Thermal acclimation of photosynthesis and respiration of southern and northern white spruce seed sources tested along a regional climatic gradient indicates limited potential to cope with temperature warming.

Background and Aims: Knowledge of thermal acclimation of physiological processes of boreal tree species is necessary to determine their ability to adapt to predicted global warming and reduce the uncertainty around the anticipated feedbacks of forest ecosystems and global carbon cycle to climate change. The objective of this work was to examine the extent of thermal acclimation of net photosynthesis (An) and dark respiration (Rd) of two distant white spruce (Picea glauca) seed sources (from south and north of the commerial forest zone in Québec) in response to latitudinal and seasonal variations in growing conditions. Methods: The temperature responses of An, its biochemical and biophysical limitations, and Rd were measured in 1-year-old needles of seedlings from the seed sources growing in eight forest plantations along a regional thermal gradient of 5.5 °C in Québec, Canada. Key Results: The average optimum temperature (Topt) for An was 19 ± 1.2 °C and was similar among seed sources and plantation sites along the thermal gradient. Net photosynthesis at Topt (Aopt) varied significantly among plantation sites and was quadratically related to the mean July temperature (MJT) of plantation sites. Topt for mesophyll conductance, maximum electron transport rate and maximum rate of carboxylation were 28, 22 and 30 °C, respectively. Basal respiration rate (Rd at 10 °C) was linearly and negatively associated with MJT. Q10 of Rd (the rate of change in Rd with a 10 °C increase in temperature) did not show any significant relationship with MJT and averaged 1.5 ± 0.1. The two seed sources were similar in their thermal responses to latitudinal and seasonal variations in growing conditions. Conclusions: The results showed moderate thermal acclimation of respiration and no evidence for thermal acclimation of photosynthesis or local genetic adaptation for traits related to thermal acclimation. Therefore, growth of local white spruces may decline in future climates.

Genetic Adaptation vs. Ecophysiological Plasticity of Photosynthetic-Related Traits in Young Picea glauca Trees along a Regional Climatic Gradient.

Assisted population migration (APM) is the intentional movement of populations within a species range to sites where future environmental conditions are projected to be more conducive to growth. APM has been proposed as a proactive adaptation strategy to maintain forest productivity and to reduce the vulnerability of forest ecosystems to projected climate change. The validity of such a strategy will depend on the adaptation capacity of populations, which can partially be evaluated by the ecophysiological response of different genetic sources along a climatic gradient. This adaptation capacity results from the compromise between (i) the degree of genetic adaptation of seed sources to their environment of origin and (ii) the phenotypic plasticity of functional trait which can make it possible for transferred seed sources to positively respond to new growing conditions. We examined phenotypic variation in morphophysiological traits of six seed sources of white spruce (Picea glauca [Moench] Voss) along a regional climatic gradient in Québec, Canada. Seedlings from the seed sources were planted at three forest sites representing a mean annual temperature (MAT) gradient of 2.2°C. During the second growing season, we measured height growth (H2014) and traits related to resources use efficiency and photosynthetic rate (A max). All functional traits showed an adaptive response to the climatic gradient. Traits such as H2014, A max, stomatal conductance (g s ), the ratio of mesophyll to stomatal conductance, water use efficiency, and photosynthetic nitrogen-use efficiency showed significant variation in both physiological plasticity due to the planting site and seed source variation related to local genetic adaptation. However, the amplitude of seed source variation was much less than that related to plantation sites in the area investigated. The six seed sources showed a similar level of physiological plasticity. H2014, A max and g s , but not carboxylation capacity (V cmax), were correlated and decreased with a reduction of the average temperature of the growing season at seed origin. The clinal variation in H2014 and A max appeared to be driven by CO2 conductance. The presence of locally adapted functional traits suggests that the use of APM may have advantages for optimizing seed source productivity in future local climates.

Greenness indices from digital cameras predict the timing and seasonal dynamics of canopy-scale photosynthesis.

The proliferation of digital cameras co-located with eddy covariance instrumentation provides new opportunities to better understand the relationship between canopy phenology and the seasonality of canopy photosynthesis. In this paper we analyze the abilities and limitations of canopy color metrics measured by digital repeat photography to track seasonal canopy development and photosynthesis, determine phenological transition dates, and estimate intra-annual and interannual variability in canopy photosynthesis. We used 59 site-years of camera imagery and net ecosystem exchange measurements from 17 towers spanning three plant functional types (deciduous broadleaf forest, evergreen needleleaf forest, and grassland/crops) to derive color indices and estimate gross primary productivity (GPP). GPP was strongly correlated with greenness derived from camera imagery in all three plant functional types. Specifically, the beginning of the photosynthetic period in deciduous broadleaf forest and grassland/crops and the end of the photosynthetic period in grassland/crops were both correlated with changes in greenness; changes in redness were correlated with the end of the photosynthetic period in deciduous broadleaf forest. However, it was not possible to accurately identify the beginning or ending of the photosynthetic period using camera greenness in evergreen needleleaf forest. At deciduous broadleaf sites, anomalies in integrated greenness and total GPP were significantly correlated up to 60 days after the mean onset date for the start of spring. More generally, results from this work demonstrate that digital repeat photography can be used to quantify both the duration of the photosynthetically active period as well as total GPP in deciduous broadleaf forest and grassland/crops, but that new and different approaches are required before comparable results can be achieved in evergreen needleleaf forest.

Fine-scale geographic variation in photosynthetic-related traits of Picea glauca seedlings indicates local adaptation to climate.

Climate-related variations in functional traits of boreal tree species can result both from physiological acclimation and genetic adaptation of local populations to their biophysical environment. To improve our understanding and prediction of the physiological and growth responses of populations to climate change, we studied the role of climate of seed origin in determining variations in functional traits and its implications for tree improvement programs for a commonly reforested boreal conifer, white spruce (Picea glauca (Moench) Voss). We evaluated growth, root-to-shoot ratio (R/S), specific leaf area (SLA), needle nitrogen (N(mass)), total non-structural carbohydrates (NSC) and photosynthetic traits of 3-year-old seedlings in a greenhouse experiment using seed from six seed orchards (SO) representing the different regions where white spruce is reforested in Québec. Height and total dry mass (TDM) were positively correlated with photosynthetic capacity (A(max)), stomatal conductance (g(s)) and mesophyll conductance (g(m)). Total dry mass, but not height growth, was strongly correlated with latitude of seed origin (SO) and associated climate variables. A(max), g(s), g(m) and more marginally, photosynthetic nitrogen-use efficiency (PNUE) were positively associated with the mean July temperature of the SO, while water use efficiency (WUE) was negatively associated. Maximum rates of carboxylation (V(cmax)), maximum rates of electron transport (J(max)), SLA, N(mass), NSC and R/S showed no pattern. Our results did not demonstrate a higher Amax for northern seed orchards, although this has been previously hypothesized as an adaptation mechanism for maintaining carbon uptake in northern regions. We suggest that gs, gm, WUE and PNUE are the functional traits most associated with fine-scale geographic clines and with the degree of local adaptation of white spruce populations to their biophysical environments. These geographic patterns may reflect in situ adaptive genetic differences in photosynthetic efficiency along the cline.

Differentiating moss from higher plants is critical in studying the carbon cycle of the boreal biome.

The satellite-derived normalized difference vegetation index (NDVI), which is used for estimating gross primary production (GPP), often includes contributions from both mosses and vascular plants in boreal ecosystems. For the same NDVI, moss can generate only about one-third of the GPP that vascular plants can because of its much lower photosynthetic capacity. Here, based on eddy covariance measurements, we show that the difference in photosynthetic capacity between these two plant functional types has never been explicitly included when estimating regional GPP in the boreal region, resulting in a substantial overestimation. The magnitude of this overestimation could have important implications regarding a change from a current carbon sink to a carbon source in the boreal region. Moss abundance, associated with ecosystem disturbances, needs to be mapped and incorporated into GPP estimates in order to adequately assess the role of the boreal region in the global carbon cycle.

Decreasing photosynthesis at different spatial scales during the late growing season on a boreal cutover.

The relationship between photosynthesis and accumulated cold degree days (CDD) over the late growing season was examined at the shoot, ecosystem and landscape scales in a boreal cutover in eastern Canada predominated by black spruce (Picea mariana Mill. BSP), lowbush blueberry (Vaccinium angustifolium Ait.) and sheep laurel (Kalmia angustifolia L.). We calculated CDD as the sum of minimum daily temperatures below a 5 degrees C threshold. Light-saturated photosynthesis at the shoot level (A(max)) of black spruce and V. angustifolium decreased steadily with increasing CDD once temperatures below the CDD threshold value became frequent in mid-September, whereas K. angustifolia showed a more irregular pattern. Tissue acclimation played an important role in the decrease in A(max) as the season progressed, but only V. angustifolium showed decreasing foliar nitrogen concentrations. Based on eddy covariance flux tower data, maximum daily gross primary productivity (GPP(max)-tower) at the ecosystem level was more strongly related to CDD (r(2) = 0.59) than was maximum daily net ecosystem exchange (r(2) = 0.32). The GPP(max) was likely influenced by both tissue acclimation and the direct effects of changing temperatures and irradiances on physiological rates. Mean daily GPP, calculated for consecutive 8-day periods for a 25 km(2) area around the tower by the MODIS MOD17A2 Collection 4 satellite algorithm (GPP- MODIS), decreased more rapidly with increasing CDD than did GPP(max)-tower. Although GPP-MODIS was closely correlated with mean daily GPP from the tower (GPP(daily)-tower, r(2) = 0.95) over the late growing season, the former was about twice as high. Although MODIS estimates of air temperature closely tracked the ground data, the maximum light-use efficiency parameter used by the MODIS algorithm was much higher than that indicated by the tower measurements. There was a 3% decline in GPP(max)-tower with an increase of 10 CDD, corresponding to the percent decline in branch-level A(max) of black spruce and V. angustifolium.

The inhibition of ammonium uptake in excised birch (Betula pendula) roots by batatasin-III.

In northern Sweden, plants growing in association with the clonal dwarf shrub Empetrum hermaphroditum usually exhibit limited growth and are N-depleted. Previous studies suggest that this negative effect by E. hermaphroditum may be explained, at least in part, by the release of phenolic compounds, particularly the dihydrostilbene, batatasin-III from foliage to soil. In the present work, we investigated whether batatasin-III has the potential to interfere with NH4+ uptake in birch (Betula pendula) roots. Excised birch roots were exposed to batatasin-III during brief periods in 15NH4+ solutions, and then analyzed for labeled N. Batatasin-III inhibited N-NH4+ uptake by 28, 89 and 95% compared with the control, when roots were treated with 0.1, 1.0 and 2.8 mM of batatasin-III, respectively. The effect of 1.0-mM batatasin-III was greater at pH 4.2 than at pH 6.8. In addition, the inhibition of N-NH4+ uptake by batatasin-III was not reversed after rinsing the roots in water and transferring them to a batatasin-III free solution. Furthermore, birch seedlings immersed in a 1.0-mM batatasin-III solution for 2 h, and then replanted in pots with soil, had decreased growth, such that 10 weeks after treatment, the dry mass of both shoots and roots was reduced by 74 and 73%, respectively, compared with control seedlings. This suggests that a brief exposure to batatasin-III may have a long-term inhibitory effect on whole plant growth. Using plasma membrane vesicles isolated from easily extractable spinach (Spinacia oleracea) leaves, it was found that batatasin-III strongly inhibited proton pumping in isolated plasma membrane vesicles, while it only slightly inhibited ATP hydrolytic activity. The uncoupling of proton pumping from ATP hydrolytic activity suggests that batatasin-III disturbs membrane integrity. This hypothesis was further supported by a greater efflux of ions from birch roots immersed in a batatasin-III solution than from roots in a control solution.

Physiological responses of black spruce layers and planted seedlings to nutrient addition.

We investigated effects of nutrient addition on several physiological characteristics of 60-cm-tall black spruce (Picea mariana Mill. B.S.P.) layers (i.e., rooted branches of overstory trees) and 20-cm-tall planted seedlings on a clear-cut, N-limited boreal site. After two growing seasons, current-year and one-year-old needles of fertilized trees (layers and seedlings combined) had higher net photosynthetic rates (A(n)) and maximum capacity of Rubisco for CO(2) fixation (V(max)) than unfertilized trees. One-year-old needles of fertilized trees had higher stomatal conductance (g(s)), higher water-use efficiency, and lower intercellular to ambient CO(2) ratio than unfertilized trees. Additionally, fertilized trees had higher predawn and midday shoot water potentials than unfertilized trees. Stomatal conductance of 1-year-old needles was 23% higher in seedlings than in layers, but there were no significant differences in g(s) of current-year needles between the regeneration types. For both needle age-classes, A(n) and V(max) of layers were 25 and 40% higher, respectively, than the corresponding values for seedlings. The higher values of A(n), V(max) and foliar N concentration of layers compared with seedlings after two growing seasons may be associated with the larger root systems of the layers compared with the transplanted seedlings.

Parameterization and testing of a coupled photosynthesis-stomatal conductance model for boreal trees.

A coupled photosynthesis-stomatal conductance model was parameterized and tested with branches of black spruce (Picea mariana (Mill.) B.S.P.) and jack pine (Pinus banksiana Lamb.) trees growing in the Northern Study Area of the Boreal Ecosystem-Atmosphere Study (BOREAS) in Manitoba, Canada. Branch samples containing foliage of all age-classes were harvested from a lowland old black spruce (OBS) and an old jack pine (OJP) stand and the responses of photosynthesis (A(n)) and stomatal conductance (g(s)) to temperature, CO(2), light, and leaf-to-air vapor pressure difference (VPD) were determined under controlled laboratory conditions at the beginning, middle, and end of the growing season (Intensive Field Campaigns (IFC) 1, 2, and 3, respectively). The parameterized model was then tested against in situ field gas-exchange measurements in a young jack pine (YJP) and an upland black spruce (UBS) stand as well as in the OBS and OJP stands. Parameterization showed that Rubisco capacity (V(max)), apparent quantum yield (alpha') and Q(10) for sink limitation were the most crucial parameters for the photosynthesis sub-model and that V(max) varied among different measurement series in the laboratory. Verification of the model against the data used to parameterize it yielded correlation coefficients (r) of 0.97 and 0.93 for black spruce and jack pine, respectively, when IFC-specific parameters were used, and 0.77 and 0.87 when IFC-2 parameters were applied to all IFCs. For both measured and modeled g(s), the stomatal conductance sub-model, which linearly relates g(s) to (A(n)h(s))/c(s) (where h(s) and c(s) are relative humidity and CO(2) mole fraction at the leaf surface, respectively), had significantly steeper slopes and higher r values when only the VPD response data were used for parameterization than when all of the response data were used for parameterization. Testing the photosynthesis sub-model against upper canopy field data yielded poor results when laboratory estimates of V(max) were used. Use of the mean V(max) estimated for all upper canopy branches measured on a given day improved model performance for jack pine (from a nonsignificant correlation between measured and modeled A(n) to r = 0.45), but not for black spruce (r = 0.45 for both cases). However, when V(max) was estimated for each branch sample individually, the model accurately predicted the 23 to 137% diurnal variation in A(n) for all stands for both the upper and lower canopy. This was true both when all of the other parameters were IFC-specific (r = 0.93 and 0.92 for black spruce and jack pine, respectively) and when only mid-growing season (IFC-2) values were used (r = 0.92 for both species). Branch-specific V(max) estimates also permitted accurate prediction of field g(s) (r = 0.75 and 0.89 for black spruce and jack pine, respectively), although parameterization with all of the response data overestimated g(s) in the field, whereas parameterization with only the VPD response data provided unbiased predictions. Thus, after parameterization with the laboratory data, accurately modeling the range of A(n) and g(s) encountered in the field for both black spruce and jack pine was reduced to a single unknown parameter, V(max).

A physiological basis for biosphere-atmosphere interactions in the boreal forest: an overview.

Interdisciplinary field experiments for global change research are large, intensive efforts that study the controls on fluxes of carbon, water, trace gases, and energy between terrestrial ecosystems and the atmosphere at a range of spatial scales. Forest ecophysiology can make significant contributions to such efforts by measuring, interpreting, and modeling these fluxes for the individual components of forest ecosystems and then integrating the results into holistic ecosystem process models. The Boreal Ecosystem-Atmosphere Study (BOREAS) was undertaken because of the importance of the boreal forest biome to various global change issues. The study was conducted from 1993 to 1996 at sites in Saskatchewan and Manitoba, Canada. Results have shown that physiological processes of plants in the boreal forest can have large-scale consequences. For example, the composition of tree species strongly influences flux rates, with deciduous species having much higher carbon and water fluxes than coniferous species. Additionally, physiological limitations to transpiration in boreal conifers, even when soil water is abundant, reduces latent heat flux and increases sensible heat flux over large regions. This physiological control of transpiration can increase the depth of the atmospheric boundary layer on warm spring days to a level similar to that found in desert biomes. This special issue features 10 articles that address various aspects of the physiological basis of biosphere-atmosphere interactions in the boreal forest. The articles emphasize the environmental controls on water flux, carbon flux, and ecosystem productivity.

Regulation of branch-level gas exchange of boreal trees: roles of shoot water potential and vapor pressure difference.

Effects of shoot water potential (Psi) and leaf-to-atmosphere vapor pressure difference (VPD) on gas exchange of jack pine (Pinus banksiana Lamb.), black spruce (Picea mariana (Mill.) B.S.P.), and aspen (Populus tremuloides Michx.) were investigated at the northern edge of the boreal forest in Manitoba, Canada. Laboratory measurements on cut branches showed that net photosynthesis (A(n)) and mesophyll conductance (g(m)) of jack pine and g(m) of black spruce did not respond to Psi until a threshold Psi was reached below which they decreased linearly. Photosynthesis of black spruce decreased slowly with decreasing Psi above the threshold and declined more rapidly thereafter. The threshold Psi was lower in black spruce than in jack pine. However, stomatal conductance (g(s)) of black spruce decreased continuously with decreasing Psi, whereas g(s) of jack pine showed a threshold response. Mesophyll limitations were primarily responsible for the decline in A(n) at low Psi for jack pine and black spruce in the middle of the growing season, but stomatal limitations became more important later in the season. Field measurements on in situ branches on warm sunny days showed that both conifer species maintained Psi above the corresponding threshold and there was no evidence of Psi limitation on A(n) of jack pine, black spruce or aspen. Vapor pressure difference was important in regulating gas exchange in all three species. An empirical model was used to quantify the g(s) response to VPD. When parameterized with laboratory data for the conifers, the model also fit the corresponding field data. When parameterized with field data, the model showed that stomata of aspen were the most sensitive of the three species to VPD, and stomata of black spruce were the least sensitive. For jack pine and aspen, stomata of foliage in the upper canopy were significantly more sensitive than stomata of foliage in the lower canopy. Vapor pressure difference had a greater impact on A(n) of aspen than on A(n) of the conifers as a result of aspen's greater stomatal sensitivity to VPD and greater slope of the relationship between A(n) and intercellular CO(2) concentration (C(i)). During the 1994 growing season, VPD averaged 1.0 kPa, corresponding to ratios of C(i) to ambient CO(2) of 0.77, 0.71 and 0.81 for jack pine, black spruce and aspen, respectively. We conclude that increases in VPD at the leaf surface in response to climate change should affect the absolute CO(2) and H(2)O fluxes per unit leaf area of the aspen component of a boreal forest landscape more than those of the conifer component.