The anatomical determinants of leaf mass per area (LMA): strong predictiveness of a novel, explicit mathematical model across diverse species

Background/Question/Methods

Across species and environments leaves vary enormously in their size and structure. To understand this huge variation in leaf traits, and their influence on plant productivity, a framework has emerged of correlated traits that make up a single, unified axis known as the “leaf economic spectrum” (LES). Leaf dry mass per unit area (LMA) is typically considered the central trait in the LES because of its strong inter-correlations with other LES traits. While various studies have shown correlations of cell and tissue anatomical traits with LMA, no fully explicit mathematical characterization of leaf anatomy has been developed to account for LMA. Thus, the principal underlying structural and compositional variables determining LMA across species have remained largely mysterious and controversies have arisen in the recent literature surrounding these drivers. To address this gap, we developed and tested new quantitative models for LMA and its underlying traits, leaf thickness (LT) and mass density (LD) (because LMA = LT × LD). We derived a formula predicting each trait based upon geometry, with inputs of measurable anatomical traits including cell cross sectional areas, cell wall thickness, cell layers and airspace for each tissue type, leaf vein length per area and cell wall and protoplast mass densities. We tested these models using empirical measurements for leaf anatomical traits and chemical component analyses for eleven diverse woody species. We further used the derived equations to determine (1) the traits with most important influence in determining LMA across species, and (2) the influence of shifts in cell size on LMA, given allometric linkages of cell and cell wall dimensions across tissues.

Results/Conclusions

Our equation predicted species specific LMA values for the 11 woody species analyzed with considerable accuracy and precision (R² > 0.80).  The strongest anatomical drivers for LMA, LT and LD were the number of cell layers in each tissue, and tissue airspace. Contrary to recent hypotheses, vein volume per area made only a minor contribution to LMA, and cell wall and protoplast each contributed substantially to total leaf mass and volume.  Future expansion of this model will provide an anatomical basis for the interspecific relationships between other LES traits including nitrogen mass per leaf mass, light-saturated photosynthetic rate per leaf mass, leaf dry matter content and drought tolerance, ultimately providing a framework to clarify in explicit terms the role of leaf tissue anatomy in leaf functional diversity worldwide.