The controversy over traits conferring shade-tolerance in trees: ontogenetic changes revisited

Successional replacement of intolerant species by shade tolerators along gap-understorey gradients is commonly associated with increasingly higher low-light carbon acquisition capacities of more tolerant species. This doctrine has recently been challenged because of evidence demonstrating larger leaf dry mass per unit area (MA), lower photosynthetic capacities and inferior whole plant relative growth rates (RGR) in both high and low irradiance in seedlings of shade-tolerators. However, as the individuals of shade-tolerant species often need to endure canopy shade for many years before gap formation, testing of the carbon gain hypothesis of shade tolerance requires examination of species carbon gain potentials during the entire plant ontogeny. Light vs. MA relationships throughout ontogeny demonstrate that saplings and canopy individuals of shade tolerators do have lower MA than intolerant species, and moderately higher photosynthetic capacities in low light, resulting in greater whole plant carbon gain capacities at lower light. The apparent discrepancy between results from studies on seedlings vs. saplings/trees is due to MA increasing at a faster rate in shade intolerators during ontogeny. A strong positive linkage between seed size and species shade tolerance further implies that shade tolerators have larger initial size, absolute growth rate and survivorship in low light despite their lower RGR. The evidence reviewed collectively suggests that the carbon balance concept of species’ successional position is valid for both seedlings and saplings, and that the apparent discrepancies in species rankings on the basis of structural and physiological characteristics are driven by variations in initial size and rate of ontogeny. Analyses of species shade tolerance potentials should therefore consider how any suite of adaptive traits varies with ontogen