Lea Hallik

Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: quantitative limitations and scaling up by models

Foliage photosynthetic and structural traits were studied in 15 species with a wide range of foliage anatomies to gain insight into the importance of key anatomical traits in the limitation of diffusion of CO2 from substomatal cavities to chloroplasts. The relative importance of different anatomical traits in constraining CO2 diffusion was evaluated using a quantitative model. Mesophyll conductance (g m) was most strongly correlated with chloroplast exposed surface to leaf area ratio (S c/S) and cell wall thickness (T cw), but, depending on foliage structure, the overall importance of g m in constraining photosynthesis and the importance of different anatomical traits in the restriction of CO2 diffusion varied. In species with mesophytic leaves, membrane permeabilities and cytosol and stromal conductance dominated the variation in g m. However, in species with sclerophytic leaves, g m was mostly limited by T cw. These results demonstrate the major role of anatomy in constraining mesophyll diffusion conductance and, consequently, in determining the variability in photosynthetic capacity among species.

A worldwide analysis of within‐canopy variations in leaf structural, chemical and physiological traits across plant functional types

Extensive within-canopy light gradients importantly affect the photosynthetic productivity of leaves in different canopy positions and lead to light-dependent increases in foliage photosynthetic capacity per area (AA). However, the controls on AA variations by changes in underlying traits are poorly known. We constructed an unprecedented worldwide database including 831 within-canopy gradients with standardized light estimates for 304 species belonging to major vascular plant functional types, and analyzed within-canopy variations in 12 key foliage structural, chemical and physiological traits by quantitative separation of the contributions of different traits to photosynthetic acclimation. Although the light-dependent increase in AA is surprisingly similar in different plant functional types, they differ fundamentally in the share of the controls on AA by constituent traits. Species with high rates of canopy development and leaf turnover, exhibiting highly dynamic light environments, actively change AA by nitrogen reallocation among and partitioning within leaves. By contrast, species with slow leaf turnover exhibit a passive AA acclimation response, primarily determined by the acclimation of leaf structure to growth light. This review emphasizes that different combinations of traits are responsible for within-canopy photosynthetic acclimation in different plant functional types, and solves an old enigma of the role of mass- vs area-based traits in vegetation acclimation.

Are species shade and drought tolerance reflected in leaf-level structural and functional differentiation in Northern Hemisphere temperate woody flora?

Leaf-level determinants of species environmental stress tolerance are still poorly understood. Here, we explored dependencies of species shade (T(shade)) and drought (T(drought)) tolerance scores on key leaf structural and functional traits in 339 Northern Hemisphere temperate woody species. In general, T(shade) was positively associated with leaf life-span (L(L)), and negatively with leaf dry mass (M(A)), nitrogen content (N(A)), and photosynthetic capacity (A(A)) per area, while opposite relationships were observed with drought tolerance. Different trait combinations responsible for T(shade) and T(drought) were observed among the key plant functional types: deciduous and evergreen broadleaves and evergreen conifers. According to principal component analysis, resource-conserving species with low N content and photosynthetic capacity, and high L(L) and M(A), had higher T(drought), consistent with the general stress tolerance strategy, whereas variation in T(shade) did not concur with the postulated stress tolerance strategy. As drought and shade often interact in natural communities, reverse effects of foliar traits on these key environmental stress tolerances demonstrate that species niche differentiation is inherently constrained in temperate woody species. Different combinations of traits among key plant functional types further explain the contrasting bivariate correlations often observed in studies seeking functional explanation of variation in species environmental tolerances.

Photosynthetic acclimation to light in woody and herbaceous species: a comparison of leaf structure, pigment content and chlorophyll fluorescence characteristics measured in the field

Acclimation of foliage photosynthetic properties occurs with varying time kinetics, but structural, chemical and physiological factors controlling the kinetics of acclimation are poorly understood, especially in field environments. We measured chlorophyll fluorescence characteristics, leaf total carotenoid (Car), chlorophyll (Chl) and nitrogen (N) content and leaf dry mass per area (LMA) along vertical light gradients in natural canopies of the herb species, Inula salicina and Centaurea jacea, and tree species, Populus tremula and Tilia cordata, in the middle of the growing season. Presence of stress was assessed on the basis of night measurements of chlorophyll fluorescence. Our aim was to compare the light acclimation of leaf traits, which respond to light availability at long (LMA and N), medium (Chl a/b ratio, Car/Chl ratio) and short time scales (fluorescence characteristics). We found that light acclimation of nitrogen content per unit leaf area (N(area)), chlorophyll content per unit dry mass (Chl(mass)) and Chl/N ratio were related to modifications in LMA. The maximum PSII quantum yield (F(v) /F(m)) increased with increasing growth irradiance in I. salicina and P. tremula but decreased in T. cordata. Leaf growth irradiance, N content and plant species explained the majority of variability in chlorophyll fluorescence characteristics, up to 90% for steady-state fluorescence yield, while the contribution of leaf total carotenoid content was generally not significant. Chlorophyll fluorescence characteristics did not differ strongly between growth forms, but differed among species within a given growth form. These data highlight that foliage acclimation to light is driven by interactions between traits with varying time kinetics.

Spectral reflectance of multispecies herbaceous and moss canopies in the boreal forest understory and open field

The reflectance signal from the forest tree canopy is influenced by the optical properties of the background formed by understory vegetation. Our study shows that the herb-moss layer in the forest tends to be brighter in the visible wavelength when the canopy above is more closed because of the specific properties of plants grown in low light. When leaf-area-based chlorophyll content falls below approximately 150 mg·m–2, reflectance in the red region of the spectrum increases compared with that of the background. The best descriptors of the herb-moss layer for deriving optical parameters are herb layer dry mass for the visible wavelength range and total aboveground water mass for near-infrared (NIR) reflectance. In addition, chlorophyll content per leaf area considerably improves the red reflectance estimate.

Seasonal Course of the Spectral Properties of Alder and Birch Leaves

To interpret time series of hyperspectral measurements of vegetation canopies, the basic characteristics of the scattering elements forming these canopies-shoots, leaves, or needles-must be known. Unfortunately, data on the seasonal variation of leaf reflectance and transmittance are very scarce. To obtain a ground truth dataset applicable to modeling the phenological development of European (hemi)boreal forests, we measured the spectral properties of green leaves of two species common to this biome, gray alder (Alnus incana), and silver birch (Betula pendula). Measurements covered the full growing season of 2008 in Tõravere, Estonia. Leaves were sampled from sunlit locations and measured in a laboratory using an integrating sphere and a VNIR spectroradiometer. We measured four different optical parameters: directional-hemispherical reflectance and transmittance factors for leaf adaxial and abaxial surfaces. Leaf reflectance was used to calculate four leaf-level indices which, according to literature, are highly correlated with leaf chlorophyll content. Additionally, we calculated the derivative spectra of leaf reflectance in the red edge (RE) spectral region and fitted it with two Gaussian curves. Our analysis indicated continuous changes of leaf optical properties almost until the end of the growing season. The changes in the weights of the two Gaussian curves led to an effect known as peak jump, an abrupt shift in the RE inflection point. In near infrared (NIR), leaf absorption was negligible in the beginning of the growing period. However, we noted a slow but steady increase in the leaf NIR absorption with time.

Why does needle photosynthesis decline with tree height in Norway spruce

Needle morphological, chemical and physiological characteristics of Norway spruce were studied in a forest chronosequence in Järvselja Experimental Forest, Estonia. Current-year shoots were sampled from upper canopy positions in five stands, ranging in height from 1.8 to 33.0 m (corresponding age range was 10-85 years). A/C(i) curves were determined to obtain maximum carboxylation rates (V(cmax)) and maximum rates of electron transport (J(max)). Needle nitrogen (N) partitioning into photosynthetic functions was calculated from the values of V(cmax), J(max) and leaf chlorophyll concentration. All needle size parameters (length, width, thickness, volume and cross-sectional areas of mesophyll and xylem) increased significantly with tree height. The needles of taller trees had lower mass-based N and chlorophyll concentrations (21% and 43% difference between shortest and tallest stands, respectively), but higher dry mass per area (35%), dry mass per volume (18%), number of cells per mesophyll cross-section area (40%) and partitioning of N into non-photosynthetic functions (12%). Light saturated net assimilation rate, V(cmax), J(max) and stomatal conductance decreased with tree age (35%, 16%, 12% and 29% difference, respectively). A path analysis model describing tree age-related reduction of photosynthetic capacity as a result of sink limitation provided the best fit to our data. However, since the path model corresponding to source limitation, where photosynthetic reduction derives from changes in needle structure and chemistry was not rejected, we conclude that the decline in photosynthesis with tree age results from several mechanisms (limited sink strength, stomatal and N limitation) operating simultaneously and sequentially.

Electron transport efficiency at opposite leaf sides: effect of vertical distribution of leaf angle, structure, chlorophyll content and species in a forest canopy

We investigated changes in chlorophyll a fluorescence from alternate leaf surfaces to assess the intraleaf light acclimation patterns in combination with natural variations in radiation, leaf angles, leaf mass per area (LMA), chlorophyll content (Chl) and leaf optical parameters. Measurements were conducted on bottom- and top-layer leaves of Tilia cordata Mill. (a shade-tolerant sub-canopy species, sampled at heights of 11 and 16 m) and Populus tremula L. (a light-demanding upper canopy species, sampled at canopy heights of 19 and 26 m). The upper canopy species P. tremula had a six times higher PSII quantum yield (Φ(II)) and ratio of open reaction centres (qP), and a two times higher LMA than T. cordata. These species-specific differences were also present when the leaves of both species were in similar light conditions. Leaf adaxial/abaxial fluorescence ratio was significantly larger in the case of more horizontal leaves. Populus tremula (more vertical leaves), had smaller differences in fluorescence parameters between alternate leaf sides compared with T. cordata (more horizontal leaves). However, optical properties on alternate leaf sides showed a larger difference for P. tremula. Intraspecifically, the measured optical parameters were better correlated with LMA than with leaf Chl. Species-specific differences in leaf anatomy appear to enhance the photosynthetic potential of leaf biochemistry by decreasing the interception of excess light in P. tremula and increasing the light absorptance in T. cordata. Our results indicate that intraleaf light absorption gradient, described here as leaf adaxial/abaxial side ratio of chlorophyll a fluorescence, varies significantly with changes in leaf light environment in a multi-layer multi-species tree canopy. However, this variation cannot be described merely as a simple function of radiation, leaf angle, Chl or LMA, and species-specific differences in light acclimation strategies should also be considered.

Population differentiation in a Mediterranean relict shrub: the potential role of local adaptation for coping with climate change

Plants can respond to climate change by either migrating, adapting to the new conditions or going extinct. Relict plant species of limited distribution can be especially vulnerable as they are usually composed of small and isolated populations, which may reduce their ability to cope with rapidly changing environmental conditions. The aim of this study was to assess the vulnerability of Cneorum tricoccon L. (Cneoraceae), a Mediterranean relict shrub of limited distribution, to a future drier climate. We evaluated population differentiation in functional traits related to drought tolerance across seven representative populations of the species’ range. We measured morphological and physiological traits in both the field and the greenhouse under three water availability levels. Large phenotypic differences among populations were found under field conditions. All populations responded plastically to simulated drought, but they differed in mean trait values as well as in the slope of the phenotypic response. Particularly, dry-edge populations exhibited multiple functional traits that favored drought tolerance, such as more sclerophyllous leaves, strong stomatal control but high photosynthetic rates, which increases water use efficiency (iWUE), and an enhanced ability to accumulate sugars as osmolytes. Although drought decreased RGR in all populations, this reduction was smaller for populations from the dry edge. Our results suggest that dry-edge populations of this relict species are well adapted to drought, which could potentially mitigate the species’ extinction risk under drier scenarios. Dry-edge populations not only have a great conservation value but can also change expectations from current species’ distribution models.

Light Acclimation of Leaf Chlorophyll Content

We Studied Light Acclimation Of Leaf Chlorophyll (Chl A) And Nitrogen (Na) Contents Per Unit Area, And Leaf Dry Mass Per Unit Area (Lma) Along A Vertical Light Gradient In Natural Herbaceous And Tree Canopies. We Found That Lma Increased Strongly With Increasing Irradiance In The Tree Canopy But Not In The Herbaceous Canopy, And That Chl A Was Much More Variable In The Herbaceous Canopy (Coefficient Of Variation 82%) Compared To The Tree Canopy (16%). This Finding Can Indicate That In The Herbaceous Canopy Mature Leaves Had Undergone Re-Acclimation To Changed Light Conditions, While In The Tree Canopy Measured Light Conditions Reflected The Light Gradient During Leaf Development. Path Analysis Revealed That The Acclimation Of Leaf Chlorophyll Content To Increased Light Availability Consists Of Two Opposing Responses, Which Operate In Different Time Scales: (I) An Increasing Effect, Which Is Mediated Via Changes In Lma And N A, And Is Therefore Related To Light Conditions During Leaf Development; (Ii) And A Decrease, Which Is A Rapid Photoprotective Response.