Lawren Sack

New handbook for standardised measurement of plant functional traits worldwide

Plant functional traits are the features (morphological, physiological, phenological) that represent ecological strategies and determine how plants respond to environmental factors, affect other trophic levels and influence ecosystem properties. Variation in plant functional traits, and trait syndromes, has proven useful for tackling many important ecological questions at a range of scales, giving rise to a demand for standardised ways to measure ecologically meaningful plant traits. This line of research has been among the most fruitful avenues for understanding ecological and evolutionary patterns and processes. It also has the potential both to build a predictive set of local, regional and global relationships between plants and environment and to quantify a wide range of natural and human-driven processes, including changes in biodiversity, the impacts of species invasions, alterations in biogeochemical processes and vegetation–atmosphere interactions. The importance of these topics dictates the urgent need for more and better data, and increases the value of standardised protocols for quantifying trait variation of different species, in particular for traits with power to predict plant- and ecosystem-level processes, and for traits that can be measured relatively easily. Updated and expanded from the widely used previous version, this handbook retains the focus on clearly presented, widely applicable, step-by-step recipes, with a minimum of text on theory, and not only includes updated methods for the traits previously covered, but also introduces many new protocols for further traits. This new handbook has a better balance between whole-plant traits, leaf traits, root and stem traits and regenerative traits, and puts particular emphasis on traits important for predicting species’ effects on key ecosystem properties. We hope this new handbook becomes a standard companion in local and global efforts to learn about the responses and impacts of different plant species with respect to environmental changes in the present, past and future.

The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta‐analysis

Increasing drought is one of the most critical challenges facing species and ecosystems worldwide, and improved theory and practices are needed for quantification of species tolerances. Leaf water potential at turgor loss, or wilting (π(tlp) ), is classically recognised as a major physiological determinant of plant water stress response. However, the cellular basis of π(tlp) and its importance for predicting ecological drought tolerance have been controversial. A meta-analysis of 317 species from 72 studies showed that π(tlp) was strongly correlated with water availability within and across biomes, indicating power for anticipating drought responses. We derived new equations giving both π(tlp) and relative water content at turgor loss point (RWC(tlp) ) as explicit functions of osmotic potential at full turgor (π(o) ) and bulk modulus of elasticity (ε). Sensitivity analyses and meta-analyses showed that π(o) is the major driver of π(tlp) . In contrast, ε plays no direct role in driving drought tolerance within or across species, but sclerophylly and elastic adjustments act to maintain RWC(tlp,) preventing cell dehydration, and additionally protect against nutrient, mechanical and herbivory stresses independent of drought tolerance. These findings clarify biogeographic trends and the underlying basis of drought tolerance parameters with applications in comparative assessments of species and ecosystems worldwide.

Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future

The design and function of leaf venation are important to plant performance, with key implications for the distribution and productivity of ecosystems, and applications in paleobiology, agriculture and technology. We synthesize classical concepts and the recent literature on a wide range of aspects of leaf venation. We describe 10 major structural features that contribute to multiple key functions, and scale up to leaf and plant performance. We describe the development and plasticity of leaf venation and its adaptation across environments globally, and a new global data compilation indicating trends relating vein length per unit area to climate, growth form and habitat worldwide. We synthesize the evolution of vein traits in the major plant lineages throughout paleohistory, highlighting the multiple origins of individual traits. We summarize the strikingly diverse current applications of leaf vein research in multiple fields of science and industry. A unified core understanding will enable an increasing range of plant biologists to incorporate leaf venation into their research.

What is conservation physiology? Perspectives on an increasingly integrated and essential science †

The definition of ‘conservation physiology’ is refined to be more inclusive, with an emphasis on characterizing diversity, understanding and predicting responses to environmental change and stressors, and generating solutions. The integrative discipline is focused on mechanisms and uses physiological tools, concepts, and knowledge to advance conservation and resource management.

Viewing leaf structure and evolution from a hydraulic perspective

More than 40 000 km3 year–1 of water flows through the intricate hydraulic pathways inside leaves. This water not only sustains terrestrial productivity, but also constitutes nearly 70% of terrestrial evapotranspiration, thereby influencing both global and local climate (Chapin et al. 2002). Thus, the central role played by leaf vascular systems in terrestrial biology provides an important context for research into the function and evolution of water transport in leaves. Significant progress has been made recently towards understanding the linkages between anatomy and water transport efficiency in leaves, and these discoveries provide a novel perspective to view the evolution of land plants.

Ecological differentiation in xylem cavitation resistance is associated with stem and leaf structural traits

Cavitation resistance is a critical determinant of drought tolerance in tropical tree species, but little is known of its association with life history strategies, particularly for seasonal dry forests, a system critically driven by variation in water availability. We analysed vulnerability curves for saplings of 13 tropical dry forest tree species differing in life history and leaf phenology. We examined how vulnerability to cavitation (P₅₀) related to dry season leaf water potentials and stem and leaf traits. P₅₀-values ranged from -0.8 to -6.2 MPa, with pioneers on average 38% more vulnerable to cavitation than shade-tolerants. Vulnerability to cavitation was related to structural traits conferring tissue stress vulnerability, being negatively correlated with wood density, and surprisingly maximum vessel length. Vulnerability to cavitation was negatively related to the Huber-value and leaf dry matter content, and positively with leaf size. It was not related to SLA. We found a strong trade-off between cavitation resistance and hydraulic efficiency. Most species in the field were operating at leaf water potentials well above their P₅₀, but pioneers and deciduous species had smaller hydraulic safety margins than shade-tolerants and evergreens. A trade-off between hydraulic safety and efficiency underlies ecological differentiation across these tropical dry forest tree species.

Hydraulic Analysis of Water Flow through Leaves of Sugar Maple and Red Oak

Leaves constitute a substantial fraction of the total resistance to water flow through plants. A key question is how hydraulic resistance within the leaf is distributed among petiole, major veins, minor veins, and the pathways downstream of the veins. We partitioned the leaf hydraulic resistance (Rleaf) for sugar maple (Acer saccharum) and red oak (Quercus rubra) by measuring the resistance to water flow through leaves before and after cutting specific vein orders. Simulations using an electronic circuit analog with resistors arranged in a hierarchical reticulate network justified the partitioning of total Rleaf into component additive resistances. On average 64% and 74% of the Rleaf was situated within the leaf xylem for sugar maple and red oak, respectively. Substantial resistance—32% and 49%— was in the minor venation, 18% and 21% in the major venation, and 14% and 4% in the petiole. The large number of parallel paths (i.e. a large transfer surface) for water leaving the minor veins through the bundle sheath and out of the leaf resulted in the pathways outside the venation comprising only 36% and 26% of Rleaf. Changing leaf temperature during measurement of Rleaf for intact leaves resulted in a temperature response beyond that expected from changes in viscosity. The extra response was not found for leaves with veins cut, indicating that water crosses cell membranes after it leaves the xylem. The large proportion of resistance in the venation can explain why stomata respond to leaf xylem damage and cavitation. The hydraulic importance of the leaf vein system suggests that the diversity of vein system architectures observed in angiosperms may reflect variation in whole-leaf hydraulic capacity.

Decline of Leaf Hydraulic Conductance with Dehydration: Relationship to Leaf Size and Venation Architecture

Across plant species, leaves vary enormously in their size and their venation architecture, of which one major function is to replace water lost to transpiration. The leaf hydraulic conductance (Kleaf) represents the capacity of the transport system to deliver water, allowing stomata to remain open for photosynthesis. Previous studies showed that Kleaf relates to vein density (vein length per area). Additionally, venation architecture determines the sensitivity of Kleaf to damage; severing the midrib caused Kleaf and gas exchange to decline, with lesser impacts in leaves with higher major vein density that provided more numerous water flow pathways around the damaged vein. Because xylem embolism during dehydration also reduces Kleaf, we hypothesized that higher major vein density would also reduce hydraulic vulnerability. Smaller leaves, which generally have higher major vein density, would thus have lower hydraulic vulnerability. Tests using simulations with a spatially explicit model confirmed that smaller leaves with higher major vein density were more tolerant of major vein embolism. Additionally, for 10 species ranging strongly in drought tolerance, hydraulic vulnerability, determined as the leaf water potential at 50% and 80% loss of Kleaf, was lower with greater major vein density and smaller leaf size (|r| = 0.85–0.90; P < 0.01). These relationships were independent of other aspects of physiological and morphological drought tolerance. These findings point to a new functional role of venation architecture and small leaf size in drought tolerance, potentially contributing to well-known biogeographic trends in leaf size.

Developmentally based scaling of leaf venation architecture explains global ecological patterns

Leaf size and venation show remarkable diversity across dicotyledons, and are key determinants of plant adaptation in ecosystems past and present. Here we present global scaling relationships of venation traits with leaf size. Across a new database for 485 globally distributed species, larger leaves had major veins of larger diameter, but lower length per leaf area, whereas minor vein traits were independent of leaf size. These scaling relationships allow estimation of intact leaf size from fragments, to improve hindcasting of past climate and biodiversity from fossil remains. The vein scaling relationships can be explained by a uniquely synthetic model for leaf anatomy and development derived from published data for numerous species. Vein scaling relationships can explain the global biogeographical trend for smaller leaves in drier areas, the greater construction cost of larger leaves and the ability of angiosperms to develop larger and more densely vascularised lamina to outcompete earlier-evolved plant lineages.

Structural determinants of leaf light-harvesting capacity and photosynthetic potentials

The traits characterizing plant functioning include simple dimensions such as leaf area, leaf thickness (T), display angle, and ratios of simple traits [e.g., leaf dry mass per unit area (MA)] as well as normalized rates [e.g., net maximum photosynthetic rate per unit mass (Amass) or per unit area (Aarea)], contents [e.g., N per unit dry mass (Nmass)], and “efficiencies” [gain/cost; e.g., photosynthetic N-use efficiency (PNUE=Amass/Nmass)]. Current plant science research mostly emphasizes the role of physiological traits in altering plant competitive ability, but the determinants of leaf light-harvesting capacity and foliar photosynthetic potentials also include numerous structural traits. In fact, while chloroplastic metabolism has remained remarkably conserved throughout phylogeny, plant evolution has led to a large diversity in foliar anatomy, morphology and shape that may tremendously modify the resource capture efficiency of leaves with essentially the same metabolic constitution (Smith et al. 2004). Apart from evolutionary adaptations, all traits have an enormous spatial and temporal variability. The evolutionary, developmental and environmental variations in traits, and the large number of potentially important traits and trait combinations, complicate predictions of relevant plant functions from the collections of traits. However, many traits that alter the same plant function co-vary along environmental gradients and among species. Understanding such coordinated variations among trait assemblages may significantly simplify projections of plant functioning in changing environmental conditions. Analyses of the trait co-variations have identified a series of general correlations among relevant plant structural and functional traits. For instance, across large species sets, Amass correlates positively with Nmass and negatively with MA and leaf life-span (Reich et al. 1997, 1999; Niinemets 2001; Wright et al. 2004b).