher
heat tolerance than species with ‘cheap’ leaves that can be readily
replaced. High investment in leaves that are relatively thick and dense
(high LMA), or with high leaf dry matter content (LDMC), is associated
with higher leaf longevity (Wright et al . 2004), and thus with
greater likelihood of the leaves experiencing temperature extremes
during their lifetime.