1 | INTRODUCTION
Tropical forest species are believed to be particularly sensitive to
global warming, as they are adapted to conditions of limited seasonal
temperature variation. Furthermore, temperatures in the lowland tropics
are already the highest known to support closed-canopy forest, and
distances to cooler refugial areas can be large (Wright, Muller-Landau
& Schipper 2009). Tropical species will therefore need to acclimate to
changing conditions for tropical forests to continue to have a
mitigating effect on anthropogenic climate change.
Despite millions of years of thermal stability in the tropics, tropical
trees have the capacity to acclimate to warming. For example,
experimental nighttime warming results in down-regulation of respiratory
carbon loss from leaves (Cheesman & Winter 2013; Slot et al. 2014; Slot
& Winter 2017a, 2018), consistent with thermal acclimation (Atkin &
Tjoelker 2003); under elevated growth temperature the optimum
temperature for photosynthetic carbon uptake shifts towards the new,
higher growth temperature (Kotisup et al. 2009; Slot & Winter 2017a);
and growth rates do not necessarily decrease under either nighttime
warming or daytime warming (Cheesman & Winter 2013; Scafaro et al.
2017; Slot & Winter 2018). Thus, despite differences among species, the
comparative thermal stability of the tropics has not deprived tropical
species of the physiological plasticity that enables them to acclimate
to moderate warming.
As plants are confronted
with rising temperatures, atmospheric CO2 concentrations
([CO2]atm) are also increasing, and
in the short term this has both direct and indirect effects on
photosynthetic carbon uptake and its response to temperature.
CO2 as the substrate for photosynthesis directly
stimulates rates of carbon uptake. Higher
[CO2]atm also suppresses carbon loss
associated with photorespiration, the result of oxygenation of Rubisco
(e.g., Long Ainsworth, Rogers & Ort. 2004; Ainsworth & Rogers 2007).
Photorespiration increases with temperature, so when photorespiration is
suppressed by elevated [CO2]atmplants can achieve a higher optimum temperature of photosynthesis than
at ambient [CO2]atm (Berry &
Björkman 1980; Long 1991). The decrease in Rubisco limitation of
photosynthesis under elevated CO2 conditions means that
net photosynthesis is increasingly limited by the maximum photosynthetic
electron transport rate (JMax), reflecting the maximum
rate of ribulose 1,5-bisphosphate (RuBP) regeneration (Sage & Kubien
2007). This affects the temperature response of net photosynthesis
because electron transport limited-photosynthesis has a higher
temperature optimum than Rubisco limited photosynthesis (Sage & Kubien
2007; Hikosaka, Ishikawa, Borjigidai, Muller & Onoda 2006). In the long
term, elevated [CO2]atm may cause a
reduction in both the maximum capacity of RuBP carboxylation
(VCMax) and RuBP regeneration (JMax).
VCMax might decrease as a result of lower investment in
Rubisco when high [CO2]atm reduces
carbon limitation of photosynthesis and optimization requires
proportionally greater investment in electron transport (Ainsworth &
Rogers 2007). VCMax and JMax might also
decrease if leaf nitrogen (N) concentrations decrease (Medlyn et al.
1999) as a result of N dilution by rapid growth (Luo, Field & Mooney
1994), or as a result of progressive soil N limitation (Luo et al. 2004;
Warren, Jensen, Medlyn, Norby & Tissue 2015). Changes in leaf N in
plants grown at elevated CO2 could directly affect the
thermal acclimation capacity of plants, as there appears to be an
important role for N allocation to Rubisco—an N-rich enzyme—during
acclimation to warming (Scafaro et al. 2017).
To assess thermal acclimation of
photosynthesis, the short-term temperature response of the
photosynthetic parameters is compared between warmed and control plants.
Berry & Björkman (1980), summarizing previous research, showed that
photosynthesis peaked at higher temperatures in plants acclimated to
warmer conditions than in cool grown plants. A recent global
meta-analysis showed that across sites, the optimum temperature for net
photosynthesis (TOpt) scaled with growth temperature,
and this pattern could be explained by thermal acclimation;
adaptation—expressed as inherent differences based on source
populations—was of lesser importance (Kumarathunge et al. 2019),
stressing the importance of physiological plasticity. A shift in the
optimum temperature (TOpt) towards higher values may or
may not be accompanied by increases in POpt, the rate of
photosynthesis at TOpt (Berry & Björkman 1980; Way &
Yamori 2014; Slot, Garcia & Winter 2016).
Vegetation models are highly
sensitive to the formulation of temperature responses (Booth et al.
2012). To inform such models about acclimation, temperature response
parameters of VCMax and JMax are
required, their activation energies, de- activation energies, entropy
factors (ΔS, sensu Medlyn et al. 2002), and their temperature optima
(Stinziano, Way & Bauerle 2018; Mercado et al. 2018). Because of the
inherent non-linearity of temperature responses and Jensen’s inequality,
implementation of acclimation parameters would be most meaningful if the
parameterization reflected the true diversity of these parameter values,
rather than single averages.
Acclimation processes are currently not well represented in most dynamic
global vegetation models and earth system models (Smith & Dukes, 2013;
Smith, Malyshev, Shevliakova, Kattge & Dukes. 2016; Lombardozzi, Bonan,
Smith, Dukes & Fisher. 2015; Mercado et al. 2018), and limited
experimental data is available on the combined effects of warming and
elevated [CO2] that can provide mechanistic
foundations for modeling acclimation (Way, Oren & Kroner 2015),
particularly for tropical plants. To address thermal acclimation of
photosynthesis several modeling studies have capitalized on the clear
trend of a decreasing JMax/VCMax ratio
with acclimation to higher growth temperatures, as synthesized by Kattge
& Knorr (2007), and more recently confirmed by Smith & Dukes (2018)
(e.g., Lombardozzi et al. 2015; Smith et al. 2016; Mercado et al. 2018).
However, [CO2]atm may affect the
JMax/VCMax ratio independent of
temperature. While acclimation to warming consistently decreases the
JMax/VCMax ratio, increased
[CO2]atm may either increase the
ratio (e.g. meta-analysis by Ainsworth & Rogers 2007), or not affect it
(e.g., meta-analysis by Medlyn et al. 1999).
These differences may be related
to nutrient supply and /or to source-sink relationships (Arp 1991; Sage
1994), as nutrient- or sink limitation may cause proportionally greater
reduction in VCMax. Fauset et al. (2019) found that the
JMax/VCMax ratio of the tropical tree
species Alchornea glandulosa decreased with increasing growth
temperature, but increased with elevated [CO2], such
that JMax/VCMax for 800 ppm
CO2 was higher at 35°C than that of control plants at
30°C. The same pattern of opposing effects of warming and elevated
CO2 on JMax/VCMax was
found in the boreal tree species Larix laricina , and to a lesser
extent in Picea mariana (Dusenge et al. 2020). The utility of
JMax/VCMax changes to model acclimation
may thus be limited when both temperature and CO2increase, and additional information on photosynthetic parameters is
needed.
The short-term temperature
response of net photosynthesis can be controlled by different factors,
including the temperature sensitivities of VCMax,
JMax, and respiration in the light, and by stomatal
conductance (Lin, Medlyn & Ellsworth 2012). We have shown that the
temperature response of net photosynthesis of field-grown lowland
tropical trees is largely controlled by decreases in stomatal
conductance as the leaf-to-air vapor pressure deficit (VPD) increases
with increasing measurement temperature (Slot & Winter 2017b, 2017c;
Hernández, Winter & Slot2020; see also Smith et al. 2020), whereas
Vårhammer et al. (2015) reported significant limitations by
JMax in tropical montane species in Rwanda. Growth at
elevated CO2 generally results in decreases in stomatal
conductance (Saxe, Ellsworth, & Heath 1998; Ainsworth & Rogers 2007),
potentially increasing stomatal control over net photosynthesis.
However, upregulation of stomatal conductance at a given VPD during
acclimation to elevated temperature and VPD has also been observed in
some species (Marchin, Broadhead, Bostic, Dunn & Hoffmann 2016; Wu et
al. 2018; Dusenge, Madhavji & Way 2020).
Knowing which process limits
photosynthetic carbon fixation is important to inform vegetation models
and to better predict how environmental change will impact
photosynthetic carbon uptake of tropical forest trees.
Here we report on an experiment with neotropical tree speciesTabebuia rosea , grown under combined warming and elevated
CO2 conditions. We evaluated the capacity for
acclimation of photosynthesis and respiration. Specifically, we examine
leaves developed under treatment conditions (“long-term acclimation”),
and of pre-existing leaves of plants transferred from control to
treatment conditions and vice versa (“short-term acclimation”). We
hypothesized that (i) acclimation would result in higher temperature
optima for photosynthetic parameters, and in lower respiration rates at
a set temperature; (ii) long-term acclimation (of newly-developed
leaves) would be stronger than short-term acclimation (of pre-existing
leaves); and (iii) stomatal limitation of photosynthesis would increase
under treatment conditions of warming and elevated CO2.
Nonlinear models characterizing the temperature responses for each
treatment were fitted using a probabilistic Bayesian approach. This
approach enabled us to present the parameters of interest in the form of
a probability distribution of values, to better reflect the range of
potential parameter values.