Lawrence B. Flanagan

Climate change and the evolution of C4 photosynthesis

Plants assimilate carbon by one of three photosynthetic pathways, commonly called the C(3), C(4), and CAM pathways. The C(4) photosynthetic pathway, found only among the angiosperms, represents a modification of C(3) metabolism that is most effective at low concentrations of CO(2). Today, C(4) plants are most common in hot, open ecosystems, and it is commonly felt that they evolved under these conditions. However, high light and high temperature, by themselves, are not sufficient to favor the evolution of C(4) photosynthesis at atmospheric CO(2) levels significantly above the current ambient values. A review of evidence suggests that C(4) plants evolved in response to a reduction in atmospheric CO(2) levels that began during the Cretaceous and continued until the Miocene.

Carbon isotope composition of boreal plants: Functional grouping of life forms

Abstract We tested the hypothesis that life forms (trees, shrubs, forbs, and mosses; deciduous or evergreen) can be used to group plants with similar physiological characteristics. Carbon isotope ratios (δ13C) and carbon isotope discrimination (Δ) were used as functional characteristics because δ13C and Δ integrate information about CO2 and water fluxes, and so are useful in global change and scaling studies. We examined δ13C values of the dominant species in three boreal forest ecosystems: wet Picea mariana stands, mesic Populus tremuloides stands, and dry Pinus banksiana stands. Life form groups explained a significant fraction of the variation in leaf carbon isotope composition; seven life-form categories explained 50% of the variation in δ13C and 42% of the variation in Δ and 52% of the variance not due to intraspecific genetic differences (n=335). The life forms were ranked in the following order based on their values: evergreen trees<deciduous trees=evergreen and deciduous shrubs=evergreen forbs<deciduous forbs=mosses. This ranking of the life forms differed between deciduous (Populus) and evergreen (Pinus and Picea) ecosystems. Furthermore, life forms in the Populus ecosystem had higher discrimination values than life forms in the dry Pinus ecosystem; the Picea ecosystem had intermediate Δ values. These correlations between Δ and life form were related to differences in plant stature and leaf longevity. Shorter plants had lower Δ values than taller plants, resulting from reduced light intensity at lower levels in the forest. After height differences were accounted for, deciduous leaves had higher discrimination values than evergreen leaves, indicating that deciduous leaves maintained higher ratios of intracellular to ambient CO2 (ci/ca) than did evergreen leaves in a similar environment within these boreal ecosystems. We found the same pattern of carbon isotope discrimination in a year with above-average precipitation as in a year with below-average precipitation, indicating that environmental fluctuations did not affect the ranking of life forms. Furthermore, plants from sites near the northern and southern boundaries of the boreal forest had similar patterns of discrimination. We concluded that life forms are robust indicators of functional groups that are related to carbon and water fluxes within boreal ecosystems.

Stable Isotope Composition of Stem and Leaf Water: Applications to the Study of Plant Water Use

Much of the past research in plant physiological ecology has focused on gas-exchange responses of individual leaves (Pearcy et al., 1987). There has been great progress in developing models that link leaf biochemical properties with leaf gas-exchange characteristics (Farquhar & von Caemmerer, 1982). Success has also come in understanding the physiological basis for the ecological differentiation of plants with C3, C4 and CAM photosynthetic pathways (Osmond, Winter & Ziegler, 1982). It has been recognized, however, that further progress in linking leaf-level, instantaneous responses to longer-term whole-plant growth would require new approaches to extend the temporal and spatial scale of physiological measurements (Ehleringer, Pearcy & Mooney, 1986). It has also been suggested that more emphasis should be placed on studies of below-ground resource acquisition (Ehleringer et al., 1986). Stable-isotope techniques offer methods to address some of these long-standing problems in plant physiological ecology (Rundel, Ehleringer & Nagy, 1988). In this paper we describe how measurements of the isotopic composition of stem and leaf water can be applied to studies of plant water use. The first application we discuss takes advantage of the different isotopic compositions of summer rain and ground water to trace the relative uptake of these two water sources by different plant species. This first technique can be used, in a relatively non-destructive manner, to study aspects of root function under field conditions. The second application we outline involves the use of known fractionation events that occur during transpiration to study the leaf-air water vapour pressure gradient, an important parameter influencing photosynthetic gas exchange. It has been suggested that this second technique could potentially be used to study canopy level interactions in photosynthetic gas exchange over longer time-scales than are possible using conventional techniques (Farquhar et al., 1988; Sternberg, Mulkey & Wright, 1989).

Effect of changes in water content on photosynthesis, transpiration and discrimination against 13CO2 and C18O16O in Pleurozium and Sphagnum

Photosynthetic gas exchange characteristics of two common boreal forest mosses, Sphagnum (section acutifolia) and Pleurozium schreberi, were measured continuously during the time required for the moss to dry out from full hydration. Similar patterns of change in CO2 assimilation with variation in water content occurred for both species. The maximum rates of CO2 assimilation for Sphagnum (approx. 7 μmol m−2 s−1) occurred at a water content of approximately 7 (fresh weight/dry weight) while for Pleurozium the maximum rate (approx. 2 μmol m−2 s−1) occurred at a water content of approximately 6 (fresh weight/dry weight). Above and below these water contents CO2 assimilation declined. In both species total conductance to water vapour (expressed as a percentage of the maximum rates) remained nearly constant at a water content above 9 (fresh weight/dry weight), but below this level declined in a strong linear manner. Short-term, “on-line” 13CO2 and C18O16O discrimination varied substantially with changes in moss water content and associated changes in the ratio of chloroplast CO2 to ambient CO2 partial pressure. At full hydration (maximum water content) both Sphagnum and Pleurozium had similar values of 13CO2 discrimination (approx. 15). Discrimination against 13CO2 increased continuously with reductions in water content to a maximum of 27 in Sphagnum and 22 in Pleurozium. In a similar manner C18C16O discrimination increased from approximately 30 at full hydration in both species to a maximum of 150 in Sphagnum and 90 in Pleurozium, at low water content. The observed changes in C18O16O were strongly correlated to predictions of a mechanistic model of discrimination processes. Field measurements of moss water content suggested that photosynthetic gas exchange by moss in the understory of a black spruce forest was regularly limited by low water content.

Carbon isotope discrimination during photosynthesis and the isotope ratio of respired CO2 in boreal forest ecosystems

Our objective was to measure the carbon isotope ratio of CO 2 released by respiration (δ r ) within forest canopies at different times during the growing season and to use this information to estimate forest ecosystem carbon isotope discrimination. We made measurements in the three major forest types (black spruce, jack pine, and aspen) at the southern and northern ends of the boreal forest in central Canada. This research was part of a larger study, the Boreal EcosystemAtmosphere Study (BOREAS). The δ r values, calculated from measurements of change in the concentration and carbon isotope ratio of atmospheric CO 2 in air samples collected at night, ranged from -28.1‰ to -25.9‰ with an average (± s.d.) of -26.8‰ ± 0.5‰. There was good correlation between calculated δ r values and measurements of (1) the carbon isotope ratio of CO 2 released directly from the soil and (2) the δ 13 C values of foliage collected from the dominant tree species at each site. Carbon isotope discrimination during photosynthetic gas exchange (Δ A ) by each forest ecosystem was estimated as the difference between the carbon isotope ratio of atmospheric CO 2 at the top of the canopy (δ a ) and the isotopic composition of respired CO 2 : Δ A = δ a - δ r . All three of the major forest types had similar values of Δ A , with an average (± s.d.) of 19.1‰ ± 0.5‰. However, a seasonal change in forest discrimination was observed for aspen forests in both the northern and southern study areas, with an increase in Δ A occurring between the middle and end of the growing season. In contrast, the evergreen conifer canopies exhibited relatively constant discrimination values throughout the active growing season.

Discrimination against C18O16O during photosynthesis and the oxygen isotope ratio of respired CO2 in boreal forest ecosystems

Our objective was to analyze factors that influence changes in the oxygen isotope ratio (δ18O) of atmospheric CO2 within boreal forest ecosystems. We made measurements in the three major forest types (black spruce, jack pine, and aspen) at the southern and northern ends of the boreal forest in central Canada. This research was part of a larger study, the Boreal Ecosystem-Atmosphere Study (BOREAS). In terrestrial ecosystems the δ18O value of atmospheric CO2 is strongly influenced by isotope effects that occur during photosynthesis and respiration. Of primary importance is an equilibrium isotope effect that occurs between oxygen in CO2 and oxygen in soil water and plant chloroplast water. During the equilibrium reaction the oxygen isotope ratio of CO2 becomes enriched in 18O relative to that of water. We measured seasonal changes in the oxygen isotope ratio of (1) water input to the ecosystems (precipitation), (2) water taken up by the major plant species from the soil (plant stem water), and (3) water in plant leaves. We used this information in calculations of isotope discrimination during photosynthesis and soil respiration. Discrimination against C18O16O during photosynthetic gas exchange (ΔA) (influenced by equilibration with chloroplast water) averaged approximately 21‰ at midday and was similar for all forest types. In contrast, CO2 released during plant and soil respiration had an average δ18O value of −14.4‰ but was less depleted in 18O than would be expected for respired CO2 in isotopic equilibrium with soil water. This effect was most pronounced in black spruce sites because of the extensive coverage of moss on the ground surface and the observation that water in the upper moss layers can have an oxygen isotope ratio substantially different from water in deeper soil layers.

Carbon isotope discrimination in forest and pasture ecosystems of the Amazon Basin, Brazil

(1) Our objective was to measure the stable carbon isotope composition of leaf tissue and CO2 released by respiration (dr), and to use this information as an estimate of changes in ecosystem isotopic discrimination that occur in response to seasonal and interannual changes in environmental conditions, and land-use change (forest-pasture conversion). We made measurements in primary forest and pastures in the Amazon Basin of Brazil. At the Santarem forest site, dr values showed a seasonal cycle varying from less than 29% to approximately 26%. The observed seasonal change in dr was correlated with variation in the observed monthly precipitation. In contrast, there was no significant seasonal variation in dr at the Manaus forest site (average dr approximately 28%), consistent with a narrower range of variation in monthly precipitation than occurred in Santarem. Despite substantial (9%) vertical variation in leaf d 13 C, the average dr values observed for all forest sites were similar to the d 13 C values of the most exposed sun foliage of the dominant tree species. This suggested that the major portion of recently respired carbon dioxide in these forests was metabolized carbohydrate fixed by the sun leaves at the top of the forest canopy. There was no significant seasonal variation observed in the d 13 C values of leaf organic matter for the forest sites. We sampled in pastures dominated by the C4 grass, Brachiaria spp., which is planted after forest vegetation has been cleared. The carbon isotope ratio of respired CO2 in pastures was enriched in 13 C by approximately 10% compared to forest ecosystems. A significant temporal change occurred in dr after the Manaus pasture was burned. Burning removed much of the encroaching C3 shrub vegetation and so allowed an increased dominance of the C4 pasture grass, which resulted in higher dr values. INDEX TERMS: 0315 Atmospheric Composition and Structure: Biosphere/atmosphere interactions; 1610 Global Change: Atmosphere (0315, 0325); 1615 Global Change: Biogeochemical processes (4805); 3309 Meteorology and Atmospheric Dynamics: Climatology (1620); KEYWORDS: carbon cycle, global change, tropical ecosystems, atmospheric carbon dioxide

Leaf δ13C in Pinus resinosa trees and understory plants: variation associated with light and CO2 gradients

Abstract Our objective was to evaluate the relative importance of gradients in light intensity and the isotopic composition of atmospheric CO2 for variation in leaf carbon isotope ratios within a Pinus resinosa forest. In addition, we measured photosynthetic gas exchange and leaf carbon isotope ratios on four understory species (Dryopteris carthusiana, Epipactus helleborine, Hieracium floribundum, Rhamnus frangula), in order to estimate the consequence of the variation in the understory light microclimate for carbon gain in these plants. During midday, CO2 concentration was relatively constant at vertical positions ranging from 15 m to 3 m above ground. Only at positions below 3 m was CO2 concentration significantly elevated above that measured at 15 m. Based on the strong linear relationship between changes in CO2 concentration and δ13C values for air samples collected during a diurnal cycle, we calculated the expected vertical profile for the carbon isotope ratio of atmospheric CO2 within the forest. These calculations indicated that leaves at 3 m height and above were exposed to CO2 of approximately the same isotopic composition during daylight periods. There was no significant difference between the daily mean δ13C values at 15 m (–7.77‰) and 3 m (–7.89‰), but atmospheric CO2 was significantly depleted in 13C closer to the ground surface, with daily average δ13C values of –8.85‰ at 5 cm above ground. The light intensity gradient in the forest was substantial, with average photosynthetically active radiation (PAR) on the forest floor approximately 6% of that received at the top of the canopy. In contrast, there were only minor changes in air temperature, and so it is likely that the leaf-air vapour pressure difference was relatively constant from the top of the canopy to the forest floor. For red pine and elm tree samples, there was a significant correlation between leaf δ13C value and the height at which the leaf sample was collected. Leaf tissue sampled near the forest floor, on average, had lower δ13C values than samples collected near the top of the canopy. We suggest that the average light intensity gradient through the canopy was the major factor influencing vertical changes in tree leaf δ13C values. In addition, there was a wide range of variation (greater than 4‰) among the four understory plant species for average leaf δ13C values. Measurements of leaf gas exchange, under natural light conditions and with supplemental light, were used to estimate the influence of the light microclimate on the observed variation in leaf carbon isotope ratios in the understory plants. Our data suggest that one species, Epipactus helleborine, gained a substantial fraction of carbon during sunflecks.

Stable oxygen and hydrogen isotope composition of leaf water in C3 and C4 plant species under field conditions

SummaryIn this paper we make comparisons between the observed oxygen and hydrogen stable isotope composition of leaf water and the predictions of the Craig-Gordon model of evaporative isotopic enrichment. Comparisons were made among two C3 species (Chenopodium album and Helianthus annuus) and two C4 species (Amaranthus retroflexus and Kochia scoparia), when plants were exposed to natural environmental conditions in the field. There were significant differences among the species for the hydrogen and oxygen isotopic composition of leaf water at mid-day. The Amaranthus and Helianthus plants had lower leaf water δD and δ18O values than did Kochia and Chenopodium. The observed leaf water δ values were significantly lower than those predicted by the evaporative enrichment model for all the species. The degree of discrepancy between the observed and modelled leaf water isotopic compositions differed among species. There was a strong linear relationship between the oxygen and hydrogen isotopic compositions of stem water, observed leaf water and the modelled leaf water for all species. The observed leaf water isotopic composition for the different species occurred at different points along the line connecting the stem water isotopic composition and the modelled leaf water isotopic composition in a plot of δD and δ18O. We interpret these linear relationships as mixing lines between the unfractionated source or stem water isotopic composition and the isotopic composition of water at the evaporation sites within leaves (as defined by the evaporative enrichment model).

Photosynthesis and carbon isotope discrimination in boreal forest ecosystems: A comparison of functional characteristics in plants from three mature forest types

In this paper we compare measurements of photosynthesis and carbon isotope discrimination characteristics among plants from three mature boreal forest types (Black spruce, Jack pine, and aspen) in order to help explain variation in ecosystem-level gas exchange processes. Measurements were made at the southern study area (SSA) and northern study area (NSA) of the boreal forest in central Canada as part of the Boreal Ecosystem-Atmosphere Study (BOREAS). In both the NSA and the SSA there were significant differences in photosynthesis among the major tree species, with aspen having the highest CO2 assimilation rates and spruce the lowest. Within a species, photosynthetic rates in the SSA were approximately twice those measured in the NSA, and this was correlated with similar variations in stomatal conductance. Calculations of the ratio of leaf intercellular to ambient CO2 concentration (ci/ca) from leaf carbon isotope discrimination (Δ) values indicated a relatively low degree of stomatal limitation of photosynthesis, despite the low absolute values of stomatal conductance in these boreal tree species. Within each ecosystem, leaf Δ values were strongly correlated with life-form groups (trees, shrubs, forbs, and mosses), and these differences are maintained between years. Although we observed significant variation in the 13C content of tree rings at the old Jack pine site in the NSA during the past decade (indicating interannual variation in the degree of stomatal limitation), changes in summer precipitation and temperature accounted for only 44% of the isotopic variance. We scaled leaf-level processes to the ecosystem level through analyses of well-mixed canopy air. On average, all three forest types had similar ecosystem-level Δ values (average value ± standard deviation, 19.1‰±0.5‰), calculated from measurements of change in the concentration and carbon isotope ratio of atmospheric CO2 during a diurnal cycle within a forest canopy. However, there were seasonal changes in ecosystem discrimination for aspen forests, while the evergreen conifer forests exhibited relatively constant discrimination values throughout the active growing season.