Leaf cellulose density as the key determinant of inter- and intra-specific variation in leaf fracture toughness in a species-rich tropical forest

Abstract

Leaves as the main photosynthetic organ of plants must be well protected against various hazards to achieve their optimal lifespans. Yet, within-species variation and the material basis of leaf strength have been explored for very few species. Here, we present a large dataset of leaf fracture toughness from a species-rich humid tropical forest on Barro Colorado Island, Panama, reporting both among- and within-species variation in relation to light environment (sun-lit canopy versus shaded understorey) and ontogeny (seedlings versus adults). In this dataset encompassing 281 free-standing woody species and 428 species-light combinations, lamina fracture toughness varied ca 10 times. A central objective of our study was to identify generalizable patterns in the structural and material basis for interspecific variation in leaf lamina fracture toughness. The leaf lamina is a heterogeneous structure in which strong materials in cell walls, such as cellulose and lignin, contribute disproportionately to fracture toughness. We found significant increases in leaf fracture toughness from shade to sun and from seedling leaves to adult leaves. Both within and across species, leaf fracture toughness increased with total bulk density (dry biomass per unit volume) and cellulose mass concentration, but decreased with mass concentrations of lignin and hemicelluose. These bivariate relationships shift between light environments, but leaf cellulose density (cellulose mass per unit leaf volume) exhibits a common relationship with lamina fracture toughness between light environments and through ontogeny. Hence, leaf cellulose density is probably a universal predictor of leaf fracture toughness.

Keywords: biomechanics; cell wall fibre; cellulose; fracture toughness; lignin; plant functional traits.

Figure 1.

Scatter plots comparing species mean values of lamina fracture toughness (a), total bulk density (b), cellulose density (c), cell wall density (d), lignin fraction (e), hemicellulose fraction (f), cellulose fraction (g) and cell wall fraction (h) for sun-exposed, canopy leaves (horizontal axes) versus shaded, understorey leaves (vertical axes) of conspecific trees and treelets from Barro Colorado Island, Panama. The solid diagonal lines are 1 : 1 lines, representing equal values for sun and shade. Points below this line means plastic increase of trait values from shade to sun. The overall significance of this pattern is tested with paired t-test (table 1).

Figure 2.

(a) Scatter plot for the relationship between lamina fracture toughness and cellulose mass fraction for sun-exposed (circles, solid regression line) and shaded (triangles, broken regression line) leaves of trees and treelets from Barro Colorado Island, Panama. Regression lines show strong positive effects of cellulose mass fraction on toughness both in sun and shade, but sun leaves are tougher than shade leaves at a given cellulose mass fraction with slightly steeper slope (table 2). (b) The same data analysed with phylogenetic independent contrasts (PICs).

Figure 3.

(a) Scatter plot for the relationship between lamina fracture toughness and cellulose density (mass per unit lamina volume) for sun-exposed (circles) and shaded (triangles) leaves of trees and treelets from Barro Colorado Island, Panama. Sun and shade leaves fall along one common regression line (table 2). (b) The same data analysed with phylogenetic independent contrasts (PICs).

Figure 4.

Fracture toughness of leaves of 2- to 4-year-old seedlings grown experimentally in treefall gaps (circles, 21 species) and deeply shaded understorey (triangles, seven species), along with the data for older plants shown as shadows (same data as figure 3a). Excluding one seedling data point (Aspidosperma cruenta grown in shade, with the highest toughness in the plot) from ANCOVA, seedlings and older plants exhibit common slopes, but seedling leaves are less tough than adult leaves for a given value of cellulose density. (Online version in colour.)