Martijn Slot

General patterns of acclimation of leaf respiration to elevated temperatures across biomes and plant types

Respiration is instrumental for survival and growth of plants, but increasing costs of maintenance processes with warming have the potential to change the balance between photosynthetic carbon uptake and respiratory carbon release from leaves. Climate warming may cause substantial increases of leaf respiratory carbon fluxes, which would further impact the carbon balance of terrestrial vegetation. However, downregulation of respiratory physiology via thermal acclimation may mitigate this impact. We have conducted a meta-analysis with data collected from 43 independent studies to assess quantitatively the thermal acclimation capacity of leaf dark respiration to warming of terrestrial plant species from across the globe. In total, 282 temperature contrasts were included in the meta-analysis, representing 103 species of forbs, graminoids, shrubs, trees and lianas native to arctic, boreal, temperate and tropical ecosystems. Acclimation to warming was found to decrease respiration at a set temperature in the majority of the observations, regardless of the biome of origin and growth form, but respiration was not completely homeostatic across temperatures in the majority of cases. Leaves that developed at a new temperature had a greater capacity for acclimation than those transferred to a new temperature. We conclude that leaf respiration of most terrestrial plants can acclimate to gradual warming, potentially reducing the magnitude of the positive feedback between climate and the carbon cycle in a warming world. More empirical data are, however, needed to improve our understanding of interspecific variation in thermal acclimation capacity, and to better predict patterns in respiratory carbon fluxes both within and across biomes in the face of ongoing global warming.

Thermal acclimation of leaf respiration of tropical trees and lianas: response to experimental canopy warming, and consequences for tropical forest carbon balance

Climate warming is expected to increase respiration rates of tropical forest trees and lianas, which may negatively affect the carbon balance of tropical forests. Thermal acclimation could mitigate the expected respiration increase, but the thermal acclimation potential of tropical forests remains largely unknown. In a tropical forest in Panama, we experimentally increased nighttime temperatures of upper canopy leaves of three tree and two liana species by on average 3 °C for 1 week, and quantified temperature responses of leaf dark respiration. Respiration at 25 °C (R25 ) decreased with increasing leaf temperature, but acclimation did not result in perfect homeostasis of respiration across temperatures. In contrast, Q10 of treatment and control leaves exhibited similarly high values (range 2.5-3.0) without evidence of acclimation. The decrease in R25 was not caused by respiratory substrate depletion, as warming did not reduce leaf carbohydrate concentration. To evaluate the wider implications of our experimental results, we simulated the carbon cycle of tropical latitudes (24°S-24°N) from 2000 to 2100 using a dynamic global vegetation model (LM3VN) modified to account for acclimation. Acclimation reduced the degree to which respiration increases with climate warming in the model relative to a no-acclimation scenario, leading to 21% greater increase in net primary productivity and 18% greater increase in biomass carbon storage over the 21st century. We conclude that leaf respiration of tropical forest plants can acclimate to nighttime warming, thereby reducing the magnitude of the positive feedback between climate change and the carbon cycle.

Global convergence in leaf respiration from estimates of thermal acclimation across time and space

Recent compilations of experimental and observational data have documented global temperature-dependent patterns of variation in leaf dark respiration (R), but it remains unclear whether local adjustments in respiration over time (through thermal acclimation) are consistent with the patterns in R found across geographical temperature gradients. We integrated results from two global empirical syntheses into a simple temperature-dependent respiration framework to compare the measured effects of respiration acclimation-over-time and variation-across-space to one another, and to a null model in which acclimation is ignored. Using these models, we projected the influence of thermal acclimation on: seasonal variation in R; spatial variation in mean annual R across a global temperature gradient; and future increases in R under climate change. The measured strength of acclimation-over-time produces differences in annual R across spatial temperature gradients that agree well with global variation-across-space. Our models further project that acclimation effects could potentially halve increases in R (compared with the null model) as the climate warms over the 21st Century. Convergence in global temperature-dependent patterns of R indicates that physiological adjustments arising from thermal acclimation are capable of explaining observed variation in leaf respiration at ambient growth temperatures across the globe.

Foliar respiration and its temperature sensitivity in trees and lianas: in situ measurements in the upper canopy of a tropical forest

Leaf dark respiration (R) and its temperature sensitivity are essential for efforts to model carbon fluxes in tropical forests under current and future temperature regimes, but insufficient data exist to generalize patterns of R in species-rich tropical forests. Here, we tested the hypothesis that R and its temperature sensitivity (expressed as Q10, the proportional increase in R with a 10 °C rise in temperature) vary in relation to leaf functional traits, and among plant functional types (PFTs). We conducted in situ measurements of R of 461 leaves of 26 species of tree and liana in the upper canopy of a tropical forest in Panama. A construction crane allowed repeated non-destructive access to measure leaves kept in the dark since the previous night and equilibrated to the ambient temperature of 23-31 °C in the morning. R at 25 °C (R25) varied among species (mean 1.11 μmol m(-2) s(-1); range 0.72-1.79 μmol m(-2) s(-1)) but did not differ significantly among PFTs. R25 correlated positively with photosynthetic capacity, leaf mass per unit area, concentrations of nitrogen and phosphorus, and negatively with leaf lifespan. Q10 estimated for each species was on average higher than the 2.0 often assumed in coupled climate-vegetation models (mean 2.19; range 1.24-3.66). Early-successional tree species had higher Q10 values than other functional types, but interspecific variation in Q10 values was not correlated with other leaf traits. Similarity in respiration characteristics across PFTs, and relatively strong correlations of R with other leaf functional traits offer potential for trait-based vegetation modeling in species-rich tropical forests.

Transient shade and drought have divergent impacts on the temperature sensitivity of dark respiration in leaves of Geum urbanum

The respiratory response of plants to temperature is a critical biotic feedback in the study of global climate change. Few studies, however, have investigated the effects of environmental stresses on the short-term temperature response of dark respiration (Rdark) at the leaf level. We investigated the effect of shade and transient drought on the temperature sensitivity (Q10; the proportional increase in respiration per 10°C increase in temperature) of Rdark of Geum urbanum L. in controlled experiments. Shade effects were most pronounced following sustained, near-darkness, when rates of leaf Rdark at a set measuring temperature (25°C) and the Q10 of Rdark were both reduced. By contrast, rates of leaf Rdark and the Q10 of Rdark both increased in response to the onset of severe water stress. Water stress was associated with a rapid (but reversible) decline in rates of light-saturated photosynthesis (Psat), stomatal closure (gs) and progressive wilting. Re-watering resulted in a rapid recovery of Psat, gs and a decline in the Q10 of Rdark (due to larger proportional reductions in the rate of Rdark measured at 25°C compared with those measured at 14°C). The concentration of soluble sugars in leaves did not decline during drought (5-7 day cycles) or shading, but during drought the starch concentration dropped, suggesting starch to sugar conversion helped to maintain homeostatic concentrations of soluble sugars. Thus, the drought and shade induced changes in Rdark were unlikely to be due to stress-induced changes in substrate supply. Collectively, the data highlight the dynamic responses of respiratory Q10 values to changes in water supply and sustained reductions in growth irradiance. If widespread, such changes in the Q10 of leaf respiration could have important implications for predicted rates of ecosystem carbon exchange in the future, particularly in areas that experience more frequent droughts.

Temperature response of CO2 exchange in three tropical tree species

Tropical forests play a critical role in the global carbon cycle, but our limited understanding of the physiological sensitivity of tropical forest trees to environmental factors complicates predictions of tropical carbon fluxes in a changing climate. We determined the short-term temperature response of leaf photosynthesis and respiration of seedlings of three tropical tree species from Panama. For one of the species net CO2 exchange was also measured in situ. Dark respiration of all species increased linearly - not exponentially - over a ~30°C temperature range. The early-successional species Ficus insipida Willd. and Ochroma pyramidale (Cav. ex Lam.) Urb. had higher temperature optima for photosynthesis (Topt) and higher photosynthesis rates at Topt than the late-successional species Calophyllum longifolium Willd. The decrease in photosynthesis above Topt could be assigned, in part, to observed temperature-stimulated photorespiration and decreasing stomatal conductance (gS), with unmeasured processes such as respiration in the light, Rubisco deactivation, and changing membrane properties probably playing important additional roles, particularly at very high temperatures. As temperature increased above Topt, gS of laboratory-measured leaves first decreased, followed by an increase at temperatures >40-45°C. In contrast, gS of canopy leaves of F. insipida in the field continued to decrease with increasing temperature, causing complete suppression of photosynthesis at ~45°C, whereas photosynthesis in the laboratory did not reach zero until leaf temperature was ~50°C. Models parameterised with laboratory-derived data should be validated against field observations when they are used to predict tropical forest carbon fluxes.

Trait‐based scaling of temperature‐dependent foliar respiration in a species‐rich tropical forest canopy

Summary 1. The scarcity of empirical data on leaf respiration (R) and its temperature sensitivity (e.g. Q10, defined as the proportional increase in R per 10 °C warming) causes uncertainty in current estimates of net primary productivity of tropical forests. 2. We measured temperature response curves of R on 123 upper-canopy leaves of 28 species of trees and lianas from a tropical forest in Panama and analysed variations in R and Q10 in relation to other leaf functional traits. 3. Respiration rates per leaf area at 25 ° C( RA) varied widely among species and were significantly higher in trees than in lianas. RA was best predicted by a multiple regression model containing leaf phosphorus concentration, photosynthetic capacity and leaf mass per area (r 2 =0 � 64). The mean Q10 value (2� 4) was significantly higher than the commonly assumed value of 2� 0. Q10 was best predicted by the combination of leaf carbohydrate concentration and growth form (trees vs lianas) (r 2 =0 � 26). 4. The night-time leaf respiratory carbon flux from this tropical forest was calculated from these multiple regression models to be 4� 5M g Ch a � 1 year � 1 , with an estimated additional 2� 9M g Ch a � 1 year � 1 being released by respiration during the day. 5. Trait-based modelling has potential for estimating R, thus facilitating carbon flux estimation in species-rich tropical forests. However, in contrast to global analyses, leaf phosphorus content was the most important correlate of R and not leaf nitrogen, so calibration of trait models to the tropics will be important. Leaf traits are poor predictors of Q10 values, and more empirical data on the temperature sensitivity of respiration are critically needed to further improve our ability to scale temperature-dependent respiration in species-rich tropical forests.

Photosynthetic acclimation to warming in tropical forest tree seedlings

Tropical forests have a mitigating effect on man-made climate change by acting as a carbon sink. For that effect to continue, tropical trees will have to acclimate to rising temperatures, but it is currently unknown whether they have this capacity. We grew seedlings of three tropical tree species over a range of temperature regimes (TGrowth = 25, 30, 35 °C) and measured the temperature response of photosynthetic CO2 uptake. All species showed signs of acclimation: the temperature-response curves shifted, such that the temperature at which photosynthesis peaked (TOpt) increased with increasing TGrowth. However, although TOpt shifted, it did not reach TGrowth at high temperature, and this difference between TOpt and TGrowth increased with increasing TGrowth, indicating that plants were operating at supra-optimal temperatures for photosynthesis when grown at high temperatures. The high-temperature CO2 compensation point did not increase with TGrowth. Hence, temperature-response curves narrowed with increasing TGrowth. TOpt correlated with the ratio of the RuBP regeneration capacity over the RuBP carboxylation capacity, suggesting that at high TGrowth photosynthetic electron transport rate associated with RuBP regeneration had greater control over net photosynthesis. The results show that although photosynthesis of tropical trees can acclimate to moderate warming, carbon gain decreases with more severe warming.

The Effects of Rising Temperature on the Ecophysiology of Tropical Forest Trees

The response of tropical trees to rising temperatures represents a key uncertainty that limits our ability to predict biosphere-atmosphere feedbacks in a warming world. We review the current understanding of temperature effects on the ecophysiology of tropical trees from organelle to biome level, where we distinguish between short-term responses, acclimation, and adaptation. We present new data on short-term temperature responses of photosynthesis and dark respiration, and temperature acclimation of photosynthesis. We also compare new field and laboratory-obtained photosynthesis-temperature response data. We identify several priority study areas. (1) Acclimation: We need to better understand photosynthetic acclimation, for example to determine whether the adjustment of the thermal optimum of photosynthesis (TOpt) is consistently negated by a decrease in photosynthesis at TOpt, as we observed. (2) Growth: Whereas tropical seedlings may grow better with warming, canopy trees reportedly grow worse; we do not currently know what explains these contrasting temperature effects. (3) Reproduction: Tropical trees may be close to reproductive temperature thresholds, as heat sterility in crops occurs in the upper 30 °C range. Nonetheless, the temperature sensitivity of tropical tree reproduction is virtually unstudied. (4) Mortality: How does heat-induced atmospheric drought (high leaf-to-air vapor pressure deficit) affect tropical tree mortality? (5) Stomatal behavior: What is the specific role of temperature in the induction of midday-stomtal closure on sunny days? Better knowledge in these areas will improve our ability to predict carbon fluxes in tropical forests experiencing ongoing warming.

Influence of arbuscular mycorrhizal colonization on whole‐plant respiration and thermal acclimation of tropical tree seedlings

Abstract Symbiotic arbuscular mycorrhizal fungi (AMF) are ubiquitous in tropical forests. AMF play a role in the forest carbon cycle because they can increase nutrient acquisition and biomass of host plants, but also incur a carbon cost to the plant. Through their interactions with their host plants they have the potential to affect how plants respond to environmental perturbation such as global warming. Our objective was to experimentally determine how plant respiration rates and responses to warmer environment are affected by AMF colonization in seedlings of five tropical tree species at the whole plant level. We evaluated the interaction between AMF colonization and temperature on plant respiration against four possible outcomes; acclimation does or does not occur regardless of AMF, or AMF can increase or decrease respiratory acclimation. Seedlings were inoculated with AMF spores or sterilized inoculum and grown at ambient or elevated nighttime temperature. We measured whole plant and belowground respiration rates, as well as plant growth and biomass allocation. There was an overall increase in whole plant, root, and shoot respiration rate with AMF colonization, whereas temperature acclimation varied among species, showing support for three of the four possible responses. The influence of AMF colonization on growth and allocation also varied among plant species. This study shows that the effect of AMF colonization on acclimation differs among plant species. Given the cosmopolitan nature of AMF and the importance of plant acclimation for predicting climate feedbacks a better understanding of the patterns and mechanisms of acclimation is essential for improving predictions of how climate warming may influence vegetation feedbacks.