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Article

Elevated CO2 and O3 Levels Influence the Uptake and Leaf Concentration of Mineral N, P, K in Phyllostachys edulis (Carrière) J.Houz. and Oligostachyum lubricum (wen) King f.

by
Minghao Zhuang
1,2,
Yingchun Li
1,
Ziwu Guo
1,*,
Yueqiao Li
3,
Wenting Pan
3 and
Shuanglin Chen
1
1
Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Fuyang 311400, China
2
School of Environment and State Key Joint Laboratory of Environment Simulation and Pollution Control, Tsinghua University, Beijing 10084, China
3
Experimental Center of Subtropical Forestry, Chinese Academy of Forestry, Fenyi 336600, China
*
Author to whom correspondence should be addressed.
Forests 2018, 9(4), 195; https://doi.org/10.3390/f9040195
Submission received: 5 March 2018 / Revised: 26 March 2018 / Accepted: 27 March 2018 / Published: 10 April 2018
(This article belongs to the Section Forest Ecology and Management)
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Abstract

:
Rising CO2 and O3 concentrations significantly affect plant growth and can alter nutrient cycles. However, the effects of elevated CO2 and O3 concentrations on the nutrient dynamics of bamboo species are not well understood. In this study, using open top chambers (OTCs), we examined the effects of elevated CO2 and O3 concentrations on leaf biomass and nutrient (N, P, and K) dynamics in two bamboo species, Phyllostachys edulis (Carrière) J.Houz. and Oligostachyum lubricum (wen) King f. Elevated O3 significantly decreased leaf biomass and nutrient uptake of both bamboo species, with the exception of no observed change in K uptake by O. lubricum. Elevated CO2 increased leaf biomass, N and K uptake of both bamboo species. Elevated CO2 and O3 simultaneously had no significant influence on leaf biomass of either species but decreased P and N uptake in P. edulis and O. lubricum, respectively, and increased K uptake in O. lubricum. The results indicate that elevated CO2 alleviated the damage caused by elevated O3 in the two bamboo species by altering the uptake of certain nutrients, which further highlights the potential interactive effects between the two gases on nutrient uptake. In addition, we found differential responses of nutrient dynamics in the two bamboo species to the two elevated gases, alone or in combination. These findings will facilitate the development of effective nutrient management strategies for sustainable management of P. edulis and O. lubricum under global change scenarios.

1. Introduction

Nitrogen (N), phosphorus (P), and potassium (K) are considered essential elements for plant growth [1], but are also the most limiting elements for terrestrial vegetation, especially under environmental change [2,3]. Two important drivers of environmental change, concentrations of atmospheric CO2 and tropospheric O3, have been increasing substantially as a result of human activities since the industrial revolution and will continue to increase in the future [4]. These changes have affected growth and N, P, and K concentrations and uptake in plants, which may influence nutrient cycles in ecosystems [5,6,7].
Most previous studies that have considered the effects of elevated CO2 and O3 on N, P, and K concentrations and uptake in plants, have mainly focused on the response of plant N and P to elevated CO2, while other nutrients, especially K, have rarely been investigated [7,8,9] Studies have shown that elevated CO2 generally reduces plant N concentration and increases plant N uptake [10,11,12]. This is partly explained by the dilution hypothesis [13,14], reduction in soil N availability [15,16], nitrate assimilation restriction [17,18,19], and a change in leaf physiological characteristics (e.g., a decrease in leaf protein and the photosynthetic enzyme RuBisCO) [14]. Compared to plant N, the effects of elevated CO2 on plant P concentration and uptake are more variable (Gifford et al., 2000). Elevated CO2 has been associated with increased [20,21], neutral [22,23] and decreased plant P concentration and uptake [24,25]. Similar results have been found in the response of plant K to elevated CO2, although relevant studies are rare [7]. Consequently, the response mechanisms of N, P, and K uptake in plants to elevated CO2 remain unclear [7,21] and warrant further study, especially regarding the complexity of the response of P and K to elevated CO2.
In comparison, a few studies have investigated nutrient concentration and uptake in plants under elevated O3 [26,27,28,29]. These studies have shown that the responses of plant N, P, and K concentrations and uptake to elevated O3 are more complicated than responses to elevated CO2 [28,30]. For example, several studies have demonstrated that elevated O3 decreases N, P, and K concentrations and uptake to some extent due to a reduction in nutrient demand by the plants, caused by O3-induced inhibition of plant growth [5,31]. However, other studies have shown either an increase [29] or no change in nutrient concentration and uptake [32,33,34], which have been partly attributed to a defense mechanism against elevated O3 and an adaptive strategy for plants. Due to the complexity of nutrient response to elevated O3, and the lack of information available, it remains unclear how N, P, and K concentrations and uptake respond to elevated O3.
In view of the contrasting effects of elevated CO2 and O3 on plant growth [35], some studies have concluded that elevated CO2 and O3 might drive plant nutrient dynamics in opposite directions [36,37,38]. However, to our knowledge, there is little evidence to support this hypothesis due to the complexity of nutrient responses to elevated CO2 and O3 described above. Moreover, limited information is available on the combined effect of elevated CO2 and O3 on plant nutrient dynamics, which may potentially limit our ability to further understand nutrient cycles [30,39]. It is important to understand how increases in CO2 and O3 concentrations will affect the concentrations and uptake of N, P, and K in plants, in order to understand nutrient cycle dynamics and predict potential nutrient limitation under future regional climate change [40,41].
Bamboo is the main important non-timber sub-tropical and tropical forest product in China, and is widely distributed in Zhejiang, Fujian, Jiangxi, Hunan, Guangxi, and Yunnan [42]. It also plays important roles in regional water and soil conservation efforts, carbon sequestration, oxygen emission, and climate regulation, making it an important element of terrestrial ecosystems [42]. Among bamboo species, Phyllostachys edulis (Carrière) J.Houz. and Oligostachyum lubricum (wen) King f. are the two dominant bamboo species in the subtropical zone of China, and are characterized by fast growth rates (60 days), hollow stems and complicated rhizome-connecting stems (ramets). Previous studies have demonstrated that elevated CO2 enhances the growth of these two bamboo species [43,44], while elevated O3 inhibits their growth [45]. Moreover, the growth of both bamboo species under climate change is related to nutrient availability [46]. However, it remains unclear how elevated CO2 and O3 independently, and interactively, affect leaf N, P, and K uptake and leaf concentrations. Therefore, the objective of this study was to reveal the dynamics of N, P, and K uptake and leaf concentrations in P. edulis and O. lubricum under conditions of elevated CO2 and O3. We attempt to answer the two following questions: (1) Do elevated CO2 and O3 independently, and interactively, affect leaf N, P, and K uptake and leaf concentrations? (2) Do the responses of N, P and K dynamics to elevated CO2 and O3 differ between P. edulis and O. lubricum?

2. Materials and Methods

2.1. Research Site and Experimental Design

The experiment was carried out at the Taihuyuan Ornamental Bamboo Planting Garden in Zhejiang, China (29°56′–30°23′ N, 118°51′–119°72′ E). The region has a subtropical monsoon climate. Average annual precipitation is 1450 mm, and average annual temperature is 15.4 °C.
Open-top chambers (OTCs) that were used in the experiments were built using steel tubes and colorless clear glass, including a filtered air system, vent system and gas distribution system. The details of the OTCs are described in Zhuang [46]. O3 and CO2 concentrations were obtained from CFG-20 O3 generator (Sankang Environmental Technology Co., Ltd., Jinan, China) and steel cylinders of pure CO2 and from, respectively. The microclimatic (temperature, relative humidity) conditions were measured. We designed four treatments based on a 2 × 2 factorial design based on the local average and observed the peak O3 and CO2 concentrations in the field of the study site. (Table 1). Specific treatments were as follows: ambient air (O3 concentration of 40 ± 5 nmol mL−1, CO2 concentration of 360 ± 20 μmol mL−1); elevated O3 (O3 concentration of 100 ± 10 nmol mL−1, CO2 concentration of 360 ± 20 μmol mL−1); elevated CO2 (O3 concentration of 40 ± 5 nmol mL−1, CO2 concentration of 700 ± 35 μmol mL−1); and combined elevated CO2 and O3 (O3 concentration of 100 ± 10 nmol mL−1, CO2 concentration of 700 ± 35 μmol mL−1). Each treatment was replicated threefold.
Experiments were conducted from 10 July to 30 October 2011. During the experimental period, CO2 was released all day (24 h) and O3 was released from 07:00 a.m. to 17:00 p.m.

2.2. Plant Materials

Two-year-old bamboo plants of two species Phyllostachys edulis (diameter: 18.2 ± 1.8 mm; height: 2.75 ± 0.25) and Oligostachyum lubricum (diameter: 12.2 ± 1.3 mm; height: 2.70 ± 0.30 m) were planted in plastic pots in October 2010. The detailed information was described in our previous study [46].

2.3. Biomass and N, P, and K Measurements

At harvest, three plants of P. edulis and O. lubricum were randomly selected from each OTC and the only green leaves were collected for biomass and N, P, and K measurements. Leaves were oven dried at 75 °C to a constant weight. To evaluate N, P, and K concentrations, the samples were first digested in a solution of H2SO4–HClO4, and the N, P, and K concentrations were determined using Kjeldahl, molybdovanadate, and atomic absorption spectrometry methods respectively [47]. All nutrient measurements were replicated three times within the same treatment.

2.4. Statistical Analysis

The N, P, and K content of leaves was obtained by multiplying the leaf N, P, and K concentrations by leaf biomass. We used one-way analysis of variance (ANOVA) in SPSS ver. 17.0 statistical software (SPSS Inc., Chicago, IL, USA) to analyze the differences among treatments. p values < 0.05 indicated a significant difference among treatments.

3. Results and Discussion

3.1. Leaf N, P, and K Concentrations

Different responses of plant N, K, and P concentrations to elevated CO2 were observed in our study in both P. edulis and O. lubricum (Table 2). Elevated CO2, in comparison with ambient air, decreased leaf P concentration in both P. edulis and O. lubricum by 19.1% and 23.6%, respectively, which may be ascribed to a dilution effect resulting from an increase in biomass [14]. Compared with ambient CO2, elevated CO2 significantly decreased leaf N concentration (−14.5%) in O. lubricum, which is consistent with extensive previous studies [14,48], and can be largely explained by the carbohydrate dilution effect [12,48,49]. However, the observed increase in leaf N concentration (+18.5%) in P. edulis under elevated CO2 is in contrast with most studies on elevated CO2. This difference may be associated with higher N uptake with increasing leaf biomass growth resulting from an adequate supply of soil N in the present study, and an acceleration of nitrate assimilation [7,12,16]. Elevated CO2 significantly increased leaf K concentration (+31.1%) in O. lubricum, but decreased K concentration (−30.1%) in P. edulis (Table 2), suggesting a complex response of leaf K concentration to elevated CO2, as reported in numerous previous studies [11,50,51]. The possible explain was that elevated CO2 enhances the activity of stomata/guard cells, the operation of which is driven by the availability of K; therefore, the potential difference between leaf stomata and the lower plant parts results in active absorption of K [52]. However, the response mechanism of K concentration to elevated CO2 remains unclear and warrants further research [53,54].
Elevated O3 had a minor effect on N and P concentrations in both bamboo species (Table 2), which is consistent with several previous studies [32,33,34], but is inconsistent with others [5,55]. The inconsistency in these results could be related to a difference in ozone-resistance level among plants [56], as evergreen species (e.g., bamboos) are more tolerant to elevated O3 than deciduous species [57]. The possible mechanism affecting the response of N and P in plants warrants further study. Elevated O3, compared with ambient O3, significantly increased K concentration (+49.4%) in O. lubricum but did not change the K concentration in P. edulis. This result indicates a difference between the two bamboo species in the response of K to elevated O3. These results suggest that increasing K concentration can be regarded as an adaptive strategy of O. lubricum that could enhance the plant defensive capability against elevated O3 [5,21]. Moreover, these results may also explain the higher tolerance of O. lubricum to elevated O3 relative to P. edulis [45].
The combination of elevated CO2 and O3, in comparison with ambient air, significantly decreased the leaf P concentration (−20.5%) in P. edulis and the N concentration (−11.5%) in O. lubricum, but increased the leaf K concentration (+31.8%) in O. lubricum (Table 2). In addition, elevated O3 significantly increased leaf P concentration in P. edulis under ambient CO2 conditions, but reduced P concentration under elevated CO2, indicating a significant interactive effect of combined elevated CO2 and O3 on leaf P concentration. Similar results were found for leaf N and K concentrations in O. lubricum under combined elevated CO2 and O3. These results demonstrate that the nutrient concentrations of both bamboo species under elevated CO2 may offset the O3-induced change, although some differences exist between P. edulis and O. lubricum in nutrient-type response to combined elevated CO2 and O3 [36,37].

3.2. Leaf Biomass

Previous studies have reported that elevated O3 significantly decreased plant biomass by reducing photosynthesis [58,59], while elevated CO2 acted as a fertilizer to increase plant biomass [16,60]. A similar phenomenon was found in our study. Compared to ambient air, elevated O3 significantly decreased leaf biomass of P. edulis and O. lubricum by 35.1% and 26.7%, respectively (Table 3), while elevated CO2 significantly increased leaf biomass of the two bamboo species by 24.9% and 20.9%, respectively. Some studies have demonstrated that combined elevated CO2 and O3 does not change leaf biomass as elevated CO2 alleviates the negative effects induced in plants by elevated O3 [35,61,62]. A similar result was found in the present study (Table 3).

3.3. N, P, and K Uptake

We found that elevated CO2, compared to ambient air, increased leaf N uptake (+47.9%) in P. edulis and K uptake (+59.6%) in O. lubricum (Figure 1). This is consistent with previous findings that elevated CO2 promotes nutrient uptake in plants to satisfy the demands of plant growth [7,11,12]. In addition, it is likely that elevated CO2 could have various implications on nutrient dynamics between bamboo requirement and supplement among different bamboo species, which have proved in other plants [63]. However, the mechanisms underlying the observed discrepancy in nutrient demand of P. edulis and O. lubricum under elevated CO2 remain unclear and need further research. Compared to ambient air, elevated O3 decreased significantly leaf N (−28.9%), P (−31.6%), and K (−29.6%) uptake in P. edulis and N (−25.7%) and P (−25.8%) uptake in O. lubricum (Figure 1), which can be attributed to nutrient-uptake limitation in the plants (including P. edulis and O. lubricum) caused by O3-induced plant growth inhibition [5,31]. In addition, the combination of elevated CO2 and O3, in comparison with ambient air, significantly decreased P uptake in P. edulis (−13.0%) and N uptake in O. lubricum (−18.3%) (Figure 1). This result implies that: (1) leaf nutrient uptake under a combination of elevated CO2 and O3 was used to repair O3-induced plant damage and maintain regular growth [27,38]; (2) the difference in nutrient uptake in P. edulis and O. lubricum further revealed that there are species-dependent physiological mechanisms and adaptive mechanisms affecting nutrient uptake under elevated CO2 and O3 conditions. Nonetheless, it should be noted that the combination of elevated CO2 and O3 significantly increased K uptake in O. lubricum (+22.1%), which is likely related to properties of K that enhance plant resistance to environmental stress [39,64] and could also explain the higher tolerance of O. lubricum under elevated CO2 and O3 as reported by Zhuang et al. from the nutrient perspective [43,44,45].

4. Conclusions

Elevated O3 decreased leaf biomass and nutrient uptake in both P. edulis and O. lubricum to some extent, while elevated CO2 increased leaf biomass and uptake of some nutrients in both bamboo species. The combination of elevated CO2 and O3 did not change leaf biomass but altered certain nutrients in the two bamboo species. The differential response of P. edulis and O. lubricum to elevated CO2 and O3 or combined in terms of nutrient uptake indicated that nutrient management in bamboo forests under further climate change should consider differences between bamboo species (Figure 2). In addition, the nutrient (N, P, and K) supply in our experimental soil was sufficient to either maintain or increase nutrient uptake of both bamboo species under elevated CO2 and O3; however, the utilization of leaf nutrients was still relatively low, especially under elevated O3. Therefore, further research on enhanced utilization of nutrients in bamboo is required for the development of effective strategies in nutrient (N, P, and K) management for sustainable management of bamboo ecosystems under climate change (e.g., elevated CO2 and O3).

Acknowledgments

This study was supported by the fundamental research funds for Central Non-Profit Research Institutes (No. RISF2014006 and RISF6915) and the National Natural Science Foundation of China (31770447).

Author Contributions

Minghao Zhuang, Yingchun Li, Ziwu Guo and Shuanglin Chen conceived and designed the experiment. Minghao Zhuang performed data analysis and wrote the manuscript. Minghao Zhuang, Yueqiao Li and Wenting Pan conducted the sampling, pre-treatment and experiment work.

Conflicts of Interest

The authors declare no competing financial interest.

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Forests 09 00195 g001 550
Figure 1. Leaf nutrient uptake (g) (mean ± s.d.) of Phyllostachys edulis and Oligostachyum lubricum in response to ambient air, elevated O3, CO2 and combined elevated O3 and CO2. Different letters indicate significant differences among treatments (p < 0.05).
Figure 1. Leaf nutrient uptake (g) (mean ± s.d.) of Phyllostachys edulis and Oligostachyum lubricum in response to ambient air, elevated O3, CO2 and combined elevated O3 and CO2. Different letters indicate significant differences among treatments (p < 0.05).
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Forests 09 00195 g002 550
Figure 2. Significant change in P uptake of Phyllostachys edulis and N and K uptake of Oligostachyum lubricum under combined elevated O3 and CO2.
Figure 2. Significant change in P uptake of Phyllostachys edulis and N and K uptake of Oligostachyum lubricum under combined elevated O3 and CO2.
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Table
Table 1. 2 × 2 factorial design.
Table 1. 2 × 2 factorial design.
O3 (nmol mL−1)CO2 (μmol mol−1)
360~380685~730
40~45Ambient airElevated CO2
92~106Elevated O3Combined elevated CO2 and O3
Table
Table 2. Leaf nutrient concentrations (g/kg DM) (mean ± s.d., kg DM) of Phyllostachys edulis and Oligostachyum lubricum in response to ambient air, elevated O3, CO2 and combined elevated O3 and CO2. Different letters indicate significant differences among treatments (p < 0.05).
Table 2. Leaf nutrient concentrations (g/kg DM) (mean ± s.d., kg DM) of Phyllostachys edulis and Oligostachyum lubricum in response to ambient air, elevated O3, CO2 and combined elevated O3 and CO2. Different letters indicate significant differences among treatments (p < 0.05).
Bamboo SpeciesDetermination IndexTreatments
Ambient Air Elevated CO2Elevated O3Combined Elevated CO2 and O3
Phyllostachys edulis (Carrière) J.Houz.N19.37 ± 0.46b22.96 ± 0.41a21.20 ± 0.58ab20.50 ± 0.61b
P1.27 ± 0.04a0.97 ± 0.02b1.35 ± 0.04a1.01 ± 0.05b
K8.41 ± 0.10ab5.88 ± 0.82c9.17 ± 0.89a7.34 ± 0.96bc
Oligostachyum lubricum (wen) King f.N17.97 ± 1.07a15.37 ± 0.45b18.30 ± 0.40a15.90 ± 0.89b
P1.05 ± 0.08a0.81 ± 0.05b1.07 ± 0.42a1.06 ± 0.16a
K4.25 ± 0.45b5.62 ± 0.20a6.35 ± 0.39a5.60 ± 0.63a
Table
Table 3. The leaf biomass (kg DM) (mean ± s.d., kg DM) of Phyllostachys edulis and Oligostachyum lubricum in response to ambient air, elevated O3, CO2 and combined elevated O3 and CO2. Different letters indicate significant differences among treatments (p < 0.05).
Table 3. The leaf biomass (kg DM) (mean ± s.d., kg DM) of Phyllostachys edulis and Oligostachyum lubricum in response to ambient air, elevated O3, CO2 and combined elevated O3 and CO2. Different letters indicate significant differences among treatments (p < 0.05).
Bamboo SpeciesTreatments
Ambient Air Elevated CO2Elevated O3Combined Elevated CO2 and O3
Phyllostachys edulis73.17 ± 6.01b91.39 ± 7.14a 47.54 ± 3.53c80.34 ± 4.84b
Oligostachyum lubricum62.67 ± 2.28b75.77 ± 1.87a 45.97 ± 2.79c58.07 ± 2.24b

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Zhuang, M.; Li, Y.; Guo, Z.; Li, Y.; Pan, W.; Chen, S. Elevated CO2 and O3 Levels Influence the Uptake and Leaf Concentration of Mineral N, P, K in Phyllostachys edulis (Carrière) J.Houz. and Oligostachyum lubricum (wen) King f. Forests 2018, 9, 195. https://doi.org/10.3390/f9040195

AMA Style

Zhuang M, Li Y, Guo Z, Li Y, Pan W, Chen S. Elevated CO2 and O3 Levels Influence the Uptake and Leaf Concentration of Mineral N, P, K in Phyllostachys edulis (Carrière) J.Houz. and Oligostachyum lubricum (wen) King f. Forests. 2018; 9(4):195. https://doi.org/10.3390/f9040195

Chicago/Turabian Style

Zhuang, Minghao, Yingchun Li, Ziwu Guo, Yueqiao Li, Wenting Pan, and Shuanglin Chen. 2018. "Elevated CO2 and O3 Levels Influence the Uptake and Leaf Concentration of Mineral N, P, K in Phyllostachys edulis (Carrière) J.Houz. and Oligostachyum lubricum (wen) King f." Forests 9, no. 4: 195. https://doi.org/10.3390/f9040195

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