Plasticity and implications of water-use traits in contrasting tropical tree species under climate change.

Plants face a trade-off between hydraulic safety and growth, leading to a range of water-use strategies in different species. However, little is known about such strategies in tropical trees and whether different water-use traits can acclimate to warming. We studied five water-use traits in 20 tropical tree species grown at three different altitudes in Rwanda (RwandaTREE): stomatal conductance (gs), leaf minimum conductance (gmin), plant hydraulic conductance (Kplant), leaf osmotic potential (ψo) and net defoliation during drought. We also explored the links between these traits and growth and mortality data. Late successional (LS) species had low Kplant, gs and gmin and, thus, low water loss, while low ψo helped improve leaf water status during drought. Early successional (ES) species, on the contrary, used more water during both moist and dry conditions and exhibited pronounced drought defoliation. The ES strategy was associated with lower mortality and more pronounced growth enhancement at the warmer sites compared to LS species. While Kplant and gmin showed downward acclimation in warmer climates, ψo did not acclimate and gs measured at prevailing temperature did not change. Due to distinctly different water use strategies between successional groups, ES species may be better equipped for a warmer climate as long as defoliation can bridge drought periods.

Contrasting warming responses of photosynthesis in early- and late-successional tropical trees.

The productivity and climate feedbacks of tropical forests depend on tree physiological responses to warmer and, over large areas, seasonally drier conditions. However, knowledge regarding such responses is limited due to data scarcity. We studied the impact of growth temperature on net photosynthesis (An), maximum rates of Rubisco carboxylation at 25 °C (Vcmax25), stomatal conductance (gs) and the slope parameter of the stomatal conductance-photosynthesis model (g1), in 10 early successional (ES) and 8 late-successional (LS) tropical tree species grown at three sites along an elevation gradient in Rwanda, differing by 6.8 °C in daytime ambient air temperature. The effect of seasonal drought on An was also investigated. We found that warm climate decreased wet-season An in LS species, but not in ES species. Values of Vcmax25 were lower at the warmest site across both successional groups, and An and Vcmax25 were higher in ES compared with LS species. Stomatal conductance exhibited no significant site differences and g1 was similar across both sites and successional groups. Drought strongly reduced An at warmer sites but not at the coolest montane site and this response was similar in both ES and LS species. Our results suggest that warming has negative effects on leaf-level photosynthesis in LS species, while both LS and ES species suffer photosynthesis declines in a warmer climate with more pronounced droughts. The contrasting responses of An between successional groups may lead to shifts in species' competitive balance in a warmer world, to the disadvantage of LS trees.

Acclimation of photosynthetic capacity and foliar respiration in Andean tree species to temperature change.

Climate warming is causing compositional changes in Andean tropical montane forests (TMFs). These shifts are hypothesised to result from differential responses to warming of cold- and warm-affiliated species, with the former experiencing mortality and the latter migrating upslope. The thermal acclimation potential of Andean TMFs remains unknown. Along a 2000 m Andean altitudinal gradient, we planted individuals of cold- and warm-affiliated species (under common soil and irrigation), exposing them to the hot and cold extremes of their thermal niches, respectively. We measured the response of net photosynthesis (Anet ), photosynthetic capacity and leaf dark respiration (Rdark ) to warming/cooling, 5 months after planting. In all species, Anet and photosynthetic capacity at 25°C were highest when growing at growth temperatures (Tg ) closest to their thermal means, declining with warming and cooling in cold-affiliated and warm-affiliated species, respectively. When expressed at Tg , photosynthetic capacity and Rdark remained unchanged in cold-affiliated species, but the latter decreased in warm-affiliated counterparts. Rdark at 25°C increased with temperature in all species, but remained unchanged when expressed at Tg . Both species groups acclimated to temperature, but only warm-affiliated species decreased Rdark to photosynthetic capacity ratio at Tg as temperature increased. This could confer them a competitive advantage under future warming.

Variations in leaf anatomical characteristics drive the decrease of mesophyll conductance in poplar under elevated ozone.

Decline in mesophyll conductance (gm ) plays a key role in limiting photosynthesis in plants exposed to elevated ozone (O3 ). Leaf anatomical traits are known to influence gm , but the potential effects of O3 -induced changes in leaf anatomy on gm have not yet been clarified. Here, two poplar clones were exposed to elevated O3 . The effects of O3 on the photosynthetic capacity and anatomical characteristics were assessed to investigate the leaf anatomical properties that potentially affect gm . We also conducted global meta-analysis to explore the general response patterns of gm and leaf anatomy to O3 exposure. We found that the O3 -induced reduction in gm was critical in limiting leaf photosynthesis. Changes in liquid-phase conductance rather than gas-phase conductance drive the decline in gm under elevated O3, and this effect was associated with thicker cell walls and smaller chloroplast sizes. The effects of O3 on palisade and spongy mesophyll cell traits and their contributions to gm were highly genotype-dependent. Our results suggest that, while anatomical adjustments under elevated O3 may contribute to defense against O3 stress, they also cause declines in gm and photosynthesis. These results provide the first evidence of anatomical constraints on gm under elevated O3 .

Optimal stomatal theory predicts CO2 responses of stomatal conductance in both gymnosperm and angiosperm trees.

Optimal stomatal theory predicts that stomata operate to maximise photosynthesis (Anet ) and minimise transpirational water loss to achieve optimal intrinsic water-use efficiency (iWUE). We tested whether this theory can predict stomatal responses to elevated atmospheric CO2 (eCO2 ), and whether it can capture differences in responsiveness among woody plant functional types (PFTs). We conducted a meta-analysis of tree studies of the effect of eCO2 on iWUE and its components Anet and stomatal conductance (gs ). We compared three PFTs, using the unified stomatal optimisation (USO) model to account for confounding effects of leaf-air vapour pressure difference (D). We expected smaller gs , but greater Anet , responses to eCO2 in gymnosperms compared with angiosperm PFTs. We found that iWUE increased in proportion to increasing eCO2 in all PFTs, and that increases in Anet had stronger effects than reductions in gs . The USO model correctly captured stomatal behaviour with eCO2 across most datasets. The chief difference among PFTs was a lower stomatal slope parameter (g1 ) for the gymnosperm, compared with angiosperm, species. Land surface models can use the USO model to describe stomatal behaviour under changing atmospheric CO2 conditions.

Convergence in phosphorus constraints to photosynthesis in forests around the world.

Tropical forests take up more carbon (C) from the atmosphere per annum by photosynthesis than any other type of vegetation. Phosphorus (P) limitations to C uptake are paramount for tropical and subtropical forests around the globe. Yet the generality of photosynthesis-P relationships underlying these limitations are in question, and hence are not represented well in terrestrial biosphere models. Here we demonstrate the dependence of photosynthesis and underlying processes on both leaf N and P concentrations. The regulation of photosynthetic capacity by P was similar across four continents. Implementing P constraints in the ORCHIDEE-CNP model, gross photosynthesis was reduced by 36% across the tropics and subtropics relative to traditional N constraints and unlimiting leaf P. Our results provide a quantitative relationship for the P dependence for photosynthesis for the front-end of global terrestrial C models that is consistent with canopy leaf measurements.

Temperature acclimation of net photosynthesis and its underlying component processes in four tropical tree species.

The effect of temperature change on leaf physiology has been extensively studied in temperate trees and to some extent in boreal and tropical tree species. While increased temperature typically stimulates leaf CO2 assimilation and tree growth in high-altitude ecosystems, tropical species are often negatively affected. These trees may operate close to their temperature optima and have a limited thermal acclimation capacity due to low seasonal and historical variation in temperature. To test this hypothesis, we studied the extent to which the temperature sensitivities of leaf photosynthesis and respiration acclimate to growth temperature in four common African tropical tree species. Tree seedlings native to different altitudes and therefore adapted to different growth temperatures were cultivated at three different temperatures in climate-controlled chambers. We estimated the acclimation capacity of the temperature sensitivities of light-saturated net photosynthesis, the maximum rates of Rubisco carboxylation (Vcmax) and thylakoid electron transport (J), and dark respiration. Leaf thylakoid membrane lipid composition, nitrogen content and leaf mass per area were also analyzed. Our results showed that photosynthesis in tropical tree species acclimated to higher growth temperatures, but that this was weakest in the species originating from the coolest climate. The temperature optimum of J acclimated significantly in three species and variation in J was linked to changes in the thylakoid membrane lipid composition. For Vcmax, there was only evidence of significant acclimation of optimal temperature in the lowest elevation species. Respiration acclimated to maintain homeostasis at growth temperature in all four species. Our results suggest that the lowest elevation species is better physiologically adapted to acclimate to high growth temperatures than the highest elevation species, indicating a potential shift in competitive balance and tree community composition to the disadvantage of montane tree species in a warmer world.

Temperature responses of photosynthesis and respiration in evergreen trees from boreal to tropical latitudes.

Evergreen species are widespread across the globe, representing two major plant functional forms in terrestrial models. We reviewed and analysed the responses of photosynthesis and respiration to warming in 101 evergreen species from boreal to tropical biomes. Summertime temperatures affected both latitudinal gas exchange rates and the degree of responsiveness to experimental warming. The decrease in net photosynthesis at 25°C (Anet25 ) was larger with warming in tropical climates than cooler ones. Respiration at 25°C (R25 ) was reduced by 14% in response to warming across species and biomes. Gymnosperms were more sensitive to greater amounts of warming than broadleaved evergreens, with Anet25 and R25 reduced c. 30-40% with > 10°C warming. While standardised rates of carboxylation (Vcmax25 ) and electron transport (Jmax25 ) adjusted to warming, the magnitude of this adjustment was not related to warming amount (range 0.6-16°C). The temperature optimum of photosynthesis (ToptA ) increased on average 0.34°C per °C warming. The combination of more constrained acclimation of photosynthesis and increasing respiration rates with warming could possibly result in a reduced carbon sink in future warmer climates. The predictable patterns of thermal acclimation across biomes provide a strong basis to improve modelling predictions of the future terrestrial carbon sink with warming.

Handling the heat - photosynthetic thermal stress in tropical trees.

Warming climate increases the risk for harmful leaf temperatures in terrestrial plants, causing heat stress and loss of productivity. The heat sensitivity may be particularly high in equatorial tropical tree species adapted to a thermally stable climate. Thermal thresholds of the photosynthetic system of sun-exposed leaves were investigated in three tropical montane tree species native to Rwanda with different growth and water use strategies (Harungana montana, Syzygium guineense and Entandrophragma exselsum). Measurements of chlorophyll fluorescence, leaf gas exchange, morphology, chemistry and temperature were made at three common gardens along an elevation/temperature gradient. Heat tolerance acclimated to maximum leaf temperature (Tleaf ) across the species. At the warmest sites, the thermal threshold for normal function of photosystem II was exceeded in the species with the highest Tleaf despite their higher heat tolerance. This was not the case in the species with the highest transpiration rates and lowest Tleaf . The results point to two differently effective strategies for managing thermal stress: tolerance through physiological adjustment of leaf osmolality and thylakoid membrane lipid composition, or avoidance through morphological adaptation and transpiratory cooling. More severe photosynthetic heat stress in low-transpiring montane climax species may result in a competitive disadvantage compared to high-transpiring pioneer species with more efficient leaf cooling.

Limited thermal acclimation of photosynthesis in tropical montane tree species.

The temperature sensitivity of physiological processes and growth of tropical trees remains a key uncertainty in predicting how tropical forests will adjust to future climates. In particular, our knowledge regarding warming responses of photosynthesis, and its underlying biochemical mechanisms, is very limited. We grew seedlings of two tropical montane rainforest tree species, the early-successional species Harungana montana and the late-successional species Syzygium guineense, at three different sites along an elevation gradient, differing by 6.8℃ in daytime ambient air temperature. Their physiological and growth performance was investigated at each site. The optimum temperature of net photosynthesis (ToptA ) did not significantly increase in warm-grown trees in either species. Similarly, the thermal optima (ToptV and ToptJ ) and activation energies (EaV and EaJ ) of maximum Rubisco carboxylation capacity (Vcmax ) and maximum electron transport rate (Jmax ) were largely unaffected by warming. However, Vcmax , Jmax and foliar dark respiration (Rd ) at 25℃ were significantly reduced by warming in both species, and this decline was partly associated with concomitant reduction in total leaf nitrogen content. The ratio of Jmax /Vcmax decreased with increasing leaf temperature for both species, but the ratio at 25℃ was constant across sites. Furthermore, in H. montana, stomatal conductance at 25℃ remained constant across the different temperature treatments, while in S. guineense it increased with warming. Total dry biomass increased with warming in H. montana but remained constant in S. guineense. The biomass allocated to roots, stem and leaves was not affected by warming in H. montana, whereas the biomass allocated to roots significantly increased in S. guineense. Overall, our findings show that in these two tropical montane rainforest tree species, the capacity to acclimate the thermal optimum of photosynthesis is limited while warming-induced reductions in respiration and photosynthetic capacity rates are tightly coupled and linked to responses of leaf nitrogen.

Combining carbon and oxygen isotopic signatures to identify ozone-induced declines in tree water-use efficiency.

Ground-level ozone (O3) pollution affects the plant carbon and water balance, but the relative contributions of impaired photosynthesis and the loss of stomatal functioning to the O3-induced reductions in water-use efficiency (WUE) remain unclear. We combined the leaf stable dual isotopic signatures of carbon (δ13C) and oxygen (δ18O) with related instantaneous gas exchange performance to determine the effects of O3 dose on the net photosynthetic rate (An), stomatal conductance (gs) and intrinsic WUE (iWUE = An/gs) in four tree species (one being a hybrid) exposed to five O3 levels. The iWUE declined for each step increase in O3 level, reflecting progressive loss of the coupling between leaf carbon gain and water loss. In ambient compared with charcoal-filtered air, the decreased iWUE was associated with reductions in both An and gs (i.e., decreased δ13C and increased δ18O). In elevated O3 treatments, however, the iWUE declines were caused by reduced An at constant or increased gs. The results show that the dual isotope approach provides a robust way to gather time-integrated information on how O3 pollution affects leaf gas exchange. Our study highlights that O3-induced decoupling between photosynthesis and stomatal regulation causes large and progressive declines in the WUE of forest trees, demonstrating the need for incorporating this hitherto unaccounted for effect into vegetation models.

Complete or overcompensatory thermal acclimation of leaf dark respiration in African tropical trees.

Tropical climates are getting warmer, with pronounced dry periods in large areas. The productivity and climate feedbacks of future tropical forests depend on the ability of trees to acclimate their physiological processes, such as leaf dark respiration (Rd ), to these new conditions. However, knowledge on this is currently limited due to data scarcity. We studied the impact of growth temperature on Rd and its dependency on net photosynthesis (An ), leaf nitrogen (N) and phosphorus (P) contents, and leaf mass per unit area (LMA) in 16 early-successional (ES) and late-successional (LS) tropical tree species in multispecies plantations along an elevation gradient (Rwanda TREE project). Moreover, we explored the effect of drought on Rd in one ES and one LS species. Leaf Rd at 20°C decreased at warmer sites, regardless if it was expressed per unit leaf area, mass, N or P. This acclimation resulted in an 8% and a 28% decrease in Rd at prevailing nighttime temperatures in trees at the intermediate and warmest sites, respectively. Moreover, drought reduced Rd , particularly in the ES species and at the coolest site. Thermal acclimation of Rd is complete or overcompensatory and independent of changes in leaf nutrients or LMA in African tropical trees.

Contrasting Dependencies of Photosynthetic Capacity on Leaf Nitrogen in Early- and Late-Successional Tropical Montane Tree Species.

Differences in photosynthetic capacity among tree species and tree functional types are currently assumed to be largely driven by variation in leaf nutrient content, particularly nitrogen (N). However, recent studies indicate that leaf N content is often a poor predictor of variation in photosynthetic capacity in tropical trees. In this study, we explored the relative importance of area-based total leaf N content (Ntot) and within-leaf N allocation to photosynthetic capacity versus light-harvesting in controlling the variation in photosynthetic capacity (i.e. V cmax, J max) among mature trees of 12 species belonging to either early (ES) or late successional (LS) groups growing in a tropical montane rainforest in Rwanda, Central Africa. Photosynthetic capacity at a common leaf temperature of 25˚C (i.e. maximum rates of Rubisco carboxylation, V cmax25 and of electron transport, J max25) was higher in ES than in LS species (+ 58% and 68% for V cmax25 and J max25, respectively). While Ntot did not significantly differ between successional groups, the photosynthetic dependency on Ntot was markedly different. In ES species, V cmax25 was strongly and positively related to Ntot but this was not the case in LS species. However, there was no significant trade-off between relative leaf N investments in compounds maximizing photosynthetic capacity versus compounds maximizing light harvesting. Both leaf dark respiration at 25˚C (+ 33%) and, more surprisingly, apparent photosynthetic quantum yield (+ 35%) was higher in ES than in LS species. Moreover, Rd25 was positively related to Ntot for both ES and LS species. Our results imply that efforts to quantify carbon fluxes of tropical montane rainforests would be improved if they considered contrasting within-leaf N allocation and photosynthetic Ntot dependencies between species with different successional strategies.

Genetic controls of short- and long-term stomatal CO2 responses in Arabidopsis thaliana.

BACKGROUND AND AIMS: The stomatal conductance (gs) of most plant species decreases in response to elevated atmospheric CO2 concentration. This response could have a significant impact on plant water use in a future climate. However, the regulation of the CO2-induced stomatal closure response is not fully understood. Moreover, the potential genetic links between short-term (within minutes to hours) and long-term (within weeks to months) responses of gs to increased atmospheric CO2 have not been explored. METHODS: We used Arabidopsis thaliana recombinant inbred lines originating from accessions Col-0 (strong CO2 response) and C24 (weak CO2 response) to study short- and long-term controls of gs. Quantitative trait locus (QTL) mapping was used to identify loci controlling short- and long-term gs responses to elevated CO2, as well as other stomata-related traits. KEY RESULTS: Short- and long-term stomatal responses to elevated CO2 were significantly correlated. Both short- and long-term responses were associated with a QTL at the end of chromosome 2. The location of this QTL was confirmed using near-isogenic lines and it was fine-mapped to a 410-kb region. The QTL did not correspond to any known gene involved in stomatal closure and had no effect on the responsiveness to abscisic acid. Additionally, we identified numerous other loci associated with stomatal regulation. CONCLUSIONS: We identified and confirmed the effect of a strong QTL corresponding to a yet unknown regulator of stomatal closure in response to elevated CO2 concentration. The correlation between short- and long-term stomatal CO2 responses and the genetic link between these traits highlight the importance of understanding guard cell CO2 signalling to predict and manipulate plant water use in a world with increasing atmospheric CO2 concentration. This study demonstrates the power of using natural variation to unravel the genetic regulation of complex traits.

Traits controlling shade tolerance in tropical montane trees.

Tropical canopies are complex, with multiple canopy layers and pronounced gap dynamics contributing to their high species diversity and productivity. An important reason for this complexity is the large variation in shade tolerance among different tree species. At present, we lack a clear understanding of which plant traits control this variation, e.g., regarding the relative contributions of whole-plant versus leaf traits or structural versus physiological traits. We investigated a broad range of traits in six tropical montane rainforest tree species with different degrees of shade tolerance, grown under three different radiation regimes (under the open sky or beneath sparse or dense canopies). The two distinct shade-tolerant species had higher fractional biomass in leaves and branches while shade-intolerant species invested more into stems, and these differences were greater under low radiation. Leaf respiration and photosynthetic light compensation point did not vary with species shade tolerance, regardless of radiation regime. Leaf temperatures in open plots were markedly higher in shade-tolerant species due to their low transpiration rates and large leaf sizes. Our results suggest that interspecific variation in shade tolerance of tropical montane trees is controlled by species differences in whole-plant biomass allocation strategy rather than by difference in physiological leaf traits determining leaf carbon balance at low radiation.

Nitrogen application is required to realize wheat yield stimulation by elevated CO2 but will not remove the CO2 -induced reduction in grain protein concentration.

Elevated CO2 (eCO2 ) generally promotes increased grain yield (GY) and decreased grain protein concentration (GPC), but the extent to which these effects depend on the magnitude of fertilization remains unclear. We collected data on the eCO2 responses of GY, GPC and grain protein yield and their relationships with nitrogen (N) application rates across experimental data covering 11 field grown wheat (Triticum aestivum) cultivars studied in eight countries on four continents. The eCO2 -induced stimulation of GY increased with N application rates up to ~200 kg/ha. At higher N application, stimulation of GY by eCO2 stagnated or even declined. This was valid both when the yield stimulation was expressed as the total effect and using per ppm CO2 scaling. GPC was decreased by on average 7% under eCO2 and the magnitude of this effect did not depend on N application rate. The net effect of responses on GY and protein concentration was that eCO2 typically increased and decreased grain protein yield at N application rates below and above ~100 kg/ha respectively. We conclude that a negative effect on wheat GPC seems inevitable under eCO2 and that substantial N application rates may be required to sustain wheat protein yields in a world with rising CO2 .

Ozone impact on wheat in Europe, Asia and North America - A comparison.

Data from experiments where field-grown wheat was exposed to ozone were collated in order to compare the effects in Europe, Asia and North America using dose-response regression. In addition to grain yield, average grain mass and harvest index were included to reflect the influence of ozone on the crop growth pattern. In order to include as many experiments as possible, daytime average ozone concentration was used as the ozone exposure index, but AOT40, estimated from average ozone concentrations, was also used to compare the performance of the two exposure metrics. The response to ozone differed significantly between the continents only for grain yield when using AOT40 as the exposure index. North American wheat was less sensitive than European and Asian that responded similarly. The variation in responses across all three continents was smallest for harvest index, followed by grain mass and grain yield. The highly consistent effect on harvest index shows that not only effects on biomass accumulation, but also on the partitioning of biomass, are important for the ozone-induced grain yield loss in wheat. The average duration of daily ozone exposure was longer in European experiments compared to North American and Asian. It cannot be excluded that this contributed to the indicated higher ozone sensitivity in European wheat in relation to North American. The main conclusions from this study are that on the average the response of wheat to ozone was lower for the older North American experiments and that the ozone response of the growth pattern reflected by grain mass and harvest index did not differ between continents.

Acclimation and adaptation components of the temperature dependence of plant photosynthesis at the global scale.

The temperature response of photosynthesis is one of the key factors determining predicted responses to warming in global vegetation models (GVMs). The response may vary geographically, owing to genetic adaptation to climate, and temporally, as a result of acclimation to changes in ambient temperature. Our goal was to develop a robust quantitative global model representing acclimation and adaptation of photosynthetic temperature responses. We quantified and modelled key mechanisms responsible for photosynthetic temperature acclimation and adaptation using a global dataset of photosynthetic CO2 response curves, including data from 141 C3 species from tropical rainforest to Arctic tundra. We separated temperature acclimation and adaptation processes by considering seasonal and common-garden datasets, respectively. The observed global variation in the temperature optimum of photosynthesis was primarily explained by biochemical limitations to photosynthesis, rather than stomatal conductance or respiration. We found acclimation to growth temperature to be a stronger driver of this variation than adaptation to temperature at climate of origin. We developed a summary model to represent photosynthetic temperature responses and showed that it predicted the observed global variation in optimal temperatures with high accuracy. This novel algorithm should enable improved prediction of the function of global ecosystems in a warming climate.

Mesophyll conductance limitation of photosynthesis in poplar under elevated ozone.

Finite mesophyll conductance (gm) reduces the rate of CO2 diffusion from the leaf intercellular space to the chloroplast and constitutes a major limitation of photosynthesis in trees. While it is well established that gm is decreased by stressors such as drought and high temperature, few studies have investigated if the phytotoxic air pollutant ozone (O3) affects gm. We quantified the relative importance of three different types of limitations of photosynthesis in poplar trees exposed to elevated O3: decreases in stomatal conductance, gm and biochemical photosynthetic capacity. The O3-induced reductions in light-saturated net photosynthesis were linked to significant declines in gm and biochemical photosynthetic capacity (in particular carboxylation). There was no significant effect of O3 on stomatal conductance. Of the O3-induced limitations on photosynthesis, gm limitation was by far the most important (-16%) while biochemical limitation (-8%) was rather small. Both limitations grew in magnitude over the study period and varied in response to leaf-specific O3 exposure. Our findings suggest that declines in gm may play a key role in limiting photosynthesis of plants exposed to elevated O3, an effect hitherto overlooked.