Environmental Pollution 206 (2015) 133e141
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Growth overcompensation against O3 exposure in two Japanese oak species, Quercus mongolica var. crispula and Quercus serrata, grown under elevated CO2 Mitsutoshi Kitao*, Masabumi Komatsu, Kenichi Yazaki, Satoshi Kitaoka, Hiroyuki Tobita Department of Plant Ecology, Forestry and Forest Products Research Institute, Matsunosato 1, Tsukuba 305-8687, Japan
a r t i c l e i n f o
a b s t r a c t
Article history: Received 20 April 2015 Received in revised form 24 June 2015 Accepted 27 June 2015 Available online xxx
To assess the effects of elevated concentrations of carbon dioxide (CO2) and ozone (O3) on the growth of two mid-successional oak species native to East Asia, Quercus mongolica var. crispula and Quercus serrata, we measured gas exchange and biomass allocation in seedlings (initially 1-year-old) grown under combinations of elevated CO2 (550 mmol mol1) and O3 (twice-ambient) for two growing seasons in an open-field experiment in which root growth was not limited. Both the oak species showed a significant growth enhancement under the combination of elevated CO2 and O3 (indicated by total dry mass; over twice of ambient-grown plants, p < .05), which probably resulted from a preferable biomass partitioning into leaves induced by O3 and a predominant enhancement of photosynthesis under elevated CO2. Such an over-compensative response in the two Japanese oak species resulted in greater plant growth under the combination of elevated CO2 and O3 than elevated CO2 alone. © 2015 Published by Elsevier Ltd.
Keywords: Biomass partitioning Elevated CO2 Elevated O3 Growth Photosynthesis Quercus mongolica var. crispula Quercus serrata
1. Introduction Tropospheric ozone (O3) levels have increased globally since preindustrial times (Stockwell et al., 1997; IPCC, 2001, 2007) and continue to rise, particularly in the region of East Asia (Fowler et al., 1999, 2008; Vingarzan, 2004; Ashmore, 2005; Dentener et al., 2006). Increased O3 levels have the potential of limiting the carbon sink strength of forest ecosystems (IPCC, 2007; Sitch et al., 2007; Wittig et al., 2009; Pretzsch et al., 2010) because of reduced net photosynthesis, accelerated leaf senescence, and increased dark respiration (for review see Matyssek and Sandermann, 2003; Matyssek et al., 2010). Atmospheric carbon dioxide (CO2) concentration is predicted to double during the next century (IPCC, 2001, 2007). Elevated CO2 has been linked to increased plant growth via enhanced photosynthetic carbon assimilation (Tissue et al., 1997; Ainsworth and Long, 2005; Norby and Zak, 2011), although long-term exposure to elevated CO2 results in photosynthetic downregulation, typically a decrease in the carboxylation capacity of Rubisco (Vc,max) (Rogers and Ellsworth,
* Corresponding author. E-mail address: [email protected] (M. Kitao). http://dx.doi.org/10.1016/j.envpol.2015.06.034 0269-7491/© 2015 Published by Elsevier Ltd.
2002; Ainsworth and Long, 2005; Bernacchi et al., 2005). Quercus mongolica var. crispula (Japanese oak) and Quercus serrata (konara oak) are representative deciduous broadleaf tree species found in Japan and throughout East Asia (Menitsky, 2005). The former is mainly distributed in the cool-temperate and the latter in the warm-temperate zone of deciduous broadleaf forests in East Asia. Both species have a high sprouting ability with welldeveloped tap roots as they are commonly used for coppicing in secondary forests in Japan (Sakai et al., 1997; Sakai and Sakai, 1998). Both have mid-successional traits, i.e., moderately shade-tolerant and need a gap formation for regeneration (Higo, 1994). Their shoot development pattern is categorized as a flush and succeeding-type leaf emergence (Kikuzawa, 1983); they flush shoots generally once in spring, sometimes flushing new shoots if environmental conditions are preferable, such as gap formation. According to Yamaguchi et al. (2011), both the oak species are relatively O3 tolerant among the Japanese tree species and are related to a noted capacity for isoprene emission (Loreto and Fares, 2007; Tani and Kawawata, 2008; Miyama et al., 2013). Although there have been several studies primarily investigating the effects of elevated CO2 and/or O3 on leaf physiological and morphological traits in oak species (e.g., Velikova et al., 2005; Paoletti et al., 2007; Watanabe et al., 2007, 2013), only a few studies have investigated
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the combined effects of elevated CO2 and O3 on the growth and carbon allocation in oak species (Quercus petraea, Broadmeadow and Jackson, 2000; cf. King et al., 2013). A thorough assessment of the effects of elevated O3 and CO2 on the growth of these oak species (Q. mongolica and Q. serrata) is necessary to predict the effects of global change on the carbon sequestering capacity of forest ecosystems, particularly in East Asia. Plant growth is mainly regulated by two factors: leaf area-based carbon assimilation rate and leaf area ratio (Poorter, 1989). The former is involved in photosynthetic capacity and the latter in photosynthate allocation. O3 exposure is known to shift carbon n et al., allocation preferably into shoots (Pell et al., 1994; Sellde 1997; Landolt et al., 2000; Oksanen and Rousi, 2001), which may promote plant growth in response to the O3-induced reduction in photosynthesis (Mooney et al., 1988; Pell et al., 1994; Yamaji et al., 2003). Conversely, carbon allocation in plants grown under elevated CO2 is reported to be relatively unresponsive when compared with that in plants under the effects of O3, which are dependent on species, resource supply, and environmental factors (Rogers et al., 1996; Poorter and Nagal, 2000). In previous studies, the root to shoot ratio of Japanese white birch seedlings was considerably changed according to water and nitrogen availability, whereas no significant response was triggered by elevated CO2 (Kitao et al., 2005, 2007). Elevated CO2 concentration may alleviate the toxicological impacts of elevated O3 if elevated CO2 level is accompanied by lower stomatal conductance (Ainsworth and Long, 2005; Ainsworth and Rogers, 2007) or by a greater quantity of carbohydrates available for detoxification and repair in elevated CO2 (Riikonen et al., 2004, 2005). If greater carbon allocation into shoots directly induced by €rvi et al., 1994; Pell O3 occurs as a defense mechanism (Kangasja et al., 1994), the impact of O3 is alleviated and photosynthesis is enhanced under elevated CO2, particularly in the Quercus species that are generally less sensitive to the damaging effects of O3; this may ultimately increase plant growth as an overcompensation. We hypothesized that the growth of the two O3-tolerant oak species (Q. mongolica var. crispula and Q. serrata) native to East Asia with a plastic shoot developmental pattern (Kikuzawa, 1983) was enhanced when grown under elevated O3 and CO2 through an O3induced carbon allocation into shoots and CO2-enhanced photosynthesis exceeding O3 impacts. Furthermore, as a greater cumulative O3 uptake via higher stomatal conductance was observed in Q. mongolica than in Q. serrata (Kinose et al., 2014), O3 impact on photosynthesis would be greater in the former species leading to a less enhancement in the growth. To test this hypothesis, we investigated the growth and photosynthetic responses in the seedlings of Q. mongolica and Q. serrata grown under free-air fumigation of elevated O3 and CO2.
Table 1 Mean O3 concentrations for different daily time windows (24 h and 10 h; 7:00e17:00), AOT40 and daytime mean CO2 concentration (10 h; 7:00e17:00) for the growth periods of two years covered by the present study (April 25, 2012eNovember 20, 2012 and April 10, 2013eNovember 24, 2013). Values are the means ± SD of six frames for each treatment.
24 h O3 (ppb) 10 h O3 (ppb) AOT40 (ppm h) 10 h CO2 (ppm)
Treatment
2012
Ambient O3 Elevated O3 Ambient O3 Elevated O3 Ambient O3 Elevated O3 Ambient CO2 Elevated CO2
24.7 36.2 36.4 61.5 11.6 57.8 377 546
± ± ± ± ± ± ± ±
2013 0.3 3.0 0.5 6.2 0.4 12.8 2.9 21.3
29.1 40.6 44.3 75.3 22.8 78.4 409 531
± ± ± ± ± ± ± ±
0.4 1.2 0.9 2.3 1.1 5.4 3.4 11.6
windscreens, each 50 cm high, were placed at 15 and 75 cm, respectively, above the soil in such a way that they do not interfere with ventilation. The windscreens facilitated the optimization of the turbulent mixing of CO2 and O3, which were injected through the holes of vertical polyethylene tubes (2 m in height with 20 cm intervals around the frames) with ambient air (Erbs and Fangmeier, 2005). Four seedlings per species were planted within each frame. The treatments were as follows: control (unchanged ambient air; refer Table 1 and Fig. 1), elevated CO2 (Target set, 550 mmol mol1), elevated O3 (Target set, twice-ambient), and elevated CO2 þ O3 (550 mmol mol1 CO2 and twice-ambient O3). A total of 12 frames were installed with three replications for each treatment. Amounts of CO2 and O3 were regulated during daytime with a proportional integral derivative (PID) control system comprising digital controllers (Model SDC35, Azbil Corporation, Tokyo, Japan). Gaseous CO2 was obtained from liquid CO2 provided by AIR WATER INC. (Osaka, Japan), and O3 was produced by an ozone generator (Model PZ2A; Kofloc, Kyoto, Japan). We used two CO2 monitors (Carbon Dioxide Probe, Model GMP343; Vaisala, Helsinki, Finland) to control CO2 concentration with rapid responses; in addition, CO2 concentration in the frames was monitored by an infrared CO2 analyzer (Model LI-820; LI-COR Inc., Lincoln, Nebraska). Ozone concentration was monitored with both an O3 analyzer (Model EG3000F; Ebara Jitsugyo Co. Ltd., Kanagawa, Japan) and an O3 monitor (Model 205; 2B Technologies, Boulder, Colorado). The tree seedlings were grown for two growing seasons under the treatment combinations described above. The fumigation periods for CO2 and O3 extended from April 25, 2012 to November 20, 2012 and April 10, 2013 to November 24, 2013, respectively. Values of mean CO2 and O3 concentrations during the growth periods are shown in Table 1. Fig. 1 shows the seasonal changes in the daytime mean amounts of the ambient and elevated O3 treatments. Mean monthly
2. Materials and methods 2.1. Plant materials, and carbon dioxide and ozone exposure The experimental field is located at the nursery of Forestry and Forest Products Research Institute in Tsukuba, Japan (36 000 N, 140 080 E, 20 m a.s.l.). Twelve frames were installed for CO2 and O3 exposure. One-year-old seedlings of Japanese oak (Q. mongolica Fisch. ex Ledeb. var. crispula (Blume) H. Ohashi) and Konara oak (Q. serrata Murray) approximately 5 cm in height under dormancy were transplanted directly to the ground in the frames at the end of March in 2012. Before transplanting, the seedlings were grown under ambient air for about 1 year after seed germination. The tree seedlings were grown and fumigated in octagonal frames 2 m in height separated by a distance of 3 m between the opposite edges and surrounded by transparent windscreens. Two transparent
Fig. 1. Seasonal changes in daytime mean O3 concentration (7:00e17:00) in the ambient (solid) and elevated O3 treatments (dashed line) in 2013. Arrows indicate the onset of first and second shoots.
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temperatures from April to October for the two growth periods ranged from 12.3 C to 27.5 C with a mean of 20.6 C. Precipitation for the growth period (AprileOctober) was 806 and 1026 mm for 2012 and 2013, respectively. 2.2. Biomass and biomass partitioning At the end of the experiments (November 2013) after two growth seasons, all seedlings of the two oak species were harvested. We used an air excavation tool (Air Schop, KF Company, Sakai, Japan) provided with an engine compressor (PDS175S, Hokuetsu Industries, Tokyo, Japan) to loosen soils with compressed air. The loosened soils were carefully removed by hand using small stainless steel rakes (Bonsai rake, Kikuwa, Sanjo, Niigata, Japan) to collect roots as intact as possible. Above-ground biomass (leaves, main shoot, and lateral shoots, individually) and below-ground biomass (roots) were measured after oven-drying at 70 C to a constant weight. Leaf area was measured for all the leaves that were still attached using a leaf area meter (LI-3100C, LI-COR). Leaf mass ratio (LMR), main shoot mass ratio (MSMR), lateral shoot mass ratio (LSMR), or root mass ratio (RMR) was calculated as the ratio of dry mass of each organ to the total dry mass. Leaf area ratio (LAR) was determined as the total leaf area per total dry mass.
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combinations were 1.0, 2.0, 2.8, and 3.4 for the first-flushed leaves and 2.3, 2.9, 3.5, and 3.6 for the second-flushed leaves. In Q. serrata, they were 1.0, 2.0, 3.0, and 3.9 for the first-flushed leaves and 2.4, 3.1, 3.9, and 4.8 for the second-flushed leaves. To investigate the integrated effects of CO2 and O3 on photosynthetic carbon assimilation at the leaf level, we calculated the weighted mean An for the first and second flushed leaves for four sequences, with measurements as follows:
tend
1 tstart
Ztend An dt;
(1)
tstart
where tstart is the leaf age at the first measurement and tend is that at the last measurement, with a corresponding leaf age of approximately 30 days and 120 days, respectively. (Note, we proceeded under the assumption that An changed linearly between the two adjacent measurements.) Weighted mean gs was also calculated as:
tend
1 tstart
Ztend gs dt:
(2)
tstart
2.3. Gas exchange measurements 2.5. Statistical analysis Measurements of gas exchange were conducted during the second growth season in 2013. Seasonal changes in photosynthetic traits were monitored for the first and second flushed leaves in Q. mongolica and Q. serrata. For both species, the first flushes were observed at the beginning of April and the second flushes were observed at the end of May 2013. Averaged daytime mean O3 (7:00e17:00) during an interval of 120 days after the first and second flush were 50 ppb and 47 ppb under ambient O3 and 85 and 81 ppb under elevated O3 treatment, respectively (cf. Fig. 1). Measurements of net photosynthetic rate (An) and stomatal conductance (gs) at ambient (380 mmol mol1) and elevated CO2 (550 mmol mol1) concentrations were conducted for leaves of three to four individual seedlings per treatment combination using a portable photosynthesis system (Model LI-6400; LI-COR). Measurements were carried out under the block temperature set at 27 C and saturating light intensity of 1500 mmol m2 s1, the latter provided by a red/blue LED array (LI-6400-40, LI-COR) with blue light comprising 10% of the total PFD (photon flux density). We chose a light intensity (1500 mmol m2 s1), which was sufficient to saturate the net photosynthetic rate in both the oak species based on a preliminary study. The gas exchange measurements were conducted from 9:00 to 15:00. To circumvent midday depression of photosynthesis, sunscreens were placed at the top of the frames in the morning to prevent direct sunlight onto the leaves used for the measurements. The mean light intensity under the sunscreens during the measurements was c.a. 200 mmol m2 s1.
All statistics were based on the mean value of the individual frame (CO2 O3 regime) as the sample unit (n ¼ 3). These values were then averaged to provide the sample estimate for that replicate. A split-plot ANOVA (CO2 O3 regime species) was used to test the differences in the weighted means of gas exchange parameters (An, gs) and the dry mass of different organs (R Development Core Team, 2014). A two-factorial ANOVA (CO2 O3) was also conducted for each species. Furthermore, when the interaction term between CO2 and O3 proved significant, the differences in their means among the combinations of CO2 and O3 were retested using one-factorial ANOVA and Holm's pairwise comparisons (Sokal and Rohlf, 1995). 3. Results 3.1. Growth responses to elevated CO2 and O3 in Q. mongolica and Q. serrata In the present study, it is noteworthy that root growth was not limited to direct planting into the soils, allowing oak seedlings to
2.4. Weighted mean photosynthetic rate and stomatal conductance We measured the seasonal changes in gas exchange in the firstand second-flushed leaves of Q. mongolica and Q. serrata four times during the growing season at the leaf age of approximately 30, 60, 90, and 120 days. There were no significant differences in the total number of flushes in the main shoots among the treatment combinations at each measurement date for Q. mongolica or Q. serrata. In Q. mongolica, the mean numbers of total flushes in the main shoots for each measurement sequence across the treatment
Fig. 2. Dry mass of different organs of the seedlings of Q. mongolica (a) and Q. serrata (b) grown under ambient air (Amb), elevated CO2 (CO2), elevated O3 (O3), and the combination of elevated CO2 and O3(CO2 þ O3). Values are means (þSE for total dry mass) (n ¼ 3).
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Table 2 Dry mass of plant organs of the seedlings of Q. mongolica and Q. serrata grown under CO2 and O3 treatment combinations for two growth periods. Values are means ± SE of three replicates for each species and treatment. Different letters indicate significant differences between the treatment combinations (P < .05, by one-factorial ANOVA and Holm's pairwise comparisons applied when the interaction term between CO2 and O3 was significant for each species). Main effects of CO2, O3, species, and their interactions are summarized in Table 3. Total Q. mongolica Ambient CO2 O3 CO2 þ O3 Q. serrata Ambient CO2 O3 CO2 þ O3
Root
Main shoot
Lateral shoot
Leaf biomass
Leaf area (m2)
283a 283a 279a 690b
± ± ± ±
6 51 4 57
133 149 125 252
± ± ± ±
5 37 11 19
58a 47a 44a 194b
± ± ± ±
2 4 4 28
54a 43a 53a 150b
± ± ± ±
6 7 8 17
38a 43a 57a 94b
± ± ± ±
2 7 4 5
0.42a 0.44a 0.64a 0.96b
± ± ± ±
0.01 0.05 0.03 0.05
320 367 482 767
± ± ± ±
67 48 36 61
135 157 183 270
± ± ± ±
31 21 14 17
82 103 158 246
± ± ± ±
18 21 13 40
38a 36a 45a 98b
± ± ± ±
7 2 4 13
66a 71a 97a 153b
± ± ± ±
12 6 8 6
0.70 0.74 1.03 1.61
± ± ± ±
0.13 0.06 0.07 0.12
Table 3 The P values for the main effects of CO2, O3, species, and their interactions on the dry mass of different organs of the seedlings of Q. mongolica and Q. serrata by split-plot ANOVA. Two-factorial ANOVA (CO2 O3) was also conducted for each species.* denotes significant differences at P < .05,**P < .01, and***P < .001. Effect Q. mongolica þ Q. serrata CO2 O3 CO2 O3 Species CO2 Species O3 Species CO2 O3 Species Q. mongolica CO2 O3 CO2 O3 Q. serrata CO2 O3 CO2 O3
Total
Root
Main shoot
Lateral shoot
Leaf
Leaf area
0.005** 0.001** 0.011* 0.011* 0.532 0.229 0.190
0.014* 0.013* 0.061 0.257 0.644 0.370 0.527
0.028* 0.005** 0.039* ambient: 58b g > CO2: 47b g > O3: 44b g (different letters indicate significant differences at
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Table 5 The P values for the main effects of CO2, O3, species, and their interactions on dry mass allocation ratio of different organs of the seedlings of Q. mongolica and Q. serrata by splitplot ANOVA. Two-factorial ANOVA (CO2 O3) was also conducted for each species.* denotes significant differences at P < .05,**P < .01, and***P < .001. Effect Q. mongolica þ Q. serrata CO2 O3 CO2 O3 Species CO2 Species O3 Species CO2 O3 Species Q. mongolica CO2 O3 CO2 O3 Q. serrata CO2 O3 CO2 O3
RMR
MSMR
LSMR
LMR
LAR
S:R ratio
0.317 0.006** 0.299 CO2: 0.16ab > ambient: 0.15b > CO2 þ O3: 0.15b
Generally, elevated CO2 would increase the total biomass of trees via enhanced photosynthesis (Tissue et al., 1997; Ainsworth and Long, 2005; Ainsworth and Rogers, 2007; Norby and Zak, 2011), whereas elevated O3 may decrease tree growth because of reduced photosynthesis (Matyssek and Sandermann, 2003; Matyssek et al., 2010; Pretsch et al., 2010; Kitao et al., 2009, 2012). Earlier studies showed that growth enhancement by elevated CO2 was consistently negated by elevated O3 in Populus tremuloides in the FACE experiment (Isebrands et al., 2001; Karnosky et al., 2003; Talhelm et al., 2014), as well as in the fieldgrown seedlings of Q. petraea, Fraxinus excelsior, and Pinus sylvetris in an open top chamber (OTC) experiment (Broadmeadow and Jackson, 2000). Conversely, no significant effects of elevated CO2 and/or O3 on the total dry mass were observed in potted seedlings of three Japanese birch species (Betula platyphylla var. japonica, Betula ermanii, and Betula maximowicziana) (Hoshika et al., 2012), while elevated CO2 increased the total dry mass of
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the field-grown silver birch (Betula pendula) without any effect of elevated O3 in the OTC experiments (Riikonen et al., 2004). In contrast to the previous studies, the growth of Q. mongolica was significantly stimulated by the combination of elevated CO2 and O3, and the growth of Q. serrata was significantly increased even by elevated O3 as well as by elevated CO2 (Fig. 2). Consistent with this finding, Watanabe et al. (2010) reported growth stimulation under the combination of elevated CO2 and O3 in the potted seedlings of Japanese beech (Fagus crenata), which is a typical late-successional species with a flush-type leaf emergence (Kikuzawa et al., 1983). An O3-induced preferable carbon allocation into shoots was n et al., 1997; observed in the two Japanese oak species (Sellde Landolt et al., 2000; Oksanen and Rousi, 2001), which could have compensating effects for plant growth in response to the O3induced reduction in photosynthesis (Mooney et al., 1988; Pell et al., 1994; Yamaji et al., 2003). The fraction of biomass partitioning into leaves (i.e., LMR) generally decreases with increasing plant size through an ontogenetic shift (Walters et al., 1993; King, 2003; Poorter et al., 2011). In our study, however, no significant decreases in LMR and LAR were observed in either oak species, despite the significantly greater total biomass under elevated O3 (Fig. 2, Tables 4 and 5). These findings seem to suggest a substantially higher biomass allocation into leaves induced by elevated O3. Apparently, the seedlings of Q. mongolica grown under elevated O3 showed a preferable allocation into leaves, as indicated by the higher LMR and LAR in the case of no total biomass enhancement (Table 4). An O3-induced increase in carbon allocation into shoots, particularly into leaves, may be dependent on species-specific shoot development patterns. The two Japanese oak species used in the present study are known to have a high ability for plastic growth because both show a flush and succeeding-type shoot development in response to a forest gap formation (Kikuzawa, 1983; Kitao et al., 2000, 2006) and naturally large root systems with considerable sprouting capacity (Sakai et al., 1997; Sakai and Sakai, 1998). Similarly, Calatayud et al. (2011) reported that elevated O3 could increase the S:R ratio in the European oak species (Quercus ilex, Quercus faginea, Quercus pyrenaica, and Quercus robur), with no decrease in total biomass, despite a reduction in the photosynthetic rate. However, Broadmeadow and Jackson (2000) showed that elevated O3 had no effect on the S:R ratio of Q. petraea and instead decreased its growth. A typical late-successional species, F. crenata, which has a flush-type leaf emergence (generally flushes once in spring), showed higher LMR in the secondflushed leaves of potted seedlings grown under the combination of elevated CO2 and O3, accompanied with growth stimulation as well (Watanabe et al., 2010). Conversely, field-grown aspen (P. tremuloides) (Karnosky et al., 2005), field-grown silver birch (B. pendula) (Yamaji et al., 2003; Riikonen et al., 2004), and pot-grown Japanese birches (Hoshika et al., 2012), categorized as fast-growing pioneer species, showed less response in carbon allocation into shoots when exposed to elevated O3. Thus, we speculate that carbon allocation in mid- and late-successional tree species with inherently conservative shoot growth patterns may be influenced by elevated O3 more markedly than in pioneer tree species, which have an intrinsically preferable carbon allocation into shoot with succeeding-type leaf emergence (Kikuzawa, 1983). A significant decrease in net photosynthetic rate (An) was observed in the older leaves of both oak species grown under elevated O3 (Fig. 3); this suggests an earlier leaf senescence induced by O3 as that observed at the late growth season in B. pendula (Yamaji et al., 2003) and certain European oak species (Calatayud et al., 2011). Although both Japanese oak species are known to be O3 tolerant (Yamaguchi et al., 2011), weighted mean An in Q. mongolica was more sensitive to O3 exposure than that in Q. serrata
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(Fig. 4). This may be attributed to the greater O3 uptake via higher stomatal conductance of Q. mongolica (Fig. 5) (Kinose et al., 2014; Matyssek et al., 2015). Even though Q. serrata showed lower weighted mean An than Q. mongolica (Fig. 4), the higher ratio of leaf to total biomass in Q. serrata (Tables 4 and 5) could compensate for the lower capacity of photosynthesis (Poorter, 1989). Tree species, such as Q. serrata, having a lower photosynthetic capacity with lower stomatal conductance but higher leaf mass or area ratio could circumvent the negative effects of O3 through less O3 uptake (Matyssek et al., 2015). In addition, a decrease in stomatal conductance under elevated CO2, as marginally observed in Q. serrata (Fig. 5), would contribute to suppressing O3 uptake (cf. Uddling et al., 2010). Significant growth enhancement observed in plants grown under the combination of elevated CO2 and O3 may result from the preferable biomass allocation into leaves by elevated O3 and photosynthetic rates enhanced by elevated CO2. Total biomass of Q. mongolica seedlings grown under elevated O3 was not different from that grown under ambient conditions, possibly because of a decreased photosynthetic rate offset by an increased partitioning into leaves (Poorter, 1989; Okusanen and Rousi, 2001; Yamaji et al., 2003; Calatayud et al., 2011). Based on the leaf and whole plantlevel responses in the present study, it would appear that the increased partitioning into leaves was not perfectly regulated to compensate for the decrease in photosynthetic carbon gain by elevated O3, but was instead directly regulated by O3. Winwood et al. (2007) reported that elevated O3 enhanced cytokinin transfer from roots to shoots through xylem in adult beech trees (Fagus sylvatica) to compensate for the destruction of cytokinins in leaves by elevated O3. Moreover, trans-zeatin-type cytokinins, key hormones synthesized in roots, enhance shoot growth when transferred through xylem flow (Sakakibara, 2006; Kiba et al., 2013). Such an effect of O3 on plant hormones may directly increase carbon allocation into leaves, thereby enhancing total plant growth independent of an O3-induced decline in photosynthesis. In conclusion, two Japanese oak species, Q. mongolica and Q. serrata, showed significant growth enhancement under the combination of elevated CO2 and O3, possibly because of preferable biomass partitioning into leaves and a predominant enhancement of photosynthesis. Such an overcompensatory growth response in the seedlings of mid-successional oak species under oncoming atmospheric conditions would improve the competitive ability of the trees at an early stage of forest regeneration and favorably shift species composition. Acknowledgments We thank Dr. Morikawa for his valuable suggestions concerning the present study. This work was supported in part by the project on “Technology development for circulatory food production systems responsive to climate change” conducted by the Ministry of Agriculture, Forestry and Fisheries, Japan, the Grant-in-Aid for Scientific Research (B) (No. 25292092) and the Grant-in-Aid for Scientific Research on Innovative Areas (No. 22114514). Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.envpol.2015.06.034. References Ainsworth, E.A., Long, S.P., 2005. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New. Phytol.
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Growth overcompensation against O3 exposure in two Japanese oak species, Quercus mongolica var. crispula and Quercus serrata, grown under elevated CO2 Mitsutoshi Kitao*, Masabumi Komatsu, Kenichi Yazaki, Satoshi Kitaoka, Hiroyuki Tobita Department of Plant Ecology, Forestry and Forest Products Research Institute, Matsunosato 1, Tsukuba 305-8687, Japan
a r t i c l e i n f o
a b s t r a c t
Article history: Received 20 April 2015 Received in revised form 24 June 2015 Accepted 27 June 2015 Available online xxx
To assess the effects of elevated concentrations of carbon dioxide (CO2) and ozone (O3) on the growth of two mid-successional oak species native to East Asia, Quercus mongolica var. crispula and Quercus serrata, we measured gas exchange and biomass allocation in seedlings (initially 1-year-old) grown under combinations of elevated CO2 (550 mmol mol1) and O3 (twice-ambient) for two growing seasons in an open-field experiment in which root growth was not limited. Both the oak species showed a significant growth enhancement under the combination of elevated CO2 and O3 (indicated by total dry mass; over twice of ambient-grown plants, p < .05), which probably resulted from a preferable biomass partitioning into leaves induced by O3 and a predominant enhancement of photosynthesis under elevated CO2. Such an over-compensative response in the two Japanese oak species resulted in greater plant growth under the combination of elevated CO2 and O3 than elevated CO2 alone. © 2015 Published by Elsevier Ltd.
Keywords: Biomass partitioning Elevated CO2 Elevated O3 Growth Photosynthesis Quercus mongolica var. crispula Quercus serrata
1. Introduction Tropospheric ozone (O3) levels have increased globally since preindustrial times (Stockwell et al., 1997; IPCC, 2001, 2007) and continue to rise, particularly in the region of East Asia (Fowler et al., 1999, 2008; Vingarzan, 2004; Ashmore, 2005; Dentener et al., 2006). Increased O3 levels have the potential of limiting the carbon sink strength of forest ecosystems (IPCC, 2007; Sitch et al., 2007; Wittig et al., 2009; Pretzsch et al., 2010) because of reduced net photosynthesis, accelerated leaf senescence, and increased dark respiration (for review see Matyssek and Sandermann, 2003; Matyssek et al., 2010). Atmospheric carbon dioxide (CO2) concentration is predicted to double during the next century (IPCC, 2001, 2007). Elevated CO2 has been linked to increased plant growth via enhanced photosynthetic carbon assimilation (Tissue et al., 1997; Ainsworth and Long, 2005; Norby and Zak, 2011), although long-term exposure to elevated CO2 results in photosynthetic downregulation, typically a decrease in the carboxylation capacity of Rubisco (Vc,max) (Rogers and Ellsworth,
* Corresponding author. E-mail address: [email protected] (M. Kitao). http://dx.doi.org/10.1016/j.envpol.2015.06.034 0269-7491/© 2015 Published by Elsevier Ltd.
2002; Ainsworth and Long, 2005; Bernacchi et al., 2005). Quercus mongolica var. crispula (Japanese oak) and Quercus serrata (konara oak) are representative deciduous broadleaf tree species found in Japan and throughout East Asia (Menitsky, 2005). The former is mainly distributed in the cool-temperate and the latter in the warm-temperate zone of deciduous broadleaf forests in East Asia. Both species have a high sprouting ability with welldeveloped tap roots as they are commonly used for coppicing in secondary forests in Japan (Sakai et al., 1997; Sakai and Sakai, 1998). Both have mid-successional traits, i.e., moderately shade-tolerant and need a gap formation for regeneration (Higo, 1994). Their shoot development pattern is categorized as a flush and succeeding-type leaf emergence (Kikuzawa, 1983); they flush shoots generally once in spring, sometimes flushing new shoots if environmental conditions are preferable, such as gap formation. According to Yamaguchi et al. (2011), both the oak species are relatively O3 tolerant among the Japanese tree species and are related to a noted capacity for isoprene emission (Loreto and Fares, 2007; Tani and Kawawata, 2008; Miyama et al., 2013). Although there have been several studies primarily investigating the effects of elevated CO2 and/or O3 on leaf physiological and morphological traits in oak species (e.g., Velikova et al., 2005; Paoletti et al., 2007; Watanabe et al., 2007, 2013), only a few studies have investigated
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the combined effects of elevated CO2 and O3 on the growth and carbon allocation in oak species (Quercus petraea, Broadmeadow and Jackson, 2000; cf. King et al., 2013). A thorough assessment of the effects of elevated O3 and CO2 on the growth of these oak species (Q. mongolica and Q. serrata) is necessary to predict the effects of global change on the carbon sequestering capacity of forest ecosystems, particularly in East Asia. Plant growth is mainly regulated by two factors: leaf area-based carbon assimilation rate and leaf area ratio (Poorter, 1989). The former is involved in photosynthetic capacity and the latter in photosynthate allocation. O3 exposure is known to shift carbon n et al., allocation preferably into shoots (Pell et al., 1994; Sellde 1997; Landolt et al., 2000; Oksanen and Rousi, 2001), which may promote plant growth in response to the O3-induced reduction in photosynthesis (Mooney et al., 1988; Pell et al., 1994; Yamaji et al., 2003). Conversely, carbon allocation in plants grown under elevated CO2 is reported to be relatively unresponsive when compared with that in plants under the effects of O3, which are dependent on species, resource supply, and environmental factors (Rogers et al., 1996; Poorter and Nagal, 2000). In previous studies, the root to shoot ratio of Japanese white birch seedlings was considerably changed according to water and nitrogen availability, whereas no significant response was triggered by elevated CO2 (Kitao et al., 2005, 2007). Elevated CO2 concentration may alleviate the toxicological impacts of elevated O3 if elevated CO2 level is accompanied by lower stomatal conductance (Ainsworth and Long, 2005; Ainsworth and Rogers, 2007) or by a greater quantity of carbohydrates available for detoxification and repair in elevated CO2 (Riikonen et al., 2004, 2005). If greater carbon allocation into shoots directly induced by €rvi et al., 1994; Pell O3 occurs as a defense mechanism (Kangasja et al., 1994), the impact of O3 is alleviated and photosynthesis is enhanced under elevated CO2, particularly in the Quercus species that are generally less sensitive to the damaging effects of O3; this may ultimately increase plant growth as an overcompensation. We hypothesized that the growth of the two O3-tolerant oak species (Q. mongolica var. crispula and Q. serrata) native to East Asia with a plastic shoot developmental pattern (Kikuzawa, 1983) was enhanced when grown under elevated O3 and CO2 through an O3induced carbon allocation into shoots and CO2-enhanced photosynthesis exceeding O3 impacts. Furthermore, as a greater cumulative O3 uptake via higher stomatal conductance was observed in Q. mongolica than in Q. serrata (Kinose et al., 2014), O3 impact on photosynthesis would be greater in the former species leading to a less enhancement in the growth. To test this hypothesis, we investigated the growth and photosynthetic responses in the seedlings of Q. mongolica and Q. serrata grown under free-air fumigation of elevated O3 and CO2.
Table 1 Mean O3 concentrations for different daily time windows (24 h and 10 h; 7:00e17:00), AOT40 and daytime mean CO2 concentration (10 h; 7:00e17:00) for the growth periods of two years covered by the present study (April 25, 2012eNovember 20, 2012 and April 10, 2013eNovember 24, 2013). Values are the means ± SD of six frames for each treatment.
24 h O3 (ppb) 10 h O3 (ppb) AOT40 (ppm h) 10 h CO2 (ppm)
Treatment
2012
Ambient O3 Elevated O3 Ambient O3 Elevated O3 Ambient O3 Elevated O3 Ambient CO2 Elevated CO2
24.7 36.2 36.4 61.5 11.6 57.8 377 546
± ± ± ± ± ± ± ±
2013 0.3 3.0 0.5 6.2 0.4 12.8 2.9 21.3
29.1 40.6 44.3 75.3 22.8 78.4 409 531
± ± ± ± ± ± ± ±
0.4 1.2 0.9 2.3 1.1 5.4 3.4 11.6
windscreens, each 50 cm high, were placed at 15 and 75 cm, respectively, above the soil in such a way that they do not interfere with ventilation. The windscreens facilitated the optimization of the turbulent mixing of CO2 and O3, which were injected through the holes of vertical polyethylene tubes (2 m in height with 20 cm intervals around the frames) with ambient air (Erbs and Fangmeier, 2005). Four seedlings per species were planted within each frame. The treatments were as follows: control (unchanged ambient air; refer Table 1 and Fig. 1), elevated CO2 (Target set, 550 mmol mol1), elevated O3 (Target set, twice-ambient), and elevated CO2 þ O3 (550 mmol mol1 CO2 and twice-ambient O3). A total of 12 frames were installed with three replications for each treatment. Amounts of CO2 and O3 were regulated during daytime with a proportional integral derivative (PID) control system comprising digital controllers (Model SDC35, Azbil Corporation, Tokyo, Japan). Gaseous CO2 was obtained from liquid CO2 provided by AIR WATER INC. (Osaka, Japan), and O3 was produced by an ozone generator (Model PZ2A; Kofloc, Kyoto, Japan). We used two CO2 monitors (Carbon Dioxide Probe, Model GMP343; Vaisala, Helsinki, Finland) to control CO2 concentration with rapid responses; in addition, CO2 concentration in the frames was monitored by an infrared CO2 analyzer (Model LI-820; LI-COR Inc., Lincoln, Nebraska). Ozone concentration was monitored with both an O3 analyzer (Model EG3000F; Ebara Jitsugyo Co. Ltd., Kanagawa, Japan) and an O3 monitor (Model 205; 2B Technologies, Boulder, Colorado). The tree seedlings were grown for two growing seasons under the treatment combinations described above. The fumigation periods for CO2 and O3 extended from April 25, 2012 to November 20, 2012 and April 10, 2013 to November 24, 2013, respectively. Values of mean CO2 and O3 concentrations during the growth periods are shown in Table 1. Fig. 1 shows the seasonal changes in the daytime mean amounts of the ambient and elevated O3 treatments. Mean monthly
2. Materials and methods 2.1. Plant materials, and carbon dioxide and ozone exposure The experimental field is located at the nursery of Forestry and Forest Products Research Institute in Tsukuba, Japan (36 000 N, 140 080 E, 20 m a.s.l.). Twelve frames were installed for CO2 and O3 exposure. One-year-old seedlings of Japanese oak (Q. mongolica Fisch. ex Ledeb. var. crispula (Blume) H. Ohashi) and Konara oak (Q. serrata Murray) approximately 5 cm in height under dormancy were transplanted directly to the ground in the frames at the end of March in 2012. Before transplanting, the seedlings were grown under ambient air for about 1 year after seed germination. The tree seedlings were grown and fumigated in octagonal frames 2 m in height separated by a distance of 3 m between the opposite edges and surrounded by transparent windscreens. Two transparent
Fig. 1. Seasonal changes in daytime mean O3 concentration (7:00e17:00) in the ambient (solid) and elevated O3 treatments (dashed line) in 2013. Arrows indicate the onset of first and second shoots.
M. Kitao et al. / Environmental Pollution 206 (2015) 133e141
temperatures from April to October for the two growth periods ranged from 12.3 C to 27.5 C with a mean of 20.6 C. Precipitation for the growth period (AprileOctober) was 806 and 1026 mm for 2012 and 2013, respectively. 2.2. Biomass and biomass partitioning At the end of the experiments (November 2013) after two growth seasons, all seedlings of the two oak species were harvested. We used an air excavation tool (Air Schop, KF Company, Sakai, Japan) provided with an engine compressor (PDS175S, Hokuetsu Industries, Tokyo, Japan) to loosen soils with compressed air. The loosened soils were carefully removed by hand using small stainless steel rakes (Bonsai rake, Kikuwa, Sanjo, Niigata, Japan) to collect roots as intact as possible. Above-ground biomass (leaves, main shoot, and lateral shoots, individually) and below-ground biomass (roots) were measured after oven-drying at 70 C to a constant weight. Leaf area was measured for all the leaves that were still attached using a leaf area meter (LI-3100C, LI-COR). Leaf mass ratio (LMR), main shoot mass ratio (MSMR), lateral shoot mass ratio (LSMR), or root mass ratio (RMR) was calculated as the ratio of dry mass of each organ to the total dry mass. Leaf area ratio (LAR) was determined as the total leaf area per total dry mass.
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combinations were 1.0, 2.0, 2.8, and 3.4 for the first-flushed leaves and 2.3, 2.9, 3.5, and 3.6 for the second-flushed leaves. In Q. serrata, they were 1.0, 2.0, 3.0, and 3.9 for the first-flushed leaves and 2.4, 3.1, 3.9, and 4.8 for the second-flushed leaves. To investigate the integrated effects of CO2 and O3 on photosynthetic carbon assimilation at the leaf level, we calculated the weighted mean An for the first and second flushed leaves for four sequences, with measurements as follows:
tend
1 tstart
Ztend An dt;
(1)
tstart
where tstart is the leaf age at the first measurement and tend is that at the last measurement, with a corresponding leaf age of approximately 30 days and 120 days, respectively. (Note, we proceeded under the assumption that An changed linearly between the two adjacent measurements.) Weighted mean gs was also calculated as:
tend
1 tstart
Ztend gs dt:
(2)
tstart
2.3. Gas exchange measurements 2.5. Statistical analysis Measurements of gas exchange were conducted during the second growth season in 2013. Seasonal changes in photosynthetic traits were monitored for the first and second flushed leaves in Q. mongolica and Q. serrata. For both species, the first flushes were observed at the beginning of April and the second flushes were observed at the end of May 2013. Averaged daytime mean O3 (7:00e17:00) during an interval of 120 days after the first and second flush were 50 ppb and 47 ppb under ambient O3 and 85 and 81 ppb under elevated O3 treatment, respectively (cf. Fig. 1). Measurements of net photosynthetic rate (An) and stomatal conductance (gs) at ambient (380 mmol mol1) and elevated CO2 (550 mmol mol1) concentrations were conducted for leaves of three to four individual seedlings per treatment combination using a portable photosynthesis system (Model LI-6400; LI-COR). Measurements were carried out under the block temperature set at 27 C and saturating light intensity of 1500 mmol m2 s1, the latter provided by a red/blue LED array (LI-6400-40, LI-COR) with blue light comprising 10% of the total PFD (photon flux density). We chose a light intensity (1500 mmol m2 s1), which was sufficient to saturate the net photosynthetic rate in both the oak species based on a preliminary study. The gas exchange measurements were conducted from 9:00 to 15:00. To circumvent midday depression of photosynthesis, sunscreens were placed at the top of the frames in the morning to prevent direct sunlight onto the leaves used for the measurements. The mean light intensity under the sunscreens during the measurements was c.a. 200 mmol m2 s1.
All statistics were based on the mean value of the individual frame (CO2 O3 regime) as the sample unit (n ¼ 3). These values were then averaged to provide the sample estimate for that replicate. A split-plot ANOVA (CO2 O3 regime species) was used to test the differences in the weighted means of gas exchange parameters (An, gs) and the dry mass of different organs (R Development Core Team, 2014). A two-factorial ANOVA (CO2 O3) was also conducted for each species. Furthermore, when the interaction term between CO2 and O3 proved significant, the differences in their means among the combinations of CO2 and O3 were retested using one-factorial ANOVA and Holm's pairwise comparisons (Sokal and Rohlf, 1995). 3. Results 3.1. Growth responses to elevated CO2 and O3 in Q. mongolica and Q. serrata In the present study, it is noteworthy that root growth was not limited to direct planting into the soils, allowing oak seedlings to
2.4. Weighted mean photosynthetic rate and stomatal conductance We measured the seasonal changes in gas exchange in the firstand second-flushed leaves of Q. mongolica and Q. serrata four times during the growing season at the leaf age of approximately 30, 60, 90, and 120 days. There were no significant differences in the total number of flushes in the main shoots among the treatment combinations at each measurement date for Q. mongolica or Q. serrata. In Q. mongolica, the mean numbers of total flushes in the main shoots for each measurement sequence across the treatment
Fig. 2. Dry mass of different organs of the seedlings of Q. mongolica (a) and Q. serrata (b) grown under ambient air (Amb), elevated CO2 (CO2), elevated O3 (O3), and the combination of elevated CO2 and O3(CO2 þ O3). Values are means (þSE for total dry mass) (n ¼ 3).
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M. Kitao et al. / Environmental Pollution 206 (2015) 133e141
Table 2 Dry mass of plant organs of the seedlings of Q. mongolica and Q. serrata grown under CO2 and O3 treatment combinations for two growth periods. Values are means ± SE of three replicates for each species and treatment. Different letters indicate significant differences between the treatment combinations (P < .05, by one-factorial ANOVA and Holm's pairwise comparisons applied when the interaction term between CO2 and O3 was significant for each species). Main effects of CO2, O3, species, and their interactions are summarized in Table 3. Total Q. mongolica Ambient CO2 O3 CO2 þ O3 Q. serrata Ambient CO2 O3 CO2 þ O3
Root
Main shoot
Lateral shoot
Leaf biomass
Leaf area (m2)
283a 283a 279a 690b
± ± ± ±
6 51 4 57
133 149 125 252
± ± ± ±
5 37 11 19
58a 47a 44a 194b
± ± ± ±
2 4 4 28
54a 43a 53a 150b
± ± ± ±
6 7 8 17
38a 43a 57a 94b
± ± ± ±
2 7 4 5
0.42a 0.44a 0.64a 0.96b
± ± ± ±
0.01 0.05 0.03 0.05
320 367 482 767
± ± ± ±
67 48 36 61
135 157 183 270
± ± ± ±
31 21 14 17
82 103 158 246
± ± ± ±
18 21 13 40
38a 36a 45a 98b
± ± ± ±
7 2 4 13
66a 71a 97a 153b
± ± ± ±
12 6 8 6
0.70 0.74 1.03 1.61
± ± ± ±
0.13 0.06 0.07 0.12
Table 3 The P values for the main effects of CO2, O3, species, and their interactions on the dry mass of different organs of the seedlings of Q. mongolica and Q. serrata by split-plot ANOVA. Two-factorial ANOVA (CO2 O3) was also conducted for each species.* denotes significant differences at P < .05,**P < .01, and***P < .001. Effect Q. mongolica þ Q. serrata CO2 O3 CO2 O3 Species CO2 Species O3 Species CO2 O3 Species Q. mongolica CO2 O3 CO2 O3 Q. serrata CO2 O3 CO2 O3
Total
Root
Main shoot
Lateral shoot
Leaf
Leaf area
0.005** 0.001** 0.011* 0.011* 0.532 0.229 0.190
0.014* 0.013* 0.061 0.257 0.644 0.370 0.527
0.028* 0.005** 0.039* ambient: 58b g > CO2: 47b g > O3: 44b g (different letters indicate significant differences at
M. Kitao et al. / Environmental Pollution 206 (2015) 133e141
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Table 5 The P values for the main effects of CO2, O3, species, and their interactions on dry mass allocation ratio of different organs of the seedlings of Q. mongolica and Q. serrata by splitplot ANOVA. Two-factorial ANOVA (CO2 O3) was also conducted for each species.* denotes significant differences at P < .05,**P < .01, and***P < .001. Effect Q. mongolica þ Q. serrata CO2 O3 CO2 O3 Species CO2 Species O3 Species CO2 O3 Species Q. mongolica CO2 O3 CO2 O3 Q. serrata CO2 O3 CO2 O3
RMR
MSMR
LSMR
LMR
LAR
S:R ratio
0.317 0.006** 0.299 CO2: 0.16ab > ambient: 0.15b > CO2 þ O3: 0.15b
Generally, elevated CO2 would increase the total biomass of trees via enhanced photosynthesis (Tissue et al., 1997; Ainsworth and Long, 2005; Ainsworth and Rogers, 2007; Norby and Zak, 2011), whereas elevated O3 may decrease tree growth because of reduced photosynthesis (Matyssek and Sandermann, 2003; Matyssek et al., 2010; Pretsch et al., 2010; Kitao et al., 2009, 2012). Earlier studies showed that growth enhancement by elevated CO2 was consistently negated by elevated O3 in Populus tremuloides in the FACE experiment (Isebrands et al., 2001; Karnosky et al., 2003; Talhelm et al., 2014), as well as in the fieldgrown seedlings of Q. petraea, Fraxinus excelsior, and Pinus sylvetris in an open top chamber (OTC) experiment (Broadmeadow and Jackson, 2000). Conversely, no significant effects of elevated CO2 and/or O3 on the total dry mass were observed in potted seedlings of three Japanese birch species (Betula platyphylla var. japonica, Betula ermanii, and Betula maximowicziana) (Hoshika et al., 2012), while elevated CO2 increased the total dry mass of
M. Kitao et al. / Environmental Pollution 206 (2015) 133e141
the field-grown silver birch (Betula pendula) without any effect of elevated O3 in the OTC experiments (Riikonen et al., 2004). In contrast to the previous studies, the growth of Q. mongolica was significantly stimulated by the combination of elevated CO2 and O3, and the growth of Q. serrata was significantly increased even by elevated O3 as well as by elevated CO2 (Fig. 2). Consistent with this finding, Watanabe et al. (2010) reported growth stimulation under the combination of elevated CO2 and O3 in the potted seedlings of Japanese beech (Fagus crenata), which is a typical late-successional species with a flush-type leaf emergence (Kikuzawa et al., 1983). An O3-induced preferable carbon allocation into shoots was n et al., 1997; observed in the two Japanese oak species (Sellde Landolt et al., 2000; Oksanen and Rousi, 2001), which could have compensating effects for plant growth in response to the O3induced reduction in photosynthesis (Mooney et al., 1988; Pell et al., 1994; Yamaji et al., 2003). The fraction of biomass partitioning into leaves (i.e., LMR) generally decreases with increasing plant size through an ontogenetic shift (Walters et al., 1993; King, 2003; Poorter et al., 2011). In our study, however, no significant decreases in LMR and LAR were observed in either oak species, despite the significantly greater total biomass under elevated O3 (Fig. 2, Tables 4 and 5). These findings seem to suggest a substantially higher biomass allocation into leaves induced by elevated O3. Apparently, the seedlings of Q. mongolica grown under elevated O3 showed a preferable allocation into leaves, as indicated by the higher LMR and LAR in the case of no total biomass enhancement (Table 4). An O3-induced increase in carbon allocation into shoots, particularly into leaves, may be dependent on species-specific shoot development patterns. The two Japanese oak species used in the present study are known to have a high ability for plastic growth because both show a flush and succeeding-type shoot development in response to a forest gap formation (Kikuzawa, 1983; Kitao et al., 2000, 2006) and naturally large root systems with considerable sprouting capacity (Sakai et al., 1997; Sakai and Sakai, 1998). Similarly, Calatayud et al. (2011) reported that elevated O3 could increase the S:R ratio in the European oak species (Quercus ilex, Quercus faginea, Quercus pyrenaica, and Quercus robur), with no decrease in total biomass, despite a reduction in the photosynthetic rate. However, Broadmeadow and Jackson (2000) showed that elevated O3 had no effect on the S:R ratio of Q. petraea and instead decreased its growth. A typical late-successional species, F. crenata, which has a flush-type leaf emergence (generally flushes once in spring), showed higher LMR in the secondflushed leaves of potted seedlings grown under the combination of elevated CO2 and O3, accompanied with growth stimulation as well (Watanabe et al., 2010). Conversely, field-grown aspen (P. tremuloides) (Karnosky et al., 2005), field-grown silver birch (B. pendula) (Yamaji et al., 2003; Riikonen et al., 2004), and pot-grown Japanese birches (Hoshika et al., 2012), categorized as fast-growing pioneer species, showed less response in carbon allocation into shoots when exposed to elevated O3. Thus, we speculate that carbon allocation in mid- and late-successional tree species with inherently conservative shoot growth patterns may be influenced by elevated O3 more markedly than in pioneer tree species, which have an intrinsically preferable carbon allocation into shoot with succeeding-type leaf emergence (Kikuzawa, 1983). A significant decrease in net photosynthetic rate (An) was observed in the older leaves of both oak species grown under elevated O3 (Fig. 3); this suggests an earlier leaf senescence induced by O3 as that observed at the late growth season in B. pendula (Yamaji et al., 2003) and certain European oak species (Calatayud et al., 2011). Although both Japanese oak species are known to be O3 tolerant (Yamaguchi et al., 2011), weighted mean An in Q. mongolica was more sensitive to O3 exposure than that in Q. serrata
139
(Fig. 4). This may be attributed to the greater O3 uptake via higher stomatal conductance of Q. mongolica (Fig. 5) (Kinose et al., 2014; Matyssek et al., 2015). Even though Q. serrata showed lower weighted mean An than Q. mongolica (Fig. 4), the higher ratio of leaf to total biomass in Q. serrata (Tables 4 and 5) could compensate for the lower capacity of photosynthesis (Poorter, 1989). Tree species, such as Q. serrata, having a lower photosynthetic capacity with lower stomatal conductance but higher leaf mass or area ratio could circumvent the negative effects of O3 through less O3 uptake (Matyssek et al., 2015). In addition, a decrease in stomatal conductance under elevated CO2, as marginally observed in Q. serrata (Fig. 5), would contribute to suppressing O3 uptake (cf. Uddling et al., 2010). Significant growth enhancement observed in plants grown under the combination of elevated CO2 and O3 may result from the preferable biomass allocation into leaves by elevated O3 and photosynthetic rates enhanced by elevated CO2. Total biomass of Q. mongolica seedlings grown under elevated O3 was not different from that grown under ambient conditions, possibly because of a decreased photosynthetic rate offset by an increased partitioning into leaves (Poorter, 1989; Okusanen and Rousi, 2001; Yamaji et al., 2003; Calatayud et al., 2011). Based on the leaf and whole plantlevel responses in the present study, it would appear that the increased partitioning into leaves was not perfectly regulated to compensate for the decrease in photosynthetic carbon gain by elevated O3, but was instead directly regulated by O3. Winwood et al. (2007) reported that elevated O3 enhanced cytokinin transfer from roots to shoots through xylem in adult beech trees (Fagus sylvatica) to compensate for the destruction of cytokinins in leaves by elevated O3. Moreover, trans-zeatin-type cytokinins, key hormones synthesized in roots, enhance shoot growth when transferred through xylem flow (Sakakibara, 2006; Kiba et al., 2013). Such an effect of O3 on plant hormones may directly increase carbon allocation into leaves, thereby enhancing total plant growth independent of an O3-induced decline in photosynthesis. In conclusion, two Japanese oak species, Q. mongolica and Q. serrata, showed significant growth enhancement under the combination of elevated CO2 and O3, possibly because of preferable biomass partitioning into leaves and a predominant enhancement of photosynthesis. Such an overcompensatory growth response in the seedlings of mid-successional oak species under oncoming atmospheric conditions would improve the competitive ability of the trees at an early stage of forest regeneration and favorably shift species composition. Acknowledgments We thank Dr. Morikawa for his valuable suggestions concerning the present study. This work was supported in part by the project on “Technology development for circulatory food production systems responsive to climate change” conducted by the Ministry of Agriculture, Forestry and Fisheries, Japan, the Grant-in-Aid for Scientific Research (B) (No. 25292092) and the Grant-in-Aid for Scientific Research on Innovative Areas (No. 22114514). Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.envpol.2015.06.034. References Ainsworth, E.A., Long, S.P., 2005. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New. Phytol.
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