Species and light environment differences in CO2 exchange and morphology
Among seedlings of five, broad-leaved cold-temperate deciduous species grown in low light, species with high whole-plant CO2 exchange at PPFD > 15 µmol quanta m−2 s−1 also had high CO2 loss rates at PPFD < 15 µmol quanta m−2 s−1. This trade-off in high vs low PPFD CO2 exchange corresponded broadly to species’ shade tolerance classifications because intolerant P. tremuloides had the greatest CO2 loss at very low PPFD and the greatest CO2 gain at low to moderately high PPFD, whereas shade-tolerant A. saccharum had the lowest CO2 loss rates at very-low PPFD and the lowest CO2 gain at low to moderately high PPFD. In cold-temperate closed-canopy forest understories, where A. saccharum seedlings are common, mean daytime light levels for most of the growing season are often < 10 µmol quanta m−2 s−1 (Ellsworth & Reich 1992; Tobin & Reich, unpublished data) which is lower than A. saccharum’s, and the other species, whole-plant CO2 compensation point in this study. Given these light environments, minimizing CO2 loss at very low PPFD could be more important for A. saccharum's whole-season carbon balance than maximizing CO2 gain at higher PPFD. In addition, A. saccharum's low LMR may benefit low-light carbon balance over the long-term because autumn leaf turnover is a lower fraction of total plant mass compared to high LMR plants (Walters & Reich 2000). In contrast to shade-tolerant A. saccharum, less tolerant species express traits (high LMR, LAR, Amax, SLA, and subsequently high RW) that suggest a predisposition to maximize growth potential even in low light, despite the possibility that light levels may be too low for these growth potential advantages to be realized. It is important to note that shade-tolerant A. saccharum had the lowest growth rates and integrated whole-plant CO2 exchange of any species in both 2·8 and 7·3% light. Thus, the light levels at which CO2 exchange would be more positive for A. saccharum than the other study species, at least for seedlings acclimated to 2·8% light, would be less than the 2·8% light treatments that the seedlings were grown in. In Walters & Reich (2000) we found that growth rates in 1·5% light were similar and near zero for A. saccharum, B. papyrifera, B. alleghaniensis and P. tremuloides, suggesting that whole-plant CO2 exchange was similar among species at that light level. However, Walters & Reich (2000) also found that seedling survival for A. saccharum was much greater than for the other species at light levels ranging from 0·6 to 7·3% light.
In contrast to the large differences in mass-based R and photosynthesis, and in biomass fractions in roots and leaves among species, leaf-area-based measures of QY and RL, and light compensation points were similar for tolerant and intolerant species, indicating that these characteristics were not important bases for differences in shade adaptation among our study species.
Although we identified potentially adaptive differences in whole-plant CO2 exchange characteristics over the entire range of reported species shade tolerances we examined (i.e. P. tremuloides to A. saccharum), the three Betulaceae species had similar CO2 exchange characteristics despite large differences in reported shade tolerance. In part, these similarities could be owing to differences in plant mass. Walters et al. (1993a) reported that respiration declined with plant mass for the same three Betulaceae species and it was lowest at a common mass for O. virginiana. In this study, mass for O. virginiana was less than half that of B. papyrifera and B. alleghaniensis. Thus, at a common mass, O. virginiana may have had a lower RW and possibly lower whole-plant CO2 loss rates at very-low PPFD than B. papyrifera and B. alleghaniensis.
Between light environments, our data support those of other studies of cold-temperate tree seedlings in indicating that: (1) plasticity in whole plant biomass distribution (i.e. LMR) is, at most, a minor component of light acclimation compared to plasticity in leaf morphology; (2) shade-intolerant species showed greater plasticity, especially in leaf characteristics, than tolerant species (see also Walters et al. 1993b;Reich, Tjoelker et al. 1998). It is important to note that, although strong and similar light effects on SLA have been reported for these species in both greenhouse/growth chamber and field experiments (Ellsworth & Reich 1992;Walters et al. 1993a,b;Walters & Reich 1996, 1997;Reich, Tjoelker et al. 1998) increasing AmaxMASS with decreasing light occurs primarily in greenhouse/growth chamber experiments (Walters et al. 1993a,b;Reich, Walters et al. 1998; this study).
Necessary caveats of our whole-plant CO2 exchange analysis include: (1) we measured respiration on washed roots at 365 µmol CO2 mol−1 and 21 °C. However, wounding, temperature (Tjoelker & Reich 1999) and CO2 (Burton et al. 1997; but not Tjoelker et al. 1999) can affect respiration rates and both temperature and soil CO2 concentration likely varied temporally in the greenhouse. Despite these and other factors affecting differences between measured and in situ rates, our strong RWvs growth relations suggest that the impact of measurement protocol on respiration was similar for all treatments; (2) our data are only relevant for first-year seedlings because morphology and CO2 exchange characteristics can change with ontogeny (Shukla & Ramakrishnan 1984; Walters et al. 1993b; Niinemets 1998); (3) greenhouse conditions do not mimic the combination of multiple resource limitations, environmental heterogeneity and biotic stresses that seedlings experience in the field (Wayne & Bazzaz 1993; Ackerly 1997). However, for O. virginiana, A. saccharum, P. tremuloides and B. alleghaniensis our greenhouse data and those for seedlings grown in forest understories (Lusk & Reich, in press) were similar in terms of rankings among species (i.e. respiration was lower in shade-tolerant species).
Low-light grown shade-tolerant A. saccharum had lower relative growth rates, LMR, SLA and whole-plant CO2 exchange at PPFD > 15 µmol quanta m−2 s−1 than intolerant P. tremuloides. These results are inconsistent with the enhanced low-light growth hypothesis of shade tolerance. Conversely, compared to P. tremuloides, A. saccharum had lower whole-plant respiration rates, which account for its lower whole-plant CO2 loss rates at PPFD < 15 µmol quanta m−2 s−1 than P. tremuloides. Three birch species (B. papyrifera, B. alleghaniensis and O. virginiana) despite large differences in reported shade tolerance, had similar characteristics and were intermediate to A. saccharum and P. tremuloides in their responses. Thus lower whole-plant respiration rates may be one of many traits underlying shade-adaptation, and they may be part of a larger resource conservation syndrome that includes traits that enhance storage and protection from herbivores, pathogens, and mechanical damage. Collectively these resource conservation traits and their possible trade-offs with enhanced low-light growth potential may account for both the higher survival and the equal to lower growth rates documented for shade-tolerant tree seedlings and saplings in low light (Lorimer 1981; Kitajima 1994; Kobe et al. 1995; Kobe & Coates 1997; Venenklaas & Poorter 1998; Walters & Reich 1996, 1999, 2000).