What Makes a Leaf Tough? Patterns of Correlated Evolution between Leaf Toughness Traits and Demographic Rates among 197 Shade-Tolerant Woody Species in a Neotropical Forest

Slow-growing juveniles of shade-tolerant plant species are predicted to have tough leaves because of the high cost of leaf replacement in shade relative to potential carbon gain. We assessed the degree of correlated evolution among eight traits associated with leaf toughness and the relationships of those traits with the growth and mortality rates of 197 tree and shrub species from the understory of the 50-ha forest dynamics plot on Barro Colorado Island, Panama. Path analysis with phylogenetically independent contrasts revealed that leaves attained material toughness (resistance to fracture per unit fracture area) through increases in tissue density, percent cellulose per unit dry mass, and vein fracture toughness. Lamina density and cellulose content evolved independently and thus represent different paths to material toughness. Structural toughness (resistance to fracture per unit fracture length) depended on material toughness and lamina thickness. Mortality rates of individuals 1-10 cm in stem diameter were negatively correlated with material toughness and lamina density but were independent of structural toughness and cell wall fiber contents. Leaf toughness traits were uncorrelated with relative growth rates. Results imply that material toughness enhances resistance to natural enemies, which increases survival and offsets the biomass allocation cost of producing tough leaves in the shaded understory.