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Physiological and Morphological Traits and Competence for Carbon Sequestration of Several Green Roof Plants under a Controlled Environmental System

The physiological and morphological traits of green roof plants are key to understanding the environmental benefits of green roofs. However, the comparative investigation of physiological and morphological traits of green roof plants is limited. Moreover, there have been few studies on the relevance of physiological and morphological traits and competence for carbon sequestration of green roof plants. In particular, Sedum L. species are generally regarded as crassulacean acid metabolism (CAM) plants, but several Sedum species are recognized as having an ‘‘inducible type of CAM.’’ These plants are C3 and C4 plants, with the ability to switch their carbon metabolism to the CAM pathway. In the case of Sedum, the inducer of CAM is drought stress. This observation suggests that differences in water regimes result in physiological and morphological changes that may have a considerable effect on the environmental benefits of Sedum green roofs. The purpose of this study is to compare the physiological and morphological traits of four green roof plants and discuss the influence of these traits on their environmental benefits under a controlled environmental system. In addition, we attempted to clarify the relevance of physiological and morphological traits and competence for carbon sequestration in each plant using growth analysis. We used Sedum mexicanum Briton, Sedum aizoon L., Zoysia matrella (L.) Merr., and Ophiopogon japonicus (Thunb.) Ker Gawl. in this study, and only the two Sedum species were assigned treatments with different frequency of irrigation to investigate physiological and morphological responses and variation in carbon sequestration. The two Sedum species exhibited the C3 photosynthetic pathway in wet and dry treatments, implying the inducible type of CAM. Morphological responses of the two Sedum species were significantly affected by the different frequencies of irrigation; plants responded to increases in below-ground resources (water and nutrients) with increased biomass allocation of leaves and stems. Owing to these physiological and morphological responses in the wet treatment, transpiration rates and competence for carbon sequestration [relative C sequestration rate per whole-plant C content (RGRc)] of the two Sedum species were higher than those of Z. matrella andO. japonicus. This result suggested that the cooling effect and carbon sequestration of Sedum in wet and increased nutrient conditions are equivalent to those observed in other plants. In addition, the net assimilation rate (NARc) and leaf area ratio per whole-plant C content (LARc) were significantly correlated with photosynthetic rates and biomass allocation. Thus, it became clear that growth analysis can reveal the relevance of physiological (NARc) and morphological (LARc) traits and RGRc. Our results will serve as a baseline of the physiological and morphological traits and carbon sequestration of green roof plants and contribute to more suitable design and maintenance of vegetation in green roofs. The green roof is known to be a beneficial technology in urban environments. Some of the benefits include cooling and insulation of buildings (Sailor, 2008; Wong et al., 2003), mitigation of the urban heat-island effect (Susca et al., 2011), stormwater management (Getter et al., 2007; Villarreal and Bengtsson, 2005), carbon sequestration and air pollution reduction (Getter et al., 2009; Yang et al., 2008), and habitat provision for other organisms (Kadas, 2006). Owing to these environmental benefits, the green roof has been adopted in many countries. These benefits depend on the presence of living plants and the growing medium. For example, the boundary layer of air over the roof is cooled by evapotranspiration, shading from plants, and the trapping of cool air by the vegetation layer (Dimoudi and Nikolopoulou, 2003; Solecki et al., 2006). In addition, air pollution is reduced through plant photosynthesis and trapping of the gases by vegetation and soil layers (Garland, 1977). Consequently, the physiological and morphological traits of the plants are key to understanding the environmental benefits of green roofs. However, the comparative investigation of physiological and morphological traits of green roof plants is limited (Lundholm et al., 2015). Moreover, there have been few studies examining the relevance of physiological and morphological traits and competence for carbon sequestration in green roof plants. Warm-season turfgrasses and Sedum species are the most common vegetation in Japan. Green roofs composed of warmseason turfgrasses or other perennials are generally installed Received for publication 16 Aug. 2016. Accepted for publication 9 Sept. 2016. Corresponding author. E-mail: hwatanabe@faculty.chiba-u.jp. J. AMER. SOC. HORT. SCI. 141(6):583–590. 2016. 583 with irrigation systems to prevent drought stress. In contrast, Sedum green roofs are not always installed with irrigation because these plants can adapt to periodic drought. They are regarded as CAM plants whose stomata remain closed during the day, with gas exchange occurring at night (VanWoert et al., 2005). This physiological pathway plays a crucial role in the plant’s response to drought stress; other CAM plants have also been investigated for utilization in green roofs (Lin and Lin, 2011). In addition, several Sedum species are recognized as having an ‘‘inducible type of CAM’’ (Gravatt andMartin, 1992; Lee and Griffiths, 1987). They are C3 and C4 plants with the ability to switch their carbon metabolism to the CAM pathway. In the case of Sedum, the inducer of CAM is drought stress (Sayed, 2001). This observation suggests that differences in water regimes result in physiological and morphological changes that may have a considerable effect on the environmental benefits of Sedum green roofs (e.g., carbon sequestration, air pollution reduction, and cooling effects). Further, although a Sedum green roof is likely to be exposed to drought conditions, the substrate may be wet during the rainy season in southeast Asian countries (Chen, 2013). Van Mechelen et al. (2015) also suggested that irrigation is necessary on green roofs in (semi)-arid climates for the survival and success of extensive green roof plantings. Therefore, it is necessary to investigate the physiological and morphological responses of Sedum to various water conditions resulting from different maintenance practices and climates. The purpose of this study is to compare the physiological and morphological traits of several green roof plants and discuss the influence of these traits on their environmental benefits. In addition, we attempted to clarify the relevance of physiological and morphological traits and competence for carbon sequestration in each plant using growth analysis. In particular, Sedum species were assigned different water regimes to investigate the physiological and morphological responses and variation in carbon sequestration. Materials and Methods

The green roof is known to be a beneficial technology in urban environments. Some of the benefits include cooling and insulation of buildings (Sailor, 2008;Wong et al., 2003), mitigation of the urban heat-island effect (Susca et al., 2011), stormwater management (Getter et al., 2007;Villarreal and Bengtsson, 2005), carbon sequestration and air pollution reduction (Getter et al., 2009;Yang et al., 2008), and habitat provision for other organisms (Kadas, 2006). Owing to these environmental benefits, the green roof has been adopted in many countries. These benefits depend on the presence of living plants and the growing medium. For example, the boundary layer of air over the roof is cooled by evapotranspiration, shading from plants, and the trapping of cool air by the vegetation layer (Dimoudi and Nikolopoulou, 2003;Solecki et al., 2006). In addition, air pollution is reduced through plant photosynthesis and trapping of the gases by vegetation and soil layers (Garland, 1977). Consequently, the physiological and morphological traits of the plants are key to understanding the environmental benefits of green roofs. However, the comparative investigation of physiological and morphological traits of green roof plants is limited (Lundholm et al., 2015). Moreover, there have been few studies examining the relevance of physiological and morphological traits and competence for carbon sequestration in green roof plants.
Warm-season turfgrasses and Sedum species are the most common vegetation in Japan. Green roofs composed of warmseason turfgrasses or other perennials are generally installed with irrigation systems to prevent drought stress. In contrast, Sedum green roofs are not always installed with irrigation because these plants can adapt to periodic drought. They are regarded as CAM plants whose stomata remain closed during the day, with gas exchange occurring at night (VanWoert et al., 2005). This physiological pathway plays a crucial role in the plant's response to drought stress; other CAM plants have also been investigated for utilization in green roofs (Lin and Lin, 2011). In addition, several Sedum species are recognized as having an ''inducible type of CAM'' (Gravatt and Martin, 1992;Lee and Griffiths, 1987). They are C 3 and C 4 plants with the ability to switch their carbon metabolism to the CAM pathway. In the case of Sedum, the inducer of CAM is drought stress (Sayed, 2001). This observation suggests that differences in water regimes result in physiological and morphological changes that may have a considerable effect on the environmental benefits of Sedum green roofs (e.g., carbon sequestration, air pollution reduction, and cooling effects). Further, although a Sedum green roof is likely to be exposed to drought conditions, the substrate may be wet during the rainy season in southeast Asian countries (Chen, 2013). Van Mechelen et al. (2015) also suggested that irrigation is necessary on green roofs in (semi)-arid climates for the survival and success of extensive green roof plantings. Therefore, it is necessary to investigate the physiological and morphological responses of Sedum to various water conditions resulting from different maintenance practices and climates.
The purpose of this study is to compare the physiological and morphological traits of several green roof plants and discuss the influence of these traits on their environmental benefits. In addition, we attempted to clarify the relevance of physiological and morphological traits and competence for carbon sequestration in each plant using growth analysis. In particular, Sedum species were assigned different water regimes to investigate the physiological and morphological responses and variation in carbon sequestration.

Plant material
We focused on groundcover herbaceous green roof plants for comparison of physiological and morphological traits; thus, S. mexicanum, S. aizoon, Z. matrella, and O. japonicus 'Tama-Ryu' were selected for this study. Although these species are widely distributed in Japan, the photosynthetic pathway of the two Sedum species is not well understood. Zoysia matrella, a warm-season turfgrass and C 4 plant, is one of the most common green roof plants in Japan. Ophiopogon japonicus is an evergreen perennial.
Comparative study of physiological traits EXPERIMENTAL DESIGN. To investigate the photosynthetic pathway of the two Sedum species in wet and dry conditions, individuals of the two Sedum species were assigned randomly to wet or dry treatments and acclimatized to each treatment for 3 weeks. Plants in the wet treatment were watered every day, and plants receiving the dry treatment were watered once per week. Zoysia matrella and O. japonicus only received the wet treatment, in accordance with general cultivation practice. In this study, to reduce the influence of nutrient-poor conditions on plant growth, an irrigation system supplied not water but nutrient solution (72 mLÁL -1 NO 3 -N, 11 mLÁL -1 NH 4 -N, 100 mLÁL -1 P 2 O 5 , 167 mLÁL -1 K 2 O, 71 mLÁL -1 CaO, and 17 mLÁL -1 MgO) for 30 min by bottom watering in every treatment. All studies were carried out in the phytotron.
COMPARISON OF PHOTOSYNTHETIC AND TRANSPIRATION RATES IN WET TREATMENT. For individuals of the four species in the wet treatment, photosynthetic and transpiration rates were measured at 15, 25, and 35°C, which are assumed roof conditions. Other measurement conditions were the same as above. Photosynthetic water use efficiency [WUE ph (photosynthetic rate/transpiration rate)] was calculated for each plant.
Comparative study of morphological traits and competence for carbon sequestration EXPERIMENTAL DESIGN. To examine morphological traits and carbon sequestration, we investigated biomass allocation and whole-plant carbon sequestration in the phytotron.
In all four species, 15 total pots per species were selected at random (three pots were chosen at 0, 1, and 2 d, and six pots were selected at 3 d after the start of the experiment). After these samples were selected, the Sedum species were divided into wet, dry, and nonirrigation treatments. Plants in all treatments were irrigated at the start of the experiment (0 d). After this irrigation, the nonirrigation treatment was never irrigated. Wet and dry treatments and the irrigation system (supplied nutrient solution) were the same as above, but there was no irrigation in the wet treatment for 1-3 d. Zoysia matrella and O. japonicus plants only received the wet treatment.
Three pots were randomly harvested once per week for 4-6 weeks after the start of the experiment (28, 35, and 42 d), and the remaining six pots were harvested at the end of the experiment (49 d). We regarded these 15 total pots (at 28, 35, 42, and 49 d) as the result of treatment. For all samples, roots were removed from the soil and washed with distilled water.
MORPHOLOGICAL RESPONSES TO WATER REGIMES OF TWO SEDUM SPECIES AND COMPARISON TO Z. MATRELLA AND O. JAPONICUS. Plants were divided into leaves, stems, roots, and flowers and dried at 70°C for 72 h. Before the leaves were dried, they were scanned (LP-A500; Epson, Suwa, Japan) and image analysis software ImageJ (Schneider et al., 2012) was used to measure the leaf area and greenness of leaves. We calculated the leaf area index [LAI (leaf area per 44 cm 2 )], and described greenness of leaves with G/R, which is related to chlorophyll content (Adamsen et al., 1999). Biomass allocation was analyzed using five indices: Growth analysis is a simple model that associates a plant's relative growth rate (RGR) with physiological [net assimilation rate (NAR)] and morphological [leaf area ratio (LAR)] traits (Lambers et al., 1989), which have a mathematical relationship (RGR = NAR · LAR). In addition, growth analysis provides a more informative comparison of a plant's relative performance because it can reduce the influence of differences in the initial size and mass among the experimental plants (Hunt, 1982). This model is generally applied to dry weights, but this experiment focused on whole-plant carbon content because our goal was to examine the relevance of physiological and morphological traits and carbon sequestration in each plant. Thus, we carried out growth analysis using a functional approach (Hunt, 1982) and calculated relative C sequestration rate per whole-plant C content (RGR c ), NAR c , and LAR per whole-plant C content (LAR c ). We used RGR c as the measure of the ability to sequester carbon. Moreover, for the two Sedum species, growth response coefficients (GRC) of NAR c and LAR c (comparisons: wet and dry, wet and nonirrigation, and dry and nonirrigation) were calculated. The GRC values of NAR and LAR sum to 1.0, indicating the relative contribution of those parameters to a change in RGR (Poorter and Nagel, 2000;Poorter and Van der Werf, 1998). For example, if GRC LAR is 1, a change in RGR is attributed only to a change in LAR. In other words, GRC NARc and GRC LARc indicate the influence of physiological and morphological changes on competence for carbon sequestration.

Statistical analysis
Data were analyzed using IBM SPSS Statistics (version 22.0; IBM Japan, Tokyo, Japan). Analysis of variance was used to assess the effects of treatments and the plant species. Differences in mean values were assessed with Student's t test or multiple comparisons [Tukey-b (homoscedasticity assumed) or Dinnett-T3 (homoscedasticity not assumed)].

Results and Discussion
Comparative study of physiological traits PHOTOSYNTHETIC PATHWAY OF S. MEXICANUM AND S. AIZOON. Individuals of S. mexicanum and S. aizoon in the wet treatment exhibited CO 2 uptake only during the light period and no dark period CO 2 uptake in any of the samples (Fig. 1). In the dry treatment, S. mexicanum and S. aizoon did not exhibit CO 2 uptake during light and dark periods at 6 d after irrigation, similar to the photosynthetic pathway of several Sedum species which had an inducible type of CAM under drought conditions (Gravatt and Martin, 1992;Lee and Griffiths, 1987). The mean photosynthetic rate during the light period under the wet treatment was significantly higher than that under the dry treatment (Student's t test at P < 0.05). Thus, these results imply that S. mexicanum and S. aizoon have an inducible type of CAM.
Soil water content in the dry treatment was below 10% at 2 to 6 d after irrigation; however, S. mexicanum displayed the C 3 photosynthetic pathway ( Fig. 2A). Moreover, although the frequency of water and nutrient supply under the dry treatment was lower than that under the wet treatment, photosynthetic and transpiration rates at 0 to 4 d after irrigation were not significantly different from those in the wet treatment ( Fig.  2A; Table 1). Sedum aizoon also exhibited the C 3 photosynthetic pathway in the dry treatment ( Fig. 2B), but the photosynthetic and transpiration rates were significantly lower than those in the wet treatment ( Fig.  2B; Table 1). In green roofs, some studies suggested that Sedum species have exhibited the C 3 photosynthetic pathway (Butler and Orians, 2011;Durhman et al., 2006). Our results are consistent with this photosynthetic response occurring in green roofs. The photosynthetic rate of S. mexicanum at all temperatures was significantly lower than that of Z. matrella and not significantly different from that of O. japonicus (Fig. 3).
Photosynthetic rates of S. aizoon were significantly higher than those of O. japonicus and similar to those of Z. matrella except at 35°C (Fig. 3). Sedum species in the wet treatment exhibited similar photosynthetic rates to those of other green roof plants, including the C 4 plant, Z. matrella. However, the photosynthetic rate of C 4 plants is generally higher at high temperatures, so Z. matrella should show the highest photosynthetic rate at 35°C. Transpiration rates of the two Sedum species at each temperature were higher than that of Z. matrella, and there were significant differences from transpiration rates of O. japonicus at 15 and 25°C (Table 2). WUE ph of the two Sedum species was lower than that of Z. matrella and O. japonicus (Table 2). Although CAM plants typically have high WUE and low transpiration rates (Nobel, 1991), the two Sedum species in the wet treatment had distinctively lower WUE and higher transpiration rates than did other green roof plants. This result supports the C 3 pathway being used for photosynthesis.
Previous research has suggested that evapotranspiration is the most important contributor toward the cooling effect in green roofs (Feng et al., 2010;Oberndorfer et al., 2007;Takakura et al., 2000). In addition, some studies reported that irrigation has enhanced the cooling effect (Blanusa et al., 2013; Lin and Lin, 2011;Solecki et al., 2006). Therefore, our results indicate that the cooling effect of Sedum in wet and increased nutrient conditions may be equivalent to that of other plants from the standpoint of evapotranspiration. Moreover, even Sedum roofs with a low frequency of irrigation or rain events may improve the thermal load because Sedum in the dry treatment exhibited the C 3 pathway.
Comparative study of morphological traits and competence for carbon sequestration PLANT STATUS. There was no significant difference in initial dry weight (±SE) between S. mexicanum (0.52 ± 0.03 g), S. aizoon (0.55 ± 0.03 g), and Z. matrella (0.50 ± 0.04 g). At the end of the experiment, the two Sedum species had significant differences in dry weight and LAI among the treatments ( Table  3). The dry weight of Z. matrella was less than that of Sedum in the wet treatment. Ophiopogon japonicus had a lower dry weight than Sedum in the dry treatments, although its initial dry weight (0.66 ± 0.02 g) was significantly higher than that of the other species (Tukey-b test at P < 0.05). Under our experimental conditions, the LAI of S. mexicanum in the wet treatment was much larger than that in the dry treatment and that of the other species (Table 3).
G/R of S. mexicanum declined significantly with decreased frequency of irrigation (Table 3). In contrast, S. aizoon showed no difference in G/R between dry and nonirrigation treatments. However, all species and treatments had a G/R greater than 1.0, which indicates all plants have not withered and are still green. Moreover, although Z. matrella and O. japonicus in the wet treatments were watered every day and not analyzed soil water content, this result suggests that plants in the wet treatment did not experience drought or waterlogging stress, which greatly affect plant growth.  Table 4. All morphological traits of S. mexicanum were significantly affected by the difference in frequency of irrigation. LMF, SMF, and SLA in the wet treatment were significantly higher than those in the nonirrigation treatment, and RMF in the wet treatment was significantly lower than that in dry and nonirrigation treatments. The morphological response of S. aizoon was similar to that of S. mexicanum, but there was no significant difference in treatments on SLA. The only species that flowered during the experiment was S. aizoon (wet treatment: flowering rate = 15/15, FMF = 0.14 ± 0.02; dry treatment: flowering rate = 5/15, FMF = 0.013 ± 0.006). It is well documented that plants respond to a decrease in belowground resources (e.g., water, nutrients) with increased biomass allocation to roots (Poorter and Nagel, 2000) which is consistent with the results of LMF, SMF, and RMF in this study.
LMF of the two Sedum species in wet and dry treatments was significantly higher than that of Z. matrella and O. japonicas (Table 4). The SMF and RMF results clearly demonstrate that Z. matrella allocated significantly more biomass to stems, and O. japonicas allocated significantly more biomass to roots. SLA of the Z. matrella and O. japonicus exhibited similar values to that of S. mexicanum in the nonirrigation treatment, and SLA of S. mexicanum in wet and dry treatments were significantly higher than that of the other species.
In green roofs, LAI and SLA were evaluated as predictors of environmental benefits (Lundholm et al., 2015;Takakura et al., 2000). There may be differences in growth condition and stage between this experiment and actual green roofs. However, results of the current study clearly indicate that these morphological indices of the two Sedum species significantly change with changes in below-ground resources (water and nutrients), which suggest that appropriate water and nutrient management improves the environmental benefits of Sedum green roofs. In Carbon concentration of the two Sedum species did not differ significantly between treatments, but there were significant differences between species (Table 5). Initial carbon content did not differ significantly between S. mexicanum (0.20 ± 0.01 g), S. aizoon (0.21 ± 0.01 g), and Z. matrella (0.21 ± 0.02 g), but O. japonicus (0.27 ± 0.01 g) had greater carbon content (Dunnett-T3 at P < 0.05). Carbon sequestration of the Sedum species was significantly influenced by the frequency of irrigation (Table 5). At the end of the experiment, carbon content of Z. matrella was similar to that of Sedum in the wet treatments, whereas O. japonicus was similar to that of Sedum in the dry treatments. The time course of whole-plant carbon content is shown in Fig. 4. Average carbon content increased across the study period.
Results of the growth analysis are shown in Table 6. RGR c of the two Sedum species was clearly affected by the difference in frequency of irrigation and was similar in each treatment. NAR c and LAR c of the two Sedum species were also influenced by the difference in frequency of irrigation, except for the LAR c of S. aizoon.
In the wet treatment, S. mexicanum and S. aizoon had the highest RGR c of the four species. Sedum mexicanum had the lowest NAR c of the four species, but its LAR c was more than double that of the others. Sedum aizoon had the second highest NAR c and LAR c in the wet treatment. In comparison, although Z. materella exhibited the highest NAR c , its RGR c was lower than that of the two Sedum species because its LAR c was lower than that of Sedum in all treatments. Ophiopogon japonicus also had high NAR c and the lowest LAR c in this experiment, which resulted in RGR c being lower than that of Sedum in the dry treatment. The four plant species in the wet treatment had a significant correlation (r = 0.972, P < 0.05) between NAR c and photosynthetic rate (25°C, 1000 mmolÁm -2 Ás -1 ). In addition, LAR is commonly known as an index derived from LMF and SLA in growth analyses. There was significant correlation (r = 0.959, P < 0.01) between LAR c and the product of LMF and SLA in all species and treatments. GRC NARc and GRC LARc of S. mexicanum were about 0.7 and 0.3, respectively, in all comparisons (Table 7). This result indicates that 70% of a change in RGR c (competence for carbon sequestration) was due to changes in NAR c and 30% was due to changes in LAR c . In contrast, GRC NARc of S. aizoon was about 0.95, so competence for carbon sequestration was strongly affected by a change in NAR c . Sedum aizoon did not differ in SLA among treatments, which may be related to this result (Table 4). Thus, variation in carbon sequestration for different below-ground resources seemed to be mainly caused by physiological responses.
The NAR c and LAR c results were consistent with the results for photosynthetic rates and biomass allocation. This finding suggested that growth analysis reveals the relevance of physiological (NAR c ) and morphological (LAR c ) traits and competence for carbon sequestration (RGR c ). Thus, it became clear that the appropriate water and nutrient regime could elevate the competence for carbon sequestration in a Sedum green roof as a result of physiological and morphological responses.
Moreover, there is an suggestion that Sedum has higher competence for carbon sequestration than a C 4 plant (Z. matrella) in appropriate below-ground resource (water and nutrient) conditions for Sedum species, and even a Sedum green roof with a low frequency of irrigation or rain events may show higher carbon sequestration than another green roof plant (O. japonicus). From the standpoint of application to actual green roofs, this study did not cover all green roof conditions (e.g., wind speed, high and low temperatures, light intensities, and nutrient conditions) which may have led to different growth of plants as compared with those in actual extensive green roofs. Thus, for other environmental conditions and plant growth stages, the relevance of physiological and morphological traits and environmental benefits should be studied further. Our results will serve as a baseline of the physiological and morphological traits and carbon sequestration of green roof plants, and contribute to more suitable design and maintenance of vegetation in green roofs.

Conclusions
This study compared physiological and morphological traits of four green roof plants and discussed the influence of these traits on their environmental benefits in controlled conditions. In wet and increased nutrient conditions, S. mexicanum and S. aizoon exhibited the C 3 photosynthetic pathway, and their LMF significantly increased in comparison with the dry and nonirrigation treatments. Consequently, transpiration rates and competence for carbon sequestration (RGR c ) of the two Sedum species were higher than those of Z. matrella and O. japonicus in our experiment.
Although this study do not cover all green roof conditions and plant growth stages, our results serve as a baseline of the physiological and morphological traits and carbon sequestration of green roof plants. In addition, growth analysis performed on plant carbon content enabled the relevance of physiological (NAR c ) and morphological (LAR c ) traits and competence for carbon sequestration (RGR c ) in green roof plants to be understood more clearly. This analysis method could apply to other experiments and green plants. Our results