Spatial and age-dependent modifications of photosynthetic capacity in four Mediterranean oak species.

Drought is one of the most important limitations of photosynthesis in Mediterranean climates. However, Mediterranean sclerophyllous species with long-lived leaves also support extensive and dynamic canopies, with potentially large spatial and age-dependent gradients. We studied within-canopy and temporal patterns in foliage structure, chemistry and photosynthesis in the evergreen species Quercus coccifera L., Q. ilex L. subsp. ballota (Desf.) Samp. in Bol. and Q. suber L. and in the semi-deciduous marcescent species Q. faginea Lam. to determine the role of within-canopy shading and leaf age on foliage functioning. There was a 2.5-fold within-canopy gradient in leaf dry mass per unit area (MA) that was accompanied by a 3-fold range in area-based leaf nitrogen (N) content, the capacity for photosynthetic electron transport (Jmax) and maximum Rubisco carboxylase activity (Vcmax), while the fractional investments of leaf nitrogen in electron transport (FB) and in Rubisco (FR) were relatively constant within the canopy. Leaf aging led to increased MA, larger or constant mass-based N content, larger phosphorous (P) and structural carbon contents, but decreased movable cation contents. Age-dependent increases in MA and N per dry mass meant that Jmax and Vcmax per area were weakly related to leaf age, with a trend of decreasing values in older leaves. However, Jmax and Vcmax per unit dry mass decreased 4-fold across the range of leaf age, primarily owing to decreases in apparent N investments in photosynthetic machinery. This decrease in apparent N investments in photosynthetic machinery was possibly the result of a larger fraction of N bound to cell walls, or of an enhanced CO2 diffusion resistance from the outer surface of cell walls to the chloroplasts in older leaves with thicker and more lignified cell walls. The age-dependent variation in apparent fractional investments of N in photosynthetic machinery reduced the generality of leaf nitrogen v. photosynthesis relationships. Photosynthetic characteristics qualitatively fitted the same patterns with leaf age in all species, but at a common leaf age, area-based leaf photosynthetic potentials depended on species-specific values of MA. These data collectively demonstrate important canopy and age-dependent controls on leaf structure, chemistry and photosynthetic potentials that should be included in larger-scale photosynthesis simulations in Mediterranean climates.

Three-dimensional lamina architecture alters light-harvesting efficiency in Fagus: a leaf-scale analysis.

Modification of foliage exposition and morphology by seasonal average integrated quantum flux density (Qint) was investigated in the canopies of the shade-tolerant late-successional deciduous tree species Fagus orientalis Lipsky and Fagus sylvatica L. Because the leaves were not entirely flat anywhere in the canopy, the leaf lamina was considered to be three-dimensional and characterized by the cross-sectional angle between the leaf halves (theta). Both branch and lamina inclination angles with respect to the horizontal scaled positively with irradiance in the canopy, allowing light to penetrate to deeper canopy horizons. Lamina cross-sectional angle varied from 170 degrees in the most shaded leaves to 90-100 degrees in leaves in the top of the canopy. Thus, the degree of leaf rolling increased with increasing Qint, further reducing the light-interception efficiency of the upper-canopy leaves. Simulations of the dependence of foliage light-interception efficiency on theta demonstrated that decreases in theta primarily reduce the interception efficiency of direct irradiance, but that diffuse irradiance was equally efficiently intercepted over the entire range of theta values in our study. Despite strong alteration in foliage light-harvesting capacity within the canopy and greater transmittance of the upper crown compared with the lower canopy, mean incident irradiances varied more than 20-fold within the canopy, indicating inherent limitations in light partitioning within the canopy. This extensive canopy light gradient was paralleled by plastic changes in foliar structure and chemistry. Leaf dry mass per unit area varied 3-4-fold between the canopy top and bottom, providing an important means of scaling foliage nitrogen contents and photosynthetic capacity per unit area with Qint. Although leaf structure versus light relationships were qualitatively similar in all cases, there were important tree-to-tree and species-to-species variations, as well as evidence of differences in investments in structural compounds within the leaf lamina, possibly in response to contrasting leaf water availability in different trees.

Stomatal constraints may affect emission of oxygenated monoterpenoids from the foliage of Pinus pinea.

Dependence of monoterpenoid emission and fractional composition on stomatal conductance (G(V)) was studied in Mediterranean conifer Pinus pinea, which primarily emits limonene and trans-beta-ocimene but also large fractions of oxygenated monoterpenoids linalool and 1,8-cineole. Strong decreases in G(V) attributable to diurnal water stress were accompanied by a significant reduction in total monoterpenoid emission rate in midday. However, various monoterpenoids responded differently to the reduction in G(V), with the emission rates of limonene and trans-beta-ocimene being unaffected but those of linalool and 1,8-cineole closely following diurnal variability in G(V). A dynamic emission model indicated that stomatal sensitivity of emissions was associated with monoterpenoid Henry's law constant (H, gas/liquid phase partition coefficient). Monoterpenoids with a large H such as trans-beta-ocimene sustain higher intercellular partial pressure for a certain liquid phase concentration, and stomatal closure is balanced by a nearly immediate increase in monoterpene diffusion gradient from intercellular air-space to ambient air. The partial pressure rises also in compounds with a low H, but more than 1,000-fold higher liquid phase concentrations of linalool and 1,8-cineole are necessary to increase intercellular partial pressure high enough to balance stomatal closure. The system response is accordingly slower, and the emission rates may be transiently suppressed by low G(V). Simulations further suggested that linalool and 1,8-cineole synthesis rates also decreased with decreasing G(V), possibly as the result of selective inhibition of various monoterpene synthases by stomata. We conclude that physicochemical characteristics of volatiles not only affect total emission but also alter the fractional composition of emitted monoterpenoids.

An analysis of light effects on foliar morphology, physiology, and light interception in temperate deciduous woody species of contrasting shade tolerance.

Maximum Rubisco activities (V(cmax)), rates of photosynthetic electron transport (J(max)), and leaf nitrogen and chlorophyll concentrations were studied along a light gradient in the canopies of four temperate deciduous species differing in shade tolerance according to the ranking: Populus tremula L. < Fraxinus excelsior L. < Tilia cordata Mill. = Corylus avellana L. Long-term light environment at the canopy sampling locations was characterized by the fractional penetration of irradiance in the photosynthetically active spectral region (I(sum)). We used a process-based model to distinguish among photosynthesis limitations resulting from variability in fractional nitrogen investments in Rubisco (P(R)), bioenergetics (P(B), N in rate-limiting proteins of photosynthetic electron transport) and light harvesting machinery (P(L), N in chlorophyll and thylakoid chlorophyll-protein complexes). On an area basis, V(cmax) and J(max) (V(a) (cmax) and J(a) (max)) increased with increasing growth irradiance in all species, and the span of variation within species ranged from two (T. cordata) to ten times (C. avellana). Examination of mass-based V(cmax) and J(max) (V(m) (cmax) and J(m) (max)) demonstrated that the positive relationships between area-based quantities and relative irradiance mostly resulted from the scaling of leaf dry mass per area (M(A)) with irradiance. Although V(m) (cmax) and J(m) (max) were positively related to growth irradiance in C. avellana, and J(m) (max) was positively related to irradiance in P. tremula, the variation range was only a factor of two. Moreover, V(m) (cmax) and J(m) (max) were negatively correlated with relative irradiance in T. cordata. Rubisco activity in crude leaf extracts generally paralleled the gas-exchange data, but it was independent of light in T. cordata, suggesting that declining V(m) (cmax) with increasing relative irradiance was related to increasing diffusive resistances from the intercellular air spaces to the sites of carboxylation in this species. Because irradiance had little effect on foliar nitrogen concentration, the relationships of P(B) and P(R) with irradiance were similar to those of V(m) (cmax) and J(m) (max). Shade-intolerant species tended to have greater P(B) and P(R) and also larger V(a) (cmax) and J(a) (max) than more shade-tolerant species. However, for the whole material, P(B) and P(R) varied only about 50%, whereas V(a) (cmax) and J(a) (max) varied more than 15-fold, further emphasizing the importance of leaf anatomical plasticity in determining photosynthetic acclimation to high irradiance. Leaf chlorophyll concentrations and fractional nitrogen investments in light harvesting increased hyperbolically with decreasing irradiance to improve quantum use efficiency for incident irradiance. The effect of irradiance on P(L) was of the same order as its effect in the opposite direction on M(A), leading to either a constant model estimate of leaf absorptance with I(sum) or a slightly positive correlation. We conclude that leaf morphological plasticity is a more relevant determinant of foliage adaptation to high irradiance than foliage biochemical properties, whereas biochemical adaptation to low irradiance is of the same magnitude as the anatomical adjustments. Although shade-tolerant species did not have greater chlorophyll concentrations and P(L) than shade-intolerant species, they possessed lower M(A), and could maintain a more extensive foliar display for light capture with constant biomass investment in leaves.

Growth and allocation of the arctic sedges Eriohorum angustifolium and E. vaginatum: effects of variable soil oxygen and nutrient availability.

In arctic tundra soil, oxygen depletion associated with soil flooding may control plant growth either directly through anoxia or indirectly through effects on nutrient availability. This study was designed to evaluate whether plant growth and physiology of two arctic sedge species are more strongly controlled by the direct or indirect effects of decreased soil aeration. Eriophorum angustifolium and E. vaginatum, which originate from flooded and well-drained habitats, respectively, were grown in an in situ transplant garden at two levels of soil oxygen, nitrogen, and phosphorus availability over two growing seasons. In both species, N addition had a stronger effect on growth and biomass allocation than P addition or soil oxygen depletion. Net photosynthesis and carbohydrate concentrations were relatively insensitive to changes in these factors. Biomass reallocated from shoots to below-ground parts in response to limited N supply was equally divided between roots (nutrient acquisition) and perennating rhizomes (storage tissue formation) in E. angustifolium. E. Vaginatum only increased its allocation to rhizomes. In the flood-tolerant E. angustifolium, growth was improved by soil anoxia and biomass allocation among plant parts was not significantly affected. Contrary to our initial hypothesis, whole-plant growth in E. vaginatum improved in flooded soils; however, it only did so when N availability was high. Under low N availability growth in flooded soils was reduced by 20% compared to growth in the aerobic environment. Reduced biomass allocation to rhizomes and thus to storage potential under anaerobic conditions may reduce long-term survival of E. vaginatum in flooded habitats.

Water relations, gas exchange, and growth of resprouts and mature plant shoots of Arbutus unedo L. and Quercus ilex L.

Resprout and mature plant shoot growth, leaf water status and gas exchange behavior, tissue nutrient content, flowering, and production were studied for co-occurring shallow-rooted (Arbutus unedo L.) and deeprooted (Quercus ilex L.) Mediterranean tree species at the Collserola Natural Park in Northeast Spain Resprouts showed higher growth rates than mature plant shoots. During fall, no differences in eco-physiological performance of leaves were found, but mobilization of carbohydrates from burls strongly stimulated growth of fall resprouts compared to spring resprouts, despite low exposed leaf area of the fall shoots. During summer drought, resprouts exhibited improved water status and carbon fixation compared to mature plant shoots. Shoot growth of Q. ilex was apparently extended due to deep rooting so that initial slower growth during spring and early summer as compared to A. unedo was compensated. Tissue nutrient contents varied only slightly and are postulated to be of minor importance in controlling rate of shoot growth, perhaps due to the relatively fertile soil of the site. Fall flowering appeared to inhibit fall shoot growth in A. unedo, but did not occur in Q. ilex. The results demonstrate that comparative examinations utilizing vegetation elements with differing morphological and physiological adaptations can be used to analyze relatively complex phenomena related to resprouting behavior. The studies provide an important multi-dimensional background framework for further studies of resprouting in the European Mediterranean region.

Coordination theory of leaf nitrogen distribution in a canopy.

It has long been observed that leaf nitrogen concentrations decline with depth in closed canopies in a number of plant communities. This phenomenon is generally believed to be related to a changing radiation environment and it has been suggested by some researchers that plants allocate nitrogen in order to optimize total whole canopy photosynthesis. Although optimization theory has been successfully utilized to describe a variety of physiological and ecological phenomena, it has some shortcomings that are subject to criticism (e.g., time constraints, oversimplifications, lack of insights, etc.). In this paper we present an alternative to the optimization theory of plant canopy nitrogen distribution, which we term coordination theory. We hypothesize that plants allocate nitrogen to maintain a balance between two processes, each of which is dependent on leaf nitrogen content and each of which potentially limits photosynthesis. These two processes are defined as Wc, the Rubiscolimited rate of carboxylation, and Wj, the electron transport-limited rate of carboxylation. We suggest that plants allocate nitrogen differentially to, leaves in different canopy layers in such a way that Wc and Wj remain roughly balanced. In this scheme, the driving force for the allocation of nitrogen within a canopy is the difference between the leaf nitrogen content that is required to bring Wc and Wj into balance and the current nitrogen content. We show that the daily carbon assimilation of a canopy with a nitrogen distribution resulting from this internal coordination of Wc and Wj is very similar to that obtained using optimization theory.