Low-light carbon balance and shade tolerance in the seedlings of woody plants: Do winter deciduous and broad-leaved evergreen species differ?

An appendix is available for this article which was not included in the print edition of the Journal. The appendix may be found at the rear of the full text, PDF version of the article. A popular conceptual model asserts that shade tolerance is characterized by morphological and physiological traits that enhance the net rate of carbon capture in low light. We tested this model by quantitatively reviewing growth, leaf lifespan, CO2 exchange and morphological data from 76 studies on woody seedlings grown under conditions of low light. Data were placed into three tolerance categories (intolerant, intermediate, tolerant), two light categories (less than 4% and 4–12%) and two leaf phenology categories (broad-leaved evergreen and winter deciduous). For both evergreen and deciduous groups, intolerant species had traits conferring greater growth potential than tolerant species in both light categories. These traits included greater leaf mass ratio, leaf area ratio, specific leaf area and mass-based photosynthetic rates above light compensation. However, in 0–4% light, growth rates were similar for intolerant and tolerant species, because low light together with higher respiration rates for intolerant species limited the expression of their growth potential differences. Deciduous and evergreen intolerant species were similar in many respects. However, both intermediate and tolerant deciduous species had markedly lower leaf mass ratios and higher root mass ratios than intermediate and tolerant evergreen species. In addition, deciduous species and intolerant evergreens must cope with as much as sixfold higher leaf turnover rates than tolerant evergreen species. Thus, rather than maximizing growth rates in low light, tolerant evergreen species minimize biomass loss through long leaf lifespans and low respiration rates. Tolerant deciduous species also minimize biomass losses by minimizing whole-plant respiration rates but they accomplish low biomass turnover though low leaf mass ratio and not low leaf turnover rates. Furthermore, unlike most tropical evergreens, tolerant deciduous species can gain large fractions of their total growing season carbon during short periods when the overstory is leafless and then allocate this carbon to storage (as reflected by high root mass ratios) rather than new leaves. In conclusion, we found no support for the low-light-enhanced carbon capture model of shade tolerance as viewed strictly from the perspective of physiological growth capacity. This can be explained by the disadvantages to net growth and survival of maintaining a high growth potential at low light, because high growth potential results in greater rates of whole-plant respiration, tissue turnover, herbivory and mechanical damage and in decreased storage. Thus, shade tolerance can be characterized by traits that maximize survival and net growth, where net growth includes losses to all agents.