Optimum air temperature for tropical forest photosynthesis: mechanisms involved and implications for climate warming (2024)

Tropical forests are characterized by a warm and humid climate (Corlett 2011); however, there is currently little consensus on whether climate change will affect tropical forests. Paleoecological studies show that neotropical vegetation largely persisted after a 3 to 5 °C warming during the Paleocene–Eocene Thermal Maximum (Jaramillo et al 2010). However, this historical warming was short-lived and considerably slower than current warming and future warming predicted for the next century. A survey of the temperatures of broad-leaved forest land cover suggests that climatic warming could have severe consequences for tropical floras (Wright et al 2009). Closed-canopy forests are found in areas with a mean annual temperature below 28 °C, whereas areas with mean temperatures above 28 °C support shrubs and grasses instead of broad-leaved evergreen trees. Given that excessively high temperatures are typically associated with a high evaporative demand and dry climate, the absence of closed-canopy forests in areas with temperatures above 28 °C could also be a consequence of water limitation. This past record and the distribution of tropical forests suggest a temperature limit, and therefore the ecosystem sensitivity to this threshold needs to be further studied.

Photosynthetic performance, the basis for carbon sequestration and ecosystem production, is temperature dependent. In general, the light-saturated photosynthetic rate increases with temperature to a peak, which is followed by a decline (Sage and Kubien 2007). It has been suggested that current temperatures in regions supporting tropical forests are very close to or even exceed their photosynthetic optimum temperature (T_opt) (Doughty and Goulden 2008). This is a potentially ominous warning sign for our warming Earth. Tropical forests store large amounts of carbon in biomass (Dixon et al 1994). Consequently, a slight perturbation in tropical carbon fluxes could have wide-ranging effects on global atmospheric CO₂ concentrations (Anderegg et al 2015). Temperatures in excess of T_opt could result in a sharp decline in photosynthetic carbon sequestration in tropical forests (Doughty and Goulden 2008, Vårhammar et al 2015). A decline in CO₂ uptake by the forests could in turn result in an increase in atmospheric CO₂, which would further accelerate warming through positive feedback.

Model simulations indicate that tropical forests are currently not at their high-temperature threshold. With the aid of widely-used process models, Lloyd and Farquhar (2008) showed that the temperature of tropical forests was still well below T_opt. They argue that the apparent decrease in photosynthetic rate with increasing temperature is predominantly an indirect effect of stomatal closure (30%) and not a direct effect of warming on mesophyll processes (2%). Temperature increases could reduce photosynthesis, either directly through inhibiting the activity of photosynthetic enzymes and electron transport, or indirectly through decreasing stomatal conductance (Farquhar et al 1980). A linear increase in temperature could lead to an exponential growth of water vapour pressure deficit (D) (Campbell and Norman 1998), whereas stomatal aperture (conductance) decreases with increased D (Damour et al 2010). Since CO₂ enters the mesophyll through stomata, intercellular CO₂ (c_i) and photosynthesis decrease when stomatal conductance (g) declines (Farquhar et al 1980). In contrast to the direct effects of temperature on the photosynthetic apparatus, a reduction in photosynthesis caused by increased stomatal resistance could be offset, at least partly, by elevated CO₂ (Lloyd and Farquhar 2008). Elevated CO₂ increases T_opt by reducing photorespiration and stomatal resistance, which has a positive effect on the acclimation potential of photosynthesis. Moreover, stomatal closure reduces transpiration and subsequently reduces its cooling effect (Doughty 2011). This could in turn lead to excessively high temperatures at the leaf level, which could cause irreversible damage to the photosynthetic machinery (Berry and Björkman 1980, Doughty 2011).

In this study, to examine the potential effects of climate change on forest photosynthesis, we first quantified the T_opt of ecosystem photosynthesis (T_optE) for seven tropical forests across different continents. We then analyzed the relationship between T_optE and mean growing season air temperature (T_a) to confirm the widely held consensus that these parameters increase simultaneously. Ecosystem physiological parameters were then inverted using a big-leaf analogized process model driven by ecosystem photosynthesis measurements. Further, we tested the hypothesis proposed by Lloyd and Farquhar (2008), which suggests that stomatal processes play a prominent role in determining T_opt, and that increasing ambient CO₂ concentrations will increase tropical forest T_opt, which would imply that these forest are not as vulnerable to climate change as may have been indicated by Doughty and Goulden (2008). Finally, we discuss the implications of different climate warming scenarios on ecosystem photosynthesis in tropical forests.

Studied sites

Eddy flux observations and data processing

Determining the optimum temperature (T_opt) of photosynthesis

The Farquhar–von Caemmerer–Berry (FvCB) model

A process-based photosynthesis model was used in this study. The model is a combination of the Farquhar–von Caemmerer–Berry photosynthesis (FvCB) model (Farquhar et al 1980) and the Ball–Berry stomatal conductance model (Ball et al 1987), with some additional parameterization information provided by von Caemmerer et al (2009). The detailed model equations are listed in table A1 in the appendix. We used an iteration method to solve intercellular CO₂ (c_i). The model was coded in the C++ environment and is available upon request.

The big-leaf analogy

The T_optE of tropical forests

The goodness-of-fit was shown in figure 3 when implemented the FvCB model to these datasets. In general, the model fitted results have a good relationship with that of observations. It suggests high reliability of these inverted parameters (table 3). Principal component analysis of these parameters identified three components that could explain over 86% of the variance. However, none of the three components were significantly correlated with T_optE (data not shown). A further correlation analysis showed that the activation energy of ecosystem respiration (R_E) was the only parameter significantly correlated with T_optE (figure 4(a)). We found that two sites (PDF and MKL indicated by open circles in figure 4(b)) differ from the remaining sites with respect to the relationship between T_optE and stomatal sensitivity (g_1E): with the exception of PDF and MKL, the sites show a negative correlation between T_optE and g_1E. These two excluded sites have special water conditions which discussed latter in the discussion section.

The PSO site, which has eight years' continuous flux data, was taken as an example of per-humid site to illustrate the contribution of stomatal processes in determine T_optE. The overall T_optE for the PSO site was 26.5 °C for the entire D_E range, as shown by the dashed line in figure 5(a) When the whole dataset was divided into different D_E levels, we found that the light-saturated photosynthesis rate (N_EEsat) increased with T_a even at values greater than 30 °C (see data points and regression line in different colours, figure 5(a). Only at the highest D_E level was NEE_sat found to decrease with T_a. In this regard, T_optE (when NEE_sat starts to decrease with an increase in T_a) should at least be 30 °C when D_E is controlled. This contrasts with the value of 26.5 °C obtained using the full D_E range and implies strong stomatal control of T_optE. We also inferred parameters of FvCB model for all D_E sub-ranges (table 4). Most of these parameters showed a unimodal pattern along with increase of D_E. A similar case was found in a site with strongly seasonal climate (figure 5(b)).

Our cross-site analysis shows that tropical forests growing in a warmer climate tend to exhibit higher T_optE (figure 2(a)). We separated the contributions of biochemical, respiratory, and stomatal processes to T_optE by means of parameter inversions. Respiratory process play a role in T_optE, as suggested by the significant relationship between T_optE and the activation energy (E_a) of respiration (R_E) (figure 4(a)). This finding differs from those of leaf level studies, which indicate that leaf respiration plays a negligible role in T_optL (Lin et al 2012). At the ecosystem level, R_E is the sum of the autotrophic respiration of all organisms (above- and below-ground) and heterotrophic respiration of soil organic matter and litter. At the leaf-level, however, R_L reflects only leaf respiration, which typically represents a small fraction of net photosynthesis. These differences emphasize the importance of respiratory processes in studying T_optE at the ecosystem level, even though it is negligible at the leaf level.

It is known that activation energy (E_a) can represent the temperature sensitivity (Q₁₀) of R_E, the relationship of which can be expressed as follows:

The relationship between decreasing T_optE and increasing Q₁₀ suggests that the R_E of tropical forests with higher T_optE and mean T_a is less sensitive to T_a variations than forests with lower T_optE. This is consistent with previous reports showing that Q₁₀ decreases with rising temperature, as a consequence of thermal acclimation (Tjoelker et al 2009, Slot and Kitajima 2015).

When we excluded PDF and MKL (two secondary forests with unique hydrological conditions) from the analysis, we identified a strong correlation between g_1E and T_optE(figure 4(b)). The forest in the PDF site is drained peat swamp forest (Hirano et al 2007), which is generally waterlogged. By contrast, the MKL site experiences seasonal water deficits (Gamo et al 2005). Since stomatal conductance or g_1E is highly sensitive to water availability, it seems appropriate to treat these two secondary forests as outliers when investigating T_optE–g_1E relationships.

Theoretically, g_1E, which is a stomatal sensitivity factor, would be expected to increase with increasing growth temperature, as does T_optE (Leuning 1990, Medlyn et al 2011). Our numeric simulation also supports this theoretic expectation for a specific site by checking T_optE with varied g_1E (data not shown). Nevertheless, we found that at the ecosystem level for tropical forests, T_optE tends to decrease with increasing g_1E (figure 4(b)). Since g_1E is strongly correlated with the E_a of R_E (Pearson's r = 0.96), it is would be difficult to state that the strong correlation shown in figure 4(b) is solely attributable to g_1E or whether it is merely an indirect reflection of the E_a–T_optE relationship shown in figure 4(a). In situ warming experiments at both leaf and ecosystem levels might be helpful in reconciling these contrasts (Cavaleri et al 2015).

Interestingly, we found that biochemical processes did not play a significant role in T_optE changes across sites. Traditionally, T_opt acclimation studies have primarily focused on biochemical processes (Hikosaka et al 2006). However, in the present study these key processes were found to make a negligible contribution to T_optE changes across sites. Subsequent to further confirmation that thermal acclimation of respiration rather than biochemical processes is a more important determinant of T_optE, these findings should be implemented in global change models (Lombardozzi et al 2015).

Previous studies have shown that stomatal processes are potentially important (Lin et al 2012, Duursma et al 2014, Slot and Winter 2017), or even the most important factors determining T_optL (Lloyd and Farquhar 2008, Rowland et al 2015). Nevertheless, how stomatal processes control T_opt is still not well understood. This uncertainty is partly caused by the confounding effects of temperature and water factors on T_opt.

Relative humidity (h_s) and vapour pressure deficit (D) are strongly dependent on temperature (Campbell and Norman 1998). When temperature rises, the saturated water vapour pressure will increase exponentially. This, in turn, will alter both h_s and D, and hence stomatal conductance. Therefore, there is an indirect effect of temperature on T_opt through its effect on stomatal conductance. This effect is illustrated in figure 5. The dashed line in figure 5(a) shows the temperature response curve represented in figure 1(f) under the full D_E range. However, when we divided the whole dataset into different D_E levels (as shown by the different colours in figure 5(a)), it was apparent that N_EEsat increases with temperature within these subsets until the temperature exceed 30 °C . This indicates that the T_optE should be at least 30 °C if there is no D_E limitation on the stomatal response, which is considerably higher than the value estimated from the entire D_E range (26.4 °C). This analysis lends support to the idea that stomatal processes play a significant role in determining T_optE, as temperature may indirectly influence photosynthesis through changing D.

In the future, the Earth's surface air is predicted to become richer in CO₂ and higher in mean temperature (Corlett 2011). At present, however, there seems little consensus on how tropical forest ecosystem will respond under such a climatic scenario (see the review by Lloyd and Farquhar (2008)). Our findings, however, provide certain insights into how tropical forest ecosystems might respond and could serve as complement to previous studies in our pursuit of a more complete understanding future changes in forest photosynthesis.

Firstly, we revealed the role of stomatal limitation in determining T_optE at the ecosystem level, which is largely consistent with leaf-level findings. The role of stomatal effects in shaping T_optL have been well demonstrated in leaf-level measurements (Koch et al 1994, Ishida et al 1996, Carswell et al 2000, Slot and Winter 2017) and have been verified by a leaf-level model (Lloyd and Farquhar 2008). Our ecosystem flux analysis showed that without D_E limitation on stomatal conductance, tropical forests could have a higher photosynthetic performance (N_EEsat) under high T_a, as indicated by their increased T_optE (figure 5). The direct implication of this finding is that factors affecting stomatal conductance will contribute substantially to the modification of T_optE. Among these factors, the most prominent is ambient air CO₂ concentration. Given unchanged moisture conditions (e.g. soil water or D), T_optE is expected to increase with CO₂ and will decrease stomatal limitation on photosynthesis (Lloyd and Farquhar 2008). Accordingly, this can be considered as a positive signal for tropical forests given the prospect of increasing CO₂ levels.

Secondly, tropical forests in environments with higher T_a tend to have higher T_optE (figure 2), which is consistent with growth chamber cultivation experiments (Kositsup et al 2009) and cross-season observations (Lange et al 1974). This pattern suggests potential acclimation of tropical forests to T_a, which is a further adaptive strategy that will increase the resilience of tropical forest given the predicted climate warming scenarios.

Thirdly, the significant relationship between the activation energy of respiration and T_optE implies the possible thermal acclimation of R_E (figure 4(a)). The temperature acclimation of ecosystem respiration, i.e. the decrease in the sensitivity of respiration to temperature changes as growth temperature increases, would have a positive effect on net photosynthesis and lead to increases in T_optE.

Collectively, our findings indicate an optimistic future for tropical forests under the predicted conditions of global climate change. Nevertheless, some uncertainties remain. Firstly, increasing CO₂ will reduce stomatal conductance and water losses and hence the cooling effect of transpiration. This could potentially result in excessively high leaf temperatures and consequently heat damage and declines in photosynthesis and carbon sequestration. Furthermore, because ecosystem respiration in the tropics and subtropics is generally more sensitive to warming than that of photosynthesis (Yi et al 2010, Zhang et al 2016), it remains unclear to what extent the warming-induced increase in night-time ecosystem respiration would offset the positive effect of thermal acclimation in photosynthesis on net carbon sequestration.