Unexpected Large Photosynthetic Thermal Plasticity of Montane Andean Trees

Abstract

Tropical forests play a significant role in global carbon sequestration. However, our understanding of how tropical tree species adjust to climate warming remains limited to studies on seedlings grown in pots and highly controlled growth conditions. To reduce this knowledge gap, we used a field experiment with 5-year-old juvenile trees of 12 naturally co-occurring dominant tropical Andean montane and lowland species growing in three common gardens established along a natural thermosequence in the tropical Andes. Based on a few previous studies, we hypothesized that montane species would exhibit a weaker photosynthetic thermal acclimation capacity compared to lowland counterparts. Our results showed that montane tree species can thermally acclimate net photosynthesis by shifting their thermal optimum (T_opt) by 0.6°C per 1°C of warming. This strong shift in T_opt was correlated to simultaneous strong shifts in T_opt of apparent photosynthetic capacity parameters (V_cmax and J_max), which increased by 0.7°C per 1°C of warming. This strong thermal acclimation resulted in similar rates of net CO₂ assimilation between montane and lowland species across different thermal environments. At last, rates of net photosynthesis at growth temperature explained 30% of the variation in the relative tree growth rates across the two species groups and thermal environments. Our results suggest that the strong physiological acclimation of photosynthesis to warming among montane Andean tree species should be considered when predicting future impacts of warming on Andean plant communities.

Keywords: Vcmax and Jmax; acclimation; climate change; photosynthesis; tropical montane forests.

FIGURE 1

Conceptual figure of a constructive adjustment of net photosynthesis in response to increasing growth temperature. (a) Key parameters that are used to examine the thermal adjustment of net photosynthesis are shown, including net photosynthesis at growth temperature (A _growth), the thermal optimum of net photosynthesis (T _optA), the b parameter, which represents the breadth of the temperature response of net photosynthesis, and the high‐temperature CO₂ compensation point (T _max). (b) Hypothesized responses of a constructive adjustment of net photosynthesis in response to warming in which, simultaneously, the T _optA and T _max shift to higher leaf temperatures and A _growth is either maintained or increased with an increase in growth temperature. This figure assumes that the breadth of the curve is not altered by growth temperature. Redrawn from Way and Yamori (2014).

FIGURE 2

Temperature responses of net photosynthesis. Panels (a–c) represent the temperature response of net photosynthesis for montane (a), lowland native at the 22°C site (b), and lowland native at the 26°C site (c). Colors represent mean annual temperature at experiment sites (14°C = blue; 22°C = orange; 26°C = red). Each data point represents the mean value (mean ± SE) of all biologically independent trees across all species at each leaf temperature, group, and site (Montane: N = 15–18 trees; Lowland 22°C: N = 5–8 trees; Lowland 26°C: N = 4–6 trees). The data were fitted with the Equation (2). Panels (d, e) represent the optimum temperature of net photosynthesis (T _optA, °C) at different sites for montane (d) and lowland (e) tree species, respectively. The x axis represents each site's mean annual temperature: 14°C, 22°C, and 26°C (Table S1). ‘Home’ indicates the native thermal environment for each species group (14°C for montane; 22°C–26°C for lowland), and arrows indicate whether species were subjected to warming or cooling. The solid and dashed bars in (e) represent lowland species originating from the 22°C and 26°C sites, respectively. Small letters are used for statistical comparisons among each species group and site combination, where a different letter denotes a significant difference at the p < 0.05 threshold from Sidak posthoc test. Further details on statistical analyses for this figure can be found in Table 1.

FIGURE 3

Key temperature sensitivity parameters of net photosynthesis. The impact of growth temperature on the b parameter that represents the breadth of the temperature response curve of net photosynthesis measured at ambient CO₂ concentration in montane (a) and lowland (b) tree species. The impact of growth temperature on the upper leaf temperature at which net photosynthesis rates measured at ambient CO₂ are zero (T _max, °C) in montane (c) and lowland (d) tree species. The x axis represents each site's mean annual temperature: 14°C, 22°C, and 26°C (Table S1). ‘Home’ indicates the native thermal environment for each species group (14°C for montane; 22°C–26°C for lowland), and arrows indicate if they were subjected to warming or cooling. The solid and dashed bars in (b, d) represent lowland species originating from the 22°C and 26°C sites, respectively. Small letters are used for statistical comparisons among each species group and site combination, where a different letter denotes a significant difference at the p < 0.05 threshold from Sidak posthoc test. Further details on statistical analyses for this figure can be found in Table 1.

FIGURE 4

Net photosynthetic rates at growth temperature. The impact of growth temperature on the rates of net photosynthesis measured at ambient CO₂ and prevailing growth temperature (A _growth, μmol m⁻² s⁻¹) in (a) montane and (b) lowland tree species. The x axis represents each site's mean annual temperature: 14°C, 22°C, and 26°C (Table S1). However, estimation of A _growth rates was done using mean daytime (6 a.m.–6 p.m.) growth temperature (14°C site = 21.4°C, 22°C site = 24.3°C, and 26°C = 31.2°C) of 1 month prior to each measurement campaign at each site, the time defined as the thermal acclimation period of photosynthesis. “Home” indicates the native thermal environment for each species group (14°C for montane; 22°C–26°C for lowland), and arrows indicate if they were subjected to warming or cooling. The solid and dashed bars in (b) represent lowland species originating from the 22°C and 26°C sites, respectively. Small letters are used for statistical comparisons among each species group and site combination, where a different letter denotes a significant difference at the p < 0.05 threshold from Sidak posthoc test. Further details on statistical analyses for this figure can be found in Table 1.

FIGURE 5

Relationship of net photosynthesis and relative growth rates. The relative growth rate (RGR, mm mm⁻¹ year⁻¹) as a function of rates of net photosynthesis measured at ambient CO₂ and growth temperature (A _growth, μmol m⁻² s⁻¹). Colors represent mean annual temperature of experiment sites (14°C = blue; 22°C = orange; 26°C = red). A simple linear regression model was used to analyse the relationship between these two variables across species and groups. Each data point represents each species mean. The statistical test was one‐sided since it was done to evaluate whether there is a positive relationship between the two variables. The solid black line represents the regression line, and the light gray area represent 95% confidence interval around the regression line.