Ülo Niinemets

The worldwide leaf economics spectrum

Bringing together leaf trait data spanning 2,548 species and 175 sites we describe, for the first time at global scale, a universal spectrum of leaf economics consisting of key chemical, structural and physiological properties. The spectrum runs from quick to slow return on investments of nutrients and dry mass in leaves, and operates largely independently of growth form, plant functional type or biome. Categories along the spectrum would, in general, describe leaf economic variation at the global scale better than plant functional types, because functional types overlap substantially in their leaf traits. Overall, modulation of leaf traits and trait relationships by climate is surprisingly modest, although some striking and significant patterns can be seen. Reliable quantification of the leaf economics spectrum and its interaction with climate will prove valuable for modelling nutrient fluxes and vegetation boundaries under changing land-use and climate.

TOLERANCE TO SHADE, DROUGHT, AND WATERLOGGING OF TEMPERATE NORTHERN HEMISPHERE TREES AND SHRUBS

Lack of information on ecological characteristics of species across different continents hinders development of general world-scale quantitative vegetation dynamic models. We constructed common scales of shade, drought, and waterlogging tolerance for 806 North American, European/West Asian, and East Asian temperate shrubs and trees representing about 40% of the extant natural Northern Hemisphere species pool. These scales were used to test the hypotheses that shade tolerance is negatively related to drought and waterlogging tolerances, and that these correlations vary among continents and plant functional types. We observed significant negative correlations among shade and drought tolerance rankings for all data pooled, and separately for every continent and plant functional type, except for evergreen angiosperms. Another significant trade-off was found for drought and waterlogging tolerance for all continents, and for evergreen and deciduous angiosperms, but not for gymnosperms. For all data pooled, for Europe and East Asia, and for evergreen and deciduous angiosperms, shade tolerance was also negatively associated with waterlogging tolerance. Quantile regressions revealed that the negative relationship between shade and drought tolerance was significant for species growing in deep to moderate shade and that the negative relationship between shade and waterlogging tolerance was significant for species growing in moderate shade to high light, explaining why all relationships between different tolerances were negative according to general regression analyses. Phylogenetic signal in the tolerance to any one of the three environmental factors studied was significant but low, with only 21-24% of cladogram nodes exhibiting significant conservatism. The inverse relationships between different tolerances were significant in phylogenetically independent analyses both for the overall pool of species and for two multispecies genera (Pinus and Quercus) for which reliable molecular phylogenies were available. Only 2.6-10.3% of the species were relatively tolerant to two environmental stresses simultaneously (tolerance value � 3), and only three species were tolerant to all three stresses, supporting the existence of functional trade-offs in adjusting to multiple environmental limitations. These trade-offs represent a constraint for niche differentiation, reducing the diversity of plant responses to the many combinations of irradiance and water supply that are found in natural ecosystems.

GLOBAL‐SCALE CLIMATIC CONTROLS OF LEAF DRY MASS PER AREA, DENSITY, AND THICKNESS IN TREES AND SHRUBS

Leaf dry mass per unit area (LMA) is a product of leaf thickness (T) and of density (D). Greater T is associated with greater foliar photosynthetic rates per unit area because of accumulation of photosynthetic compounds; greater D results in decreased foliage photosynthetic potentials per unit dry mass because of lower concentrations of assimilative leaf compounds and decreases in intercellular transfer conductance to CO2. To understand the considerable variation in T and D at the global scale, literature data were analyzed for 558 broad-leaved and 39 needle-leaved shrubs and trees from 182 geographical locations distributed over all major earth biomes with woody vegetation. Site climatic data were interpolated from long-term world climatologies (monthly precipitation, surface temperature) or modeled using the Canadian Climate Center Model (monthly global solar radiation). Influences of total annual precipitation (WT), precipitation of the driest month (Wmin), monthly mean precipitation of the three dries...

Mesophyll diffusion conductance to CO2: An unappreciated central player in photosynthesis

Mesophyll diffusion conductance to CO(2) is a key photosynthetic trait that has been studied intensively in the past years. The intention of the present review is to update knowledge of g(m), and highlight the important unknown and controversial aspects that require future work. The photosynthetic limitation imposed by mesophyll conductance is large, and under certain conditions can be the most significant photosynthetic limitation. New evidence shows that anatomical traits, such as cell wall thickness and chloroplast distribution are amongst the stronger determinants of mesophyll conductance, although rapid variations in response to environmental changes might be regulated by other factors such as aquaporin conductance. Gaps in knowledge that should be research priorities for the near future include: how different is mesophyll conductance among phylogenetically distant groups and how has it evolved? Can mesophyll conductance be uncoupled from regulation of the water path? What are the main drivers of mesophyll conductance? The need for mechanistic and phenomenological models of mesophyll conductance and its incorporation in process-based photosynthesis models is also highlighted.

A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance

Changes in the efficiency of light interception and in the costs for light harvesting along the light gradients from the top of the plant canopy to the bottom are the major means by which efficient light harvesting is achieved in ecosystems. In the current review analysis, leaf, shoot and canopy level determinants of plant light harvesting, the light-driven plasticity in key traits altering light harvesting, and variations among different plant functional types and between species of different shade tolerance are analyzed. In addition, plant age- and size-dependent alterations in light harvesting efficiency are also examined. At the leaf level, the variations in light harvesting are driven by alterations in leaf chlorophyll content modifies the fraction of incident light harvested by given leaf area, and in leaf dry mass per unit area (MA) that determines the amount of leaf area formed with certain fraction of plant biomass in the leaves. In needle-leaved species with complex foliage cross-section, the degree of foliage surface exposure also depends on the leaf total-to-projected surface area ratio. At the shoot scale, foliage inclination angle distribution and foliage spatial aggregation are the major determinants of light harvesting, while at the canopy scale, branching frequency, foliage distribution and biomass allocation to leaves (FL) modify light harvesting significantly. FL decreases with increasing plant size from herbs to shrubs to trees due to progressively larger support costs in plant functional types with greater stature. Among trees, FL and stand leaf area index scale positively with foliage longevity. Plant traits altering light harvesting have a large potential to adjust to light availability. Chlorophyll per mass increases, while MA, foliage inclination from the horizontal and degree of spatial aggregation decrease with decreasing light availability. In addition, branching frequency decreases and canopies become flatter in lower light. All these plastic modifications greatly enhance light harvesting in low light. Species with greater shade tolerance typically form a more extensive canopy by having lower MA in deciduous species and enhanced leaf longevity in evergreens. In addition, young plants of shade tolerators commonly have less strongly aggregated foliage and flatter canopies, while in adult plants partly exposed to high light, higher shade tolerance of foliage allows the shade tolerators to maintain more leaf layers, resulting in extended crowns. Within a given plant functional type, increases in plant age and size result in increases in MA, reductions in FL and increases in foliage aggregation, thereby reducing plant leaf area index and the efficiency of light harvesting. Such dynamic modifications in plant light harvesting play a key role in stand development and productivity. Overall, the current review analysis demonstrates that a suite of chemical and architectural traits at various scales and their plasticity drive plant light harvesting efficiency. Enhanced light harvesting can be achieved by various combinations of traits, and these suites of traits vary during plant ontogeny.

Leaf Functional Anatomy in Relation to Photosynthesis

Rubisco is a large enzyme with a molecular mass of approximately 550 kD. The maximum rate of CO2 fixation (i.e. ribulose-1,5-bisphosphate [RuBP] carboxylation) at CO2 saturation is only 15 to 30 mol CO2 mol−1 Rubisco protein s−1 at 25°C. Affinity to CO2 is also low, and the K m, K c, at 25°C

Sensitivity of leaf size and shape to climate: global patterns and paleoclimatic applications

• Paleobotanists have long used models based on leaf size and shape to reconstruct paleoclimate. However, most models incorporate a single variable or use traits that are not physiologically or functionally linked to climate, limiting their predictive power. Further, they often underestimate paleotemperature relative to other proxies. • Here we quantify leaf-climate correlations from 92 globally distributed, climatically diverse sites, and explore potential confounding factors. Multiple linear regression models for mean annual temperature (MAT) and mean annual precipitation (MAP) are developed and applied to nine well-studied fossil floras. • We find that leaves in cold climates typically have larger, more numerous teeth, and are more highly dissected. Leaf habit (deciduous vs evergreen), local water availability, and phylogenetic history all affect these relationships. Leaves in wet climates are larger and have fewer, smaller teeth. Our multivariate MAT and MAP models offer moderate improvements in precision over univariate approaches (± 4.0 vs 4.8°C for MAT) and strong improvements in accuracy. For example, our provisional MAT estimates for most North American fossil floras are considerably warmer and in better agreement with independent paleoclimate evidence. • Our study demonstrates that the inclusion of additional leaf traits that are functionally linked to climate improves paleoclimate reconstructions. This work also illustrates the need for better understanding of the impact of phylogeny and leaf habit on leaf-climate relationships.

Mild versus severe stress and BVOCs: thresholds, priming and consequences.

Plant-generated volatile organic compounds (BVOCs) play key roles in large-scale atmospheric processes and serve the plants as important defense and signal molecules. The main emphasis in quantitative BVOC studies has been on constitutive emissions of isoprene and specific monoterpene species that are present in only certain emitting plant species. However, environmental and biotic stresses can induce emissions of an array of organic compounds in any plant species, whereas the magnitude of emissions induced by given stress depends on stress tolerance, timing, duration and severity (mild versus strong) of the stress. The main view put forward in this review is that quantitative understanding of stress effects is the key for constructing realistic models of both constitutive and induced BVOC emissions.

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.

Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field

Limited mesophyll diffusion conductance to CO(2) (g(m)) can significantly constrain plant photosynthesis, but the extent of g(m)-limitation is still imperfectly known. As g(m) scales positively with foliage photosynthetic capacity (A), the CO(2) drawdown from substomatal cavities (C(i)) to chloroplasts (C(C), C(i)-C(C)=A/g(m)) rather than g(m) alone characterizes the mesophyll diffusion limitations of photosynthesis. The dependencies of g(m) on A, foliage structure (leaf dry mass per unit area, M(A)), and the resulting drawdowns across a dataset of 81 species of contrasting foliage structure and photosynthetic potentials measured under non-stressed conditions were analysed to describe the structure-driven potential photosynthetic limitations due to g(m). Further the effects of key environmental stress factors and leaf and plant developmental alterations on g(m) and CO(2) drawdown were evaluated and the implications of varying g(m) on foliage photosynthesis in the field were simulated. The meta-analysis demonstrated that g(m) of non-stressed leaves was negatively correlated with M(A), and despite the positive relationship between g(m) and A, the CO(2) drawdown was larger in leaves with more robust structure. The correlations were stronger with mass-based g(m) and A, probably reflecting the circumstance that mesophyll diffusion is a complex three-dimensional process that scales better with mesophyll volume-weighted than with leaf area-weighted traits. The analysis of key environmental stress effects on g(m) and CO(2) drawdowns demonstrated that the effect of individual stresses on CO(2) drawdowns varies depending on the stress effects on foliage structure and assimilation rates. Leaf diffusion limitations are larger in non-senescent older leaves and also in senescent leaves, again reflecting more robust leaf structure and/or non-co-ordinated alterations in leaf photosynthesis and g(m). According to simulation analyses, in plants with a larger part of the overall diffusion conductance from the ambient atmosphere to the chloroplasts in the mesophyll, photosynthesis is less sensitive to changes in stomatal conductance. Accordingly, in harsher environments that support vegetation with tougher long-living stress-tolerant leaves with lower g(m), reductions in stomatal conductance that are common during stress periods are expected to alter photosynthesis less than in species where a larger part of the total diffusion limitation is determined by stomata. While structural robustness improves plant performance under environmental stress, low g(m) and inherently large CO(2) drawdown in robust leaves limits the photosynthesis of these plants more severely under favourable conditions when stomatal conductance is high. The differences in overall responsiveness to environmental modifications of plants with varying g(m) need consideration in current large-scale ecosystem productivity models.