Temperature and air pollution affected tree ring δ13C and water-use efficiency of pine and oak trees under rising CO2 in a humid temperate forest
Introduction
Intrinsic water-use efficiency (WUEi), the ratio of net photosynthetic assimilation rate (AN) to stomatal conductance (gs) for water vapor during photosynthesis, is an integrator of the carbon gain and water loss response of trees to environmental changes, as variations in AN, gs, or both cause changes in WUEi (Farquhar et al., 1989). Among the environmental variables, the effect of rising atmospheric CO2 concentration ([CO2]) on WUEi of trees has been extensively studied to show that rising [CO2] is likely to increase WUEi across biomes (Peñuelas et al., 2011, Wang and Feng, 2012 and references cited therein). For example, WUEi of trees estimated from the carbon isotope ratio (δ13C) of annual rings has been found to increase by 20–30% with increasing atmospheric [CO2] over 50 ppmv during the second half of the 20th century (Peñuelas et al., 2011, Wang and Feng, 2012). Such responses were ascribed primarily to the rising [CO2]-induced stomatal closure that reduces the gs of trees (Ainsworth and Rogers, 2007, Peñuelas et al., 2011).
Based on responses of trees to rising [CO2], a number of single and multi-factor experiments (Dieleman et al., 2012) and earth system models (Sitch et al., 2008) have suggested that increased WUEi may enhance tree growth. In a meta-analysis based on data from 47 sites across the world, however, Peñuelas et al. (2011) found that increased WUEi during the 20th century did not translate into faster tree growth, highlighting the significant influences of other environmental constraints such as drought (Maseyk et al., 2011), warming (Wang et al., 2012), and air pollution (Li et al., 2010, Rinne et al., 2010). These constraints may negate the “CO2 fertilization effect” via either stomatal closure by drought stress under limited precipitation (Lévesque et al., 2014), warming-induced increases in photorespiration (Peñuelas et al., 2011), or stomatal closure induced by SO2 pollution (Savard et al., 2004, Rinne et al., 2010). Therefore, to better predict future forest productivity under rising [CO2], it is important to understand how WUEi and its relationship to tree growth are affected by concomitant changes of multiple environmental variables.
Among the dominant constraints, the effect of drought on gs (and thus WUEi) is very well recognized (Peñuelas et al., 2011, Wang and Feng, 2012). For example, Lévesque et al. (2014) reported that a direct drought stress (due to low precipitation) and warming-induced drought stress (due to decreased soil water availability by increased evaporation) reduced tree growth on dry sites in spite of the increased WUEi. Without the increases in WUEi, the decrease in tree growth due to drought stress could be even greater. However, changes in WUEi and their relationship with tree growth under rising [CO2] in humid regions where water is not limiting have rarely been reported. Specifically, the following questions still remain unanswered: 1) do increases in WUEi translate into faster tree growth in humid regions? 2) if not, what are the key environmental constraints that affect tree growth in such regions where water is not limiting?, and 3) may the WUEi of tree species with dissimilar ecophysiological traits show different responses to those constraints?
To answer these questions, we investigated annual changes in radial growth and WUEi in tree rings of two functionally different species, Pinus densiflora (a needle-leaved coniferous species) and Quercus variabilis (a broad-leaved deciduous species), over four decades since industrialization in South Korea in a humid temperate forest where data on multiple environmental variables including atmospheric [CO2], temperature, precipitation (P), evaporation (E), P/E, and air pollution (NOx and SO2 emissions and their atmospheric concentrations) are available. To decipher the contribution of stomatal and non-stomatal regulations to changes in WUEi, C isotope discrimination (Δ13C), the difference in δ13C between atmospheric CO2 (δ13Cair) and plant biomass C (δ13Cplant) (Farquhar et al., 1989), was calculated from tree-ring δ13C data. We hypothesized that 1) trees growing in humid regions may not be affected by seasonal drought-induced stomatal closure and thus increased WUEi under rising [CO2] may lead to increased tree growth; 2) if other stresses such as SO2 pollution- and warming-induced stresses that either cause stomatal closure or increase respiration rates of trees are imposed, however, WUEi and tree growth may be decoupled; and 3) such responses may differ between P. densiflora and Q. variabilis as the latter is known to have low stomatal sensitivity to environmental constraints (Rinne et al., 2010, Leonelli et al., 2012).
Section snippets
Site description
This study was conducted in a humid temperate forest located in Mt. Naejang (35° 26′ N, 126° 45′ E), a national park in Chonnam province in South Korea (Fig. 1). The studied forest was located approximately 20 km north of Gwangju, the fifth largest metropolis in the country. All the meteorological data including monthly temperature (average, minimum, and maximum), P and E were obtained from the Gwangju meteorological monitoring station (Fig. 1). At this station, temperature and precipitation
Patterns of BAI, δ13C, Δ13C, and WUEi
The patterns for the changes of BAI, δ13C, Δ13C, and WUEi values in tree rings over time were similar among the four trees sampled for both P. densiflora and Q. variabilis (Fig. 3, Fig. 4), suggesting that all trees of the same species experienced similar environmental conditions and responded to them similarly in spite of the different tree sizes. The similarity was confirmed by correlation analysis between trees for both species; except for BAI between QV1 and QV4, all the tree ring data were
Annual trends of BAI, Δ13C, and WUEi under rising [CO2]
Although BAI responded to rising [CO2] in a similar manner for both species, the pattern of Δ13C and WUEi under rising [CO2] differed between species (Fig. 3, Fig. 4). For P. densiflora, a decreasing trend of Δ13C (and thus increasing WUEi) (Fig. 3) in combination with a negative relationship between Δ13C and [CO2] (and thus a positive relationship between WUEi and [CO2]) (Table 3, Table 4) can be ascribed primarily to the rising [CO2]-induced reduction in the gs of trees or an increase in AN
Conclusions
At the study site located in a humid climate region, high precipitation and thus sufficient water availability seemed to lead to the lack of difference in WUEi between P. densiflora and Q. variabilis under rising [CO2]. Multiple regression models revealed that the two species react differently toward environment changes including [CO2], temperature, and air pollution and pinpointed the dominant environmental constraints of tree growth and the mechanisms of their effect on WUEi and tree growth.
Acknowledgments
We thank Dr. Brian A Schubert (University of Louisianan at Lafayette) for providing valuable information on tree ring isotope correction. We also acknowledge that the comments from three reviewers improved the earlier version of the paper. This research was supported by grants from the National Research Foundation of Korea (NRF) (grant number NRF-2011-0015758) of the Ministry of Education, Science and Technology and from the Forest Science and Technology Projects of the Korea Forest Service
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