Components explain, but do eddy fluxes constrain? Carbon budget of a nitrogen-fertilized boreal Scots pine forest.

Nitrogen (N) fertilization increases biomass and soil organic carbon (SOC) accumulation in boreal pine forests, but the underlying mechanisms remain uncertain. At two Scots pine sites, one undergoing annual N fertilization and the other a reference, we sought to explain these responses. We measured component fluxes, including biomass production, SOC accumulation, and respiration, and summed them into carbon budgets. We compared the resulting summations to ecosystem fluxes measured by eddy covariance. N fertilization increased most component fluxes (P < 0.05), especially SOC accumulation (20×). Only fine-root, mycorrhiza, and exudate production decreased, by 237 (SD = 28) g C m-2 yr-1 . Stemwood production increases were ascribed to this partitioning shift, gross primary production (GPP), and carbon-use efficiency, in that order. The methods agreed in their estimates of GPP in both stands (P > 0.05), but the components detected an increase in net ecosystem production (NEP) (190 (54) g C m-2 yr-1 ; P < 0.01) that eddy covariance did not (19 (62) g C m-2 yr-1 ; ns). The pairing of plots, the simplicity of the sites, and the strength of response provide a compelling description of N effects on the C budget. However, the disagreement between methods calls for further paired tests of N fertilization effects in simple forest ecosystems.

Limits to photosynthesis: seasonal shifts in supply and demand for CO2 in Scots pine.

Boreal forests undergo a strong seasonal photosynthetic cycle; however, the underlying processes remain incompletely characterized. Here, we present a novel analysis of the seasonal diffusional and biochemical limits to photosynthesis (Anet ) relative to temperature and light limitations in high-latitude mature Pinus sylvestris, including a high-resolution analysis of the seasonality of mesophyll conductance (gm ) and its effect on the estimation of carboxylation capacity ( VCmax ). We used a custom-built gas-exchange system coupled to a carbon isotope analyser to obtain continuous measurements for the estimation of the relevant shoot gas-exchange parameters and quantified the biochemical and diffusional controls alongside the environmental controls over Anet . The seasonality of Anet was strongly dependent on VCmax and the diffusional limitations. Stomatal limitation was low in spring and autumn but increased to 31% in June. By contrast, mesophyll limitation was nearly constant (19%). We found that VCmax limited Anet in the spring, whereas daily temperatures and the gradual reduction of light availability limited Anet in the autumn, despite relatively high VCmax . We describe for the first time the role of mesophyll conductance in connection with seasonal trends in net photosynthesis of P. sylvestris, revealing a strong coordination between gm and Anet , but not between gm and stomatal conductance.

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.

The mycorrhizal tragedy of the commons.

Trees receive growth-limiting nitrogen from their ectomycorrhizal symbionts, but supplying the fungi with carbon can also cause nitrogen immobilization, which hampers tree growth. We present results from field and greenhouse experiments combined with mathematical modelling, showing that these are not conflicting outcomes. Mycorrhizal networks connect multiple trees, and we modulated C provision by strangling subsets of Pinus sylvestris trees, assuming that carbon supply to fungi was reduced proportionally to the strangled fraction. We conclude that trees gain additional nitrogen at the expense of their neighbours by supplying more carbon to the fungi. But this additional carbon supply aggravates nitrogen limitation via immobilization of the shared fungal biomass. We illustrate the evolutionary underpinnings of this situation by drawing on the analogous tragedy of the commons, where the shared mycorrhizal network is the commons, and explain how rising atmospheric CO2 may lead to greater nitrogen immobilization in the future.

Linking canopy-scale mesophyll conductance and phloem sugar δ13 C using empirical and modelling approaches.

Interpreting phloem carbohydrate or xylem tissue carbon isotopic composition as measures of water-use efficiency or past tree productivity requires in-depth knowledge of the factors altering the isotopic composition within the pathway from ambient air to phloem contents and tree ring. One of least understood of these factors is mesophyll conductance (gm ). We formulated a dynamic model describing the leaf photosynthetic pathway including seven alternative gm descriptions and a simple transport of sugars from foliage down the trunk. We parameterised the model for a boreal Scots pine stand and compared simulated gm responses with weather variations. We further compared the simulated δ13 C of new photosynthates among the different gm descriptions and against measured phloem sugar δ13 C. Simulated gm estimates of the seven descriptions varied according to weather conditions, resulting in varying estimates of phloem δ13 C during cold/moist and warm/dry periods. The model succeeded in predicting a drought response and a postdrought release in phloem sugar δ13 C indicating suitability of the model for inverse prediction of leaf processes from phloem isotopic composition. We suggest short-interval phloem sampling during and after extreme weather conditions to distinguish between mesophyll conductance drivers for future model development.

Reduced photosynthetic thermal acclimation capacity under elevated ozone in poplar (Populus tremula) saplings.

The sensitivity of photosynthesis to temperature has been identified as a key uncertainty for projecting the magnitude of the terrestrial carbon cycle response to future climate change. Although thermal acclimation of photosynthesis under rising temperature has been reported in many tree species, whether tropospheric ozone (O3 ) affects the acclimation capacity remains unknown. In this study, temperature responses of photosynthesis (light-saturated rate of photosynthesis (Asat ), maximum rates of RuBP carboxylation (Vcmax ), and electron transport (Jmax ) and dark respiration (Rdark ) of Populus tremula exposed to ambient O3 (AO3 , maximum of 30 ppb) or elevated O3 (EO3 , maximum of 110 ppb) and ambient or elevated temperature (ambient +5°C) were investigated in solardomes. We found that the optimum temperature of Asat (ToptA ) significantly increased in response to warming. However, the thermal acclimation capacity was reduced by O3 exposure, as indicated by decreased ToptA , and temperature optima of Vcmax (ToptV ) and Jmax (ToptJ ) under EO3 . Changes in both stomatal conductance (gs ) and photosynthetic capacity (Vcmax and Jmax ) contributed to the shift of ToptA by warming and EO3 . Neither Rdark measured at 25°C ( R dark 25 ) nor the temperature response of Rdark was affected by warming, EO3 , or their combination. The responses of Asat , Vcmax , and Jmax to warming and EO3 were closely correlated with changes in leaf nitrogen (N) content and N use efficiency. Overall, warming stimulated growth (leaf biomass and tree height), whereas EO3 reduced growth (leaf and woody biomass). The findings indicate that thermal acclimation of Asat may be overestimated if the impact of O3 pollution is not taken into account.

Global photosynthetic capacity is optimized to the environment.

Earth system models (ESMs) use photosynthetic capacity, indexed by the maximum Rubisco carboxylation rate (Vcmax ), to simulate carbon assimilation and typically rely on empirical estimates, including an assumed dependence on leaf nitrogen determined from soil fertility. In contrast, new theory, based on biochemical coordination and co-optimization of carboxylation and water costs for photosynthesis, suggests that optimal Vcmax can be predicted from climate alone, irrespective of soil fertility. Here, we develop this theory and find it captures 64% of observed variability in a global, field-measured Vcmax dataset for C3 plants. Soil fertility indices explained substantially less variation (32%). These results indicate that environmentally regulated biophysical constraints and light availability are the first-order drivers of global photosynthetic capacity. Through acclimation and adaptation, plants efficiently utilize resources at the leaf level, thus maximizing potential resource use for growth and reproduction. Our theory offers a robust strategy for dynamically predicting photosynthetic capacity in ESMs.

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.

Diurnal variation in mesophyll conductance and its influence on modelled water-use efficiency in a mature boreal Pinus sylvestris stand.

Mesophyll conductance (gm) is a critical variable for the use of stable carbon isotopes to infer photosynthetic water-use efficiency (WUE). Although gm is similar in magnitude to stomatal conductance (gs), it has been measured less often, especially under field conditions and at high temporal resolution. We mounted an isotopic CO2 analyser on a field photosynthetic gas exchange system to make continuous online measurements of gas exchange and photosynthetic 13C discrimination (Δ13C) on mature Pinus sylvestris trees. This allowed the calculation of gm, gs, net photosynthesis (Anet), and WUE. These measurements highlighted the asynchronous diurnal behaviour of gm and gs. While gs declined from around 10:00, Anet declined first after 12:00, and gm remained near its maximum until 16:00. We suggest that high gm played a role in supporting an extended Anet peak despite stomatal closure. Comparing three models to estimate WUE from ∆13C, we found that a simple model, assuming constant net fractionation during carboxylation (27‰), predicted WUE well, but only for about 75% of the day. A more comprehensive model, accounting explicitly for gm and the effects of daytime respiration and photorespiration, gave reliable estimates of WUE, even in the early morning hours when WUE was more variable. Considering constant, finite gm or gm/gs yielded similar WUE estimates on the diurnal scale, while assuming infinite gm led to overestimation of WUE. These results highlight the potential of high-resolution gm measurements to improve modelling of Anet and WUE and demonstrate that such gm data can be acquired, even under field conditions.

Temperature responses of photosynthetic capacity parameters were not affected by foliar nitrogen content in mature Pinus sylvestris.

A key weakness in current Earth System Models is the representation of thermal acclimation of photosynthesis in response to changes in growth temperatures. Previous studies in boreal and temperate ecosystems have shown leaf-scale photosynthetic capacity parameters, the maximum rates of carboxylation (Vcmax ) and electron transport (Jmax ), to be positively correlated with foliar nitrogen (N) content at a given reference temperature. It is also known that Vcmax and Jmax exhibit temperature optima that are affected by various environmental factors and, further, that N partitioning among the foliar photosynthetic pools is affected by N availability. However, despite the strong recent anthropogenic influence on atmospheric temperatures and N deposition to forests, little is known about the role of foliar N contents in controlling the photosynthetic temperature responses. In this study, we investigated the temperature dependencies of Vcmax and Jmax in 1-year-old needles of mature boreal Pinus sylvestris (Scots pine) trees growing under low and high N availabilities in northern Sweden. We found that needle N status did not significantly affect the temperature responses of Vcmax or Jmax when the responses were fitted to a peaked function. If such N insensitivity is a common tree trait it will simplify the interpretation of the results from gradient and multi-species studies, which commonly use sites with differing N availabilities, on temperature acclimation of photosynthetic capacity. Moreover, it will simplify modeling efforts aimed at understanding future carbon uptake by precluding the need to adjust the shape of the temperature response curves to variation in N availability.

Ecophysiological variation of transpiration of pine forests: synthesis of new and published results.

Canopy transpiration (EC ) is a large fraction of evapotranspiration, integrating physical and biological processes within the energy, water, and carbon cycles of forests. Quantifying EC is of both scientific and practical importance, providing information relevant to questions ranging from energy partitioning to ecosystem services, such as primary productivity and water yield. We estimated EC of four pine stands differing in age and growing on sandy soils. The stands consisted of two wide-ranging conifer species: Pinus taeda and Pinus sylvestris, in temperate and boreal zones, respectively. Combining results from these and published studies on all soil types, we derived an approach to estimate daily EC of pine forests, representing a wide range of conditions from 35° S to 64° N latitude. During the growing season and under moist soils, maximum daily EC (ECm ) at day-length normalized vapor pressure deficit of 1 kPa (ECm-ref ) increased by 0.55 ± 0.02 (mean ± SE) mm/d for each unit increase of leaf area index (L) up to L = ~5, showing no sign of saturation within this range of quickly rising mutual shading. The initial rise of ECm with atmospheric demand was linearly related to ECm-ref . Both relations were unaffected by soil type. Consistent with theoretical prediction, daily EC was sensitive to decreasing soil moisture at an earlier point of relative extractable water in loamy than sandy soils. Our finding facilitates the estimation of daily EC of wide-ranging pine forests using remotely sensed L and meteorological data. We advocate an assembly of worldwide sap flux database for further evaluation of this approach.

A test of the 'one-point method' for estimating maximum carboxylation capacity from field-measured, light-saturated photosynthesis.

Simulations of photosynthesis by terrestrial biosphere models typically need a specification of the maximum carboxylation rate (Vcmax ). Estimating this parameter using A-Ci curves (net photosynthesis, A, vs intercellular CO2 concentration, Ci ) is laborious, which limits availability of Vcmax data. However, many multispecies field datasets include net photosynthetic rate at saturating irradiance and at ambient atmospheric CO2 concentration (Asat ) measurements, from which Vcmax can be extracted using a 'one-point method'. We used a global dataset of A-Ci curves (564 species from 46 field sites, covering a range of plant functional types) to test the validity of an alternative approach to estimate Vcmax from Asat via this 'one-point method'. If leaf respiration during the day (Rday ) is known exactly, Vcmax can be estimated with an r(2) value of 0.98 and a root-mean-squared error (RMSE) of 8.19 µmol m(-2) s(-1) . However, Rday typically must be estimated. Estimating Rday as 1.5% of Vcmax, we found that Vcmax could be estimated with an r(2) of 0.95 and an RMSE of 17.1 µmol m(-2) s(-1) . The one-point method provides a robust means to expand current databases of field-measured Vcmax , giving new potential to improve vegetation models and quantify the environmental drivers of Vcmax variation.

Seasonal and within-canopy variation in shoot-scale resource-use efficiency trade-offs in a Norway spruce stand.

Previous leaf-scale studies of carbon assimilation describe short-term resource-use efficiency (RUE) trade-offs where high use efficiency of one resource requires low RUE of another. However, varying resource availabilities may cause long-term RUE trade-offs to differ from the short-term patterns. This may have important implications for understanding canopy-scale resource use and allocation. We used continuous gas exchange measurements collected at five levels within a Norway spruce, Picea abies (L.) karst., canopy over 3 years to assess seasonal differences in the interactions between shoot-scale resource availability (light, water and nitrogen), net photosynthesis (An ) and the use efficiencies of light (LUE), water (WUE) and nitrogen (NUE) for carbon assimilation. The continuous data set was used to develop and evaluate multiple regression models for predicting monthly shoot-scale An . These models showed that shoot-scale An was strongly dependent on light availability and was generally well described with simple one- or two-parameter models. WUE peaked in spring, NUE in summer and LUE in autumn. However, the relative importance of LUE for carbon assimilation increased with canopy depth at all times. Our results suggest that accounting for seasonal and within-canopy trade-offs may be important for RUE-based modelling of canopy carbon uptake.

Weak vertical canopy gradients of photosynthetic capacities and stomatal responses in a fertile Norway spruce stand.

The sensitivity of carbon (C) assimilation to within-canopy nitrogen (N) allocation and of stomatal conductance (g s) to environmental variables were investigated along a vertical canopy gradient in a fertile Norway spruce [Picea abies (L.) Karst.] stand. Maximum rates of ribulose bisphosphate-saturated carboxylation (V (cmax)) and electron transport (J (max)) exhibited weak relationships with needle N content. Using these relationships together with a combined stomatal-photosynthesis model, it was found that the sensitivity of C assimilation of 12 1-year old shoots to within-canopy N allocation pattern was very weak. Modelled C assimilation based on optimal compared to observed N allocation pattern increased by only 1-2 %, and altering total needle N content by ± 30 % resulted in a 2-4 % change in modelled C assimilation. C assimilation was more sensitive to water use and changed by 8-12 % in response to ± 30 % altered stomatal conductance. No indications of significant limitations of photosynthesis by other nutrients or non-optimal within-canopy allocation of water were detected. The sensitivity of g s to photosynthetic photon flux density (PPFD) was found to be stronger in the lower canopy, while no significant within-canopy variation was observed in light-saturated g( s) or stomatal sensitivity to vapour pressure deficit (VPD). The results of this study show that, at this N rich site, photosynthesis integrated for shoots at different canopy positions is only marginally affected by N allocation pattern and that increased stand-scale N availability would only be truly beneficial to canopy photosynthesis if it resulted in increased leaf area.

Elevated ozone decreases the activity of Rubisco in poplar but not its activation under fluctuating light.

Increasing tropospheric ozone (O3) is well-known to decrease leaf photosynthesis under steady-state light through reductions in biochemical capacity. However, the effects of O3 on photosynthetic induction and its biochemical limitations in response to fluctuating light remain unclear, despite the rapid fluctuations of light intensity occurring under field conditions. In this study, two hybrid poplar clones with different O3 sensitivities were exposed to elevated O3. Dynamic photosynthetic CO2 response measurements were conducted to quantify the impact of elevated O3 and exposure duration on biochemical limitations during photosynthetic induction. We found that elevated O3 significantly reduced the steady-state light-saturated photosynthetic rate, the maximum rate of carboxylation (Vcmax) and Rubisco content. In addition, elevated O3 significantly decreased the time constants for slow phases and weighting of the fast phase of the Vcmax induction in poplar clone '546' but not in clone '107'. However, elevated O3 did not affect the time, it took to reach a given percentage of full Vcmax activation or photosynthetic induction in either clone. Overall, photosynthetic induction was primarily limited by the activity of Rubisco rather than the regeneration of ribulose-1,5-biphosphate regardless of O3 concentration and exposure duration. The lack of O3-induced effects on the activation of Rubisco observed here would simplify the simulation of impacts of O3 on nonsteady-state photosynthesis in dynamic photosynthetic models.

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.

Stomatal response drives between-species difference in predicted leaf water-use efficiency under elevated ozone.

Ozone-induced changes in the relationship between photosynthesis (An) and stomatal conductance (gs) vary among species, leading to inconsistent water use efficiency (WUE) responses to elevated ozone (O3). Thus, few vegetation models can accurately simulate the effects of O3 on WUE. Here, we conducted an experiment exposing two differently O3-sensitive species (Cotinus coggygria and Magnolia denudata) to five O3 concentrations and investigated the impact of O3 exposure on predicted WUE using a coupled An-gs model. We found that increases in stomatal O3 uptake caused linear reductions in the maximum rates of Rubisco carboxylation (Vcmax) and electron transport (Jmax) in both species. In addition, a negative linear correlation between O3-induced changes in the minimal gs of the stomatal model (g0) derived from the theory of optimal stomatal behavior and light-saturated photosynthesis was found in the O3-sensitive M. denudata. When the O3 dose-based responses of Vcmax and Jmax were included in a coupled An-gs model, simulated An under elevated O3 were in good agreement with observations in both species. For M. denudata, incorporating the O3 response of g0 into the coupled model further improved the accuracy of the simulated gs and WUE. In conclusion, the modified Vcmax, Jmax and g0 method presented here provides a foundation for improving the prediction for O3-induced changes in An, gs and WUE.

Limited vertical CO2 transport in stems of mature boreal Pinus sylvestris trees.

Several studies have suggested that CO2 transport in the transpiration stream can considerably bias estimates of root and stem respiration in ring-porous and diffuse-porous tree species. Whether this also happens in species with tracheid xylem anatomy and lower sap flow rates, such as conifers, is currently unclear. We infused 13C-labelled solution into the xylem near the base of two 90-year-old Pinus sylvestris L. trees. A custom-built gas exchange system and an online isotopic analyser were used to sample the CO2 efflux and its isotopic composition continuously from four positions along the bole and one upper canopy shoot in each tree. Phloem and needle tissue 13C enrichment was also evaluated at these positions. Most of the 13C label was lost by diffusion within a few metres of the infusion point indicating rapid CO2 loss during vertical xylem transport. No 13C enrichment was detected in the upper bole needle tissues. Furthermore, mass balance calculations showed that c. 97% of the locally respired CO2 diffused radially to the atmosphere. Our results support the notion that xylem CO2 transport is of limited magnitude in conifers. This implies that the concerns that stem transport of CO2 derived from root respiration biases chamber-based estimates of forest carbon cycling may be unwarranted for mature conifer stands.

Effect of elevated ozone, nitrogen availability and mesophyll conductance on the temperature responses of leaf photosynthetic parameters in poplar.

Although ozone (O3) concentration and nitrogen (N) availability are well known to affect plant physiology, their impacts on the photosynthetic temperature response are poorly understood. We addressed this knowledge gap by exposing seedlings of hybrid poplar clone '107' (Populous euramericana cv. '74/76') to elevated O3 (E-O3) and N availability variation in a factorial experiment. E-O3 decreased light-saturated net photosynthesis (Asat), mesophyll conductance (gm) and apparent maximum rate of carboxylation (Vcmax, based on intercellular CO2 concentration) but not actual Vcmax (based on chloroplast CO2 concentration) and increased respiration in light (Rd) at 25 °C. Nitrogen fertilization increased Asat, gm, Vcmax and the maximum rate of electron transport (Jmax) and reduced Rd at 25 °C and the activation energy of actual Vcmax. No E-O3 or E-O3 x N interaction effects on the temperature response parameters were detected, simplifying the inclusion of O3 impacts on photosynthesis in vegetation models. gm peaked at 30 °C, apparent Vcmax and Jmax at 32-33 °C, while the optimum temperatures of actual Vcmax and Jmax exceeded the measured temperature range (15-35 °C). Ignoring gm would, thus, have resulted in mistakenly attributing the decrease in Asat at high temperatures to reduced biochemical capacity rather than to greater diffusion limitation.