The data suggest that, unlike plastic responses to shade, adaptation to shade in evergreens does not involve enhanced light-interception efficiency (Grime, 1965
). Crown silhouette-to-area ratios were not systematically related to shade tolerance, and in the larger size classes the most shade-tolerant species had low STAR values (Fig. F). This is a consequence of the increasing self-shading attending the accumulation of four to six leaf cohorts by the shade-tolerant species (Table and Fig. E). Neither have other studies provided any convincing evidence that shade-tolerant species intercept light particularly efficiently. A study of five deciduous species found no relationship between light-interception efficiency and shade tolerance (Delagrange et al., 2006
). Although a YPLANT-based comparative study reported that shade-tolerant Psychotria
species had higher light interception efficiencies than light-demanding congeners (Pearcy et al., 2004
), this finding could be largely a reflection of plastic (rather than inherent) variation in crown architecture, as light environments were not standardized across species. Plants in general respond plastically to shade by reducing leaf overlap and/or leaf angles, resulting in increased light-interception efficiency (McMillen and McClendon, 1979
; Valladares and Pearcy, 1998
; Gálvez and Pearcy, 2003
; Delagrange et al., 2006
). The pattern reported for Psychotria
spp. thus likely reflects the fact that light-demanding species were sampled in brighter light environments than their shade-tolerant congeners (Pearcy et al., 2004
, fig. 4).
Although most species of low to intermediate shade tolerance underwent only minor ontogenetic declines in light-interception efficiency, the exception presented by Nothofagus
requires some explanation (Fig. F). The low STAR values of large individuals of light-demanding Nothofagus
reflected the accumulation of large numbers of leaves, but this was associated with the small size of individual leaves (Fig. ) rather than retention of many leaf cohorts. Although a mean lifespan of only about 2 years for this species was calculated (Table ), large, highly branched Nothofagus
juveniles had >100 leaves, leading to heavy self-shading (Fig. E). A study of 38 Australian sclerophyll evergreens reported that self-shading within shoots was strongly negatively correlated with leaf size, and positively correlated with leaf number (Falster and Westoby, 2003
Variation in leaf inclination angles contributed little to species differences in light-interception efficiency (Fig. D). This agrees well with Delagrange et al. (2006)
, who found that leaf angles of five deciduous species compared in common light environments were not related to reputed shade tolerance. In contrast, Pearcy et al. (2004)
reported that slightly flatter leaf angles contributed to shade-tolerant Psychotria
species' advantage in light-interception efficiency over their light-demanding congeners. However, as mentioned above, this reported variation in both leaf angles and light-interception efficiency is probably attributable to the lack of standardization of light environments in the study in question. Shade-tolerant species of Psychotria
were on average sampled at shadier microsites than light-demanders, and leaf angles are known to respond plastically to light availability, with sun leaves being more steeply inclined than shade leaves (McMillen and McClendon, 1979
; Valladares and Pearcy, 1998
; Delagrange et al., 2006
The present results suggest that night-time respiration is a sizeable component of seedling carbon balance. In view of the well-known responsiveness of dark respiration to short-term changes in temperature, dark respiration rates might be expected to be lower at night. However, night-time and daytime dark respiration rates were statistically indistinguishable (Table ), despite the approx. 5° C difference between average midday and midnight temperatures. As mitochondrial respiration is strongly inhibited in the light (Villar et al., 1995
; Atkin et al., 1998
), total night-time respiratory losses by the plants studied should therefore exceed actual respiration during the daytime, even at the summer solstice when nights are shortest. We are aware of few studies reporting comparable field measurements of both daytime and night-time leaf respiration at ambient temperatures. However, a study of Quercus ilex
in a low-rainfall Mediterranean environment reported that daytime and night-time dark respiration shared a common response to temperature (Zaragoza-Castells et al., 2008
). As a result, dark respiration rates were higher during the day, in sharp contrast to the present own findings. More research would help clarify whether these two divergent results can be ascribed to environmental differences between the study sites, or to other causes.
Ontogenetic increases in self-shading nullified the expected low-light carbon gain advantages of low respiration rates in shade-tolerant species. Although Rd
was only weakly related to light requirements of the seven study species (Table ), shade-tolerant species in general have lower dark respiration rates and leaf-level compensation points than their light-demanding associates (e.g. Lusk, 2002
; Baltzer and Thomas, 2007
), leading to the expectation of that the former should have higher instantaneous net carbon gain in low light. However, this expectation was not supported by simulations incorporating the effects of self-shading at crown level, which generally indicated lower net daily carbon gain by the shade-tolerant species. Simulations were carried out in moderate shade (approx. 4·0 % light availability), and the rank order of net daily carbon gain by the study species would undoubtedly be different in deeper shade under dense rainforest canopies, where seedlings generally receive <2 % of full sunlight (Chazdon and Fetcher, 1984
; Lusk et al., 2006
). However, even under the overcast scenario, in which average PFD reaching the plants was estimated at only approx. 22 % of that penetrating the understorey on clear days, net daily carbon gain of large seedlings still tended to be lowest in shade-tolerant species (Fig. I), reflecting the considerable self-shading associated with the accumulation of four to six leaf cohorts.
The long leaf lifespans of the shade-tolerant evergreens did not result in them displaying larger effective
leaf areas in low light than their light-demanding counterparts. As reported previously for a subset of these species (Lusk, 2004
), LAR of shade-tolerant species declined more gradually with size than those of light-demanding taxa (Fig. C). However, because the ontogenetic decrease in crown silhouette-to-area ratio tended to be steepest in shade-tolerant species (Fig. F), LARd
of 500-mm-tall juveniles was not correlated with species light requirements (Table ). Accumulation of multiple leaf cohorts thus brings diminishing returns for displayed leaf area, with increasing self-shading apparently nullifying the expected advantages of long leaf lifespans for maximization of light interception by shade-tolerant species. The present findings therefore seem consistent with the view that the main advantage of long leaf lifespans in shade-tolerant evergreens is in reducing the costs of crown maintenance (King, 1994
; Walters and Reich, 1999
), rather than in maximizing light capture.
In conclusion, as far as we are aware, this is the first study to compare light interception and simulate net daily carbon gain by evergreens of differing shade tolerance in a standardized understorey environment. Integration of data on gas exchange, biomass distribution and crown architecture indicated that the shade-tolerant evergreens studied were not particularly efficient at harvesting light or fixing carbon in the understorey; this was especially true of large seedlings that bore several leaf cohorts, resulting in considerable self-shading. Rather, they appear to succeed by incrementally constructing persistent crowns that require only modest annual carbon allocation to replace losses due to foliage turnover, herbivory and mechanical damage.