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

Abstract

Summary1 Successional replacement of intolerant species by shade tolerators along gapunderstorey 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 ( M A ), 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. 2 Light vs. M A relationships throughout ontogeny demonstrate that saplings and canopy individuals of shade tolerators do have lower M A 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 M A 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. 3 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 ontogeny.

Does ontogeny modulate irradiance-elicited plasticity of leaf traits in saplings of rain-forest tree species? A test with Dicorynia guianensis and Tachigali melinonii (Fabaceae, Caesalpinioideae)

“…Lusk and Warton, 2007;Niinemets, 1999aNiinemets, , 2006Thomas and Winner, 2002). In the present study we observed a significant increase of LMA with the sequence of ASDs in juvenile T. melinonii and to a lesser extent D. guianensis.…”

“…The two species are known to be rather shade-intolerant and the observed differences cannot be attributed to different ecological requirements. Moreover, to characterize shade tolerance as a trait, there is a need to scale up from leaf to at least branch level (if not canopy level) and to take into account potential effects of leaf life span (Lusk and Warton, 2007;Lusk et al, 2008;Niinemets, 2006;Valladares and Niinemets, 2008). Taking into account such integrative traits would be a target for future developments in the assessment of potential interactions between ontogeny and irradiance on tree physiology and carbon balance.…”

“…Plasticity may therefore be confounded with ontogenetic responses (Veneklaas and Poorter, 1988). This was particularly emphasised in studies of shade tolerance (Lusk and Warton, 2007;Lusk et al, 2008;McConnaughay and Coleman, 1999;Niinemets, 2006).…”

Leaf Morphological Plasticity of Tree Species from Two Developmental Stages in Araucaria Forest

“…Gaps, which represent an important facilitator of natural regeneration, may not occur. Many individuals need adjustments to heterogeneous light conditions in understory and it is expressed on leaf morphology (Niinemets 2006). However, morphological variations in the individuals the seedling and adult stages have been little explored.…”

“…Although the knowledge about the shade tolerance of the plants goes back to the 18th century, there are still controversies about what are the main morphological traits of tolerant species (Niinemets 2006). The knowledge about the adaptations to shade conditions is based mainly on the development of seedlings and the observed patterns are influenced by the interspecific variation of seed size (Sack et al 2006;Valladares and Niinemets 2008).…”