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Influences of plant species and radial oxygen loss on nitrous oxide fluxes in constructed wetlands
Ecological Engineering 142 (2020) 105644
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Influences of plant species and radial oxygen loss on nitrous oxide fluxes in constructed wetlands ⁎
Xuyao Jianga, Yunfei Tiana, Xiyan Jia, Changyu Lub, , Jibiao Zhanga, a b
T
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Department of Environmental Science and Engineering, Fudan University, Shanghai 200433, PR China Department of Water Resource and Environment, Hebei Geo University, Shijiazhuang 050031, PR China
A R T I C LE I N FO
A B S T R A C T
Keywords: Constructed wetlands N2O fluxes Radial oxygen loss Correlations Significant difference
Constructed wetlands have been used as a green technology to treat wastewaters for several decades. However, constructed wetlands are considered to be great sources of nitrous oxide, a potent greenhouse gas contributing to global warming. Plants play an important role in the nitrogen cycling in wetland ecosystems. To investigate the effects of wetland plants on nitrous oxide fluxes through radial oxygen loss and nutrient removal, integrated vertical flow constructed wetlands were used and planted with three wetland plants (Canna indica L. (C. indica), Acorus calamus L. (A. calamus) and Scirpus validus Vahl (S. validus)). The results showed that integrated vertical flow constructed wetlands were significant sources of nitrous oxide fluxes. However, the nitrous oxide fluxes from the C. indica, A. calamus and S. validus wetlands differed substantially, ranging from 0.05 ± 0.01 to 1.80 ± 0.34, 0.08 ± 0.00 to 0.62 ± 0.20, and 0.03 ± 0.00 to 0.27 ± 0.01 mg N2O-N/m2/h, respectively, and had a similar tendency of seasonal variations: summer > autumn > spring > winter. The nitrous oxide fluxes from the down-flow cells were higher than those from the up-flow cells in every season. Among the three plant species, S. validus was most efficient in removing total nitrogen and ammonium nitrogen while minimizing nitrous oxide fluxes, and could be utilized preferentially as wetland plant. The radial oxygen loss of species has a seasonal tendency: summer > autumn > spring > winter. The nitrous oxide fluxes had positive significant correlations with temperatures, ammonium nitrogen and total nitrogen removal efficiencies and radial oxygen loss. These results contributed to linear prediction and reduction for nitrous oxide fluxes in constructed wetlands.
1. Introduction
contributes to global warming. A CW consists of a mosaic of aerobic and anaerobic microsites where nitrification and denitrification could occur at the same time (Mander et al., 2014). Therefore, N2O emissions are highly variable under different environmental conditions. A literature review by (Mander et al., 2014) indicated that average N2O fluxes in various types of CWs was 1.40–1.97 mg N2O-N/m2/h, and can be influenced by many physical, hydrological and operational factors such as dissolved oxygen (DO), hydraulic retention time, water depth, inflow loading, influent C/N ratio, climate and vegetation. Therefore, to maximise the environmental benefits of CWs as a sustainable wastewater treatment technology, improved understanding of the factors regulating N2O emissions in the treatment processes are necessary for the design of best CW systems. The selection of plants is important in wetland system. Climate, terrain, and human landscape should also be considered. Secondly, strong purification capacity and pollution tolerance of plants were important. It was reported that C. indica, A. calamus and other plants
Nitrous oxide (N2O) accounted for around 6% of the total anthropogenic greenhouse gases, and its concentration in the atmosphere is increasing by 0.2–0.3% per year (IPCC, 2014). N2O in the atmosphere from human activities are approximately equal to that from natural systems. N2O remains in the atmosphere for almost 114 years, and destructs stratosphere (Solomon et al., 2007). Constructed wetlands (CWs) have been widely used for wastewater treatment because of their many advantages including easy operation, low cost and less maintenance (Inamori et al., 2008). The aerobic and anaerobic conditions in CWs are in favor of nutrients removal, especially for nitrogen (N). Effective conversion of N pollutants to gaseous products through nitrification and denitrification was essential for sustainable operation of the system. However, substantial N2O emissions can occur in CWs (Mander et al., 2003), which poses a serious environmental concern as their accumulation in the atmosphere can
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Corresponding authors. E-mail addresses: [email protected] (C. Lu), [email protected] (J. Zhang).
https://doi.org/10.1016/j.ecoleng.2019.105644 Received 31 October 2018; Received in revised form 3 September 2019; Accepted 30 October 2019 Available online 13 November 2019 0925-8574/ © 2019 Elsevier B.V. All rights reserved.
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Roots of Canna and A. calamus were stronger and thicker than others. C. indica and A. calamus leaves' superficial areas were bigger than that of S. validus, which was beneficial to compare ROL, gas emission, and pollutant removal among different plants. Each IVCW was grown with one plant species, at a density of 20 plants/m2 for A. calamus and C. indica, and 20 clusters/m2 for S. validus. Plant seedlings of A. calamus, C. indica and S. validus were obtained from ShangHai AiDe Garden Limited. Synthetic domestic wastewater was employed in the experiment for minimizing the variation in the concentrations of influent pollutants. Specially, the characteristics of the influents were total organic carbon (TOC) 64–84 mg/L, total nitrogen (TN) 50–59 mg/L, ammonia nitrogen (NH4+-N) 20–28 mg/L, total phosphorus (TP) 4–6 mg/L. The IVCW systems were flushed with fresh wastewater once per week, at a hydraulic loading of 330 mm/d.
had high removal of nitrogen and phosphorus (Wu et al., 2016). In addition, flourishing root was one of the factors when selecting wetland plants. Flourishing roots could release much root exudate, which was beneficial for microbial transformation, root biodegradation, and purification capacity of wetlands (Anderson et al., 1994). Roots had important effect on holding the soil, keeping plants and microorganisms vigorous. The root exudates positively influenced the microbial abundance of denitrifying bacteria. Oxygen availability was of great importance to the growth and reproduction of bacteria involved in the nitrogen cycling, especially nitrification and denitrification (Coleman et al., 2001; Pauldaniel et al., 2008). N2O can be produced through a number of different pathways, both chemical and biochemical, during anoxic denitrification and aerobic nitrification (Coleman et al., 2001; Pauldaniel et al., 2008). Plant roots can release oxygen (O2) into their surrounding soil and are a primary oxygen source in the wetland matrix (Soda et al., 2007). The phenomenon that wetland plant roots release oxygen through aerenchyma to rhizosphere is known as “radial oxygen loss (ROL)” (Kludze et al., 1994). As a result of ROL, aerobic and anoxic zones can occur concurrently around the rhizosphere, with the coexistence of aerobic, anaerobic and facultative microorganisms. Therefore, ROL is one of the most important functional characteristics of wetland plants (Cheng et al., 2014). The relationship between ROL and N2O fluxes in constructed wetlands have not been systematically researched. The objectives of this study were to: (Andersen et al., 2003) investigate the seasonal changes on N2O fluxes from the integrated vertical flow constructed wetlands (IVCWs) under three typical plant species, and influence of plant pieces and temperatures on N2O fluxes (Anderson et al., 1994) assess the relationship between N2O fluxes and nutrient removal from the wetlands, and (Bastviken et al., 2009) explore the relationship between N2O fluxes and ROL of the plants.
2.2. Gas sample collection and measurement Gas sampling was conducted using closed chambers. The chambers were made of polymethyl methacrylate with a dimension of 50 cm × 50 cm × 50 cm. The stainless steel base had a dimension of 50 cm × 50 cm × 30 cm. The base was inserted into the soil in each cell to a depth of 10 cm in advance, 30 min before sampling. There was a fan inside the chamber to mix the air. The gases emitted from the treatment cells were trapped by the chamber, and sampled from the air outlet in the middle of the top panel using a 50-ml syringe with a threeway valve. Gas sampling of three plant wetlands were carried out simultaneously. Four gas samples were collected at 0, 20, 40 and 60 min after closure of each chamber between 9:00 and 10:00 am after 48 h of waste water intake. The gas sampling was conducted three times a month. Then the data were used to calculate standard deviation. The sampling campaigns were conducted in summer (July and August of 2016), autumn (September, October, and November of 2016), winter (December of 2016 and January of 2017) and spring (April and May of 2017). Air temperature was recorded before and after air sample collection. To minimize any effects of weather in emissions, samples were taken on both sunny and cloudy days. The air samples were analyzed with a gas chromatograph (Agilent Technologies 7890B, USA) equipped with an electron capture detector (ECD) running at 300 °C. The fluxes were calculated by linear model from the change of gas concentration in the chamber with time over a 60 min period (n = 4) using the following formula as described by Wu et al. (2009):
2. Materials and methods 2.1. Construction of the wetland Three IVCWs were constructed and installed in the campus of Fudan University, Shanghai, China. Shanghai has a subtropical monsoon climate, with an annual average temperature of approximately 17 °C. Two parallel pilot-scale IVCW cells consisting of a down-flow cell (75 cm ∗ 90 cm ∗ 90 cm) and an up-flow cell (75 cm ∗ 90 cm ∗ 90 cm) connected in series, were constructed (Fig. 1). The down-flow cell was filled, from bottom to top, with 20 cm of large gravel (φ = 30–50 mm), 20 cm of small gravel (φ = 10–20 mm), 20 cm of fine sand and 10 cm of soil. The up-flow cell was constructed similarly, but with only 10 cm of fine sand for water falling. Three species of macrophytes, C. indica, A. calamus and S. validus, with different leaves superficial area and roots' thickness, were transplanted into the surface soil on May 20th, 2016.
J=
dc M P T0 28 ∙ ∙ ∙ ∙H∙ dt V0 P0 T 44
(1)
where J is flux (mg N2O-N/m /h); dc/dt is the slope of the gas concentration vs. time plot (mm3/m3/h); M is the N2O mole; P is the atmosphere pressure (Kpa); T is the absolute temperature (K); V0, P0, T0 are volume, absolute temperature and pressure under standard conditions, respectively; and H is chamber height above water surface (m). The monthly average emission rate was calculated by averaging all the N2O fluxes in each month. 2
2.3. Water sampling and analysis Influent and effluent of the cells were sampled to evaluate nutrients transformation and treatment performance, about 50 mL/per sample. The effluent samples were taken from the outlets at the end of every waste water flushing event, three times a month from July of 2016 to May of 2017, immediately before each gas sampling event. Water sampling was conducted three times a month. Then the data were used to calculate standard deviation. The water samples were analyzed for TOC, TP, TN, and NH4+-N. TP and NH4+-N were determined using the methods described by Walter (1989). TOC and TN were measured using a liquid TOC/TN analyser (TOC-L CPH, Shimadzu, Japan). The nutrient removal efficiency was calculated as:
Fig. 1. Diagram of the integrated vertical flow constructed wetlands. 2
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Ce ⎞ × 100 R = ⎛1 − Ci ⎠ ⎝
calamus wetland and S. validus wetland were significantly different (P < 0.05) (Table S4). The annual average N2O emissions for A. calamus, C. indica, and S. validus were 0.52, 0.32 and 0.12 mg N2O-N/m2/ h, respectively. The fluxes from the down-flow cell were higher than the fluxes from the up-flow cell in every season (A. calamus (p < 0.05), C. indica (p < 0.05), S. validus (p > 0.05)) (Tables S5, S6, and S7). Positive correlation was detected between N2O fluxes from the three wetlands and air temperature (p < 0.05). Thus, the N2O fluxes of IVCWs could be predicted approximately from air temperature with the formulas shown in Fig. 2.
(2)
where R is the removal efficiency (%) for a pollutant; Ci and Ce are, respectively, the concentrations of a pollutant in the influent and effluent (mg/L). The monthly mean removal efficiency of a nutrient was calculated as the average value of the nutrient removal efficiencies in the month. 2.4. Radial oxygen loss ROLs of plants were determined in an indoor laboratory of Fudan university in summer (July and August of 2016), autumn (September, October, and November of 2016), winter (December of 2016 and January of 2017) and spring (April and May of 2017) in three replicates for calculating standard deviation. The plants were carefully separated from the soil. The roots were coated with paraffin oil to inhibit contamination by atmospheric O2 and were put in a Ti3+ citrate solution in a flask for 6 h from 9:00 am to 3:00 pm on 15th of every month. The solution was previously purged with N2 gas for 30 min to remove dissolved O2. At the end of the incubation, the flask was lightly shaken to ensure the color liquor well-mixed. Then, 5 mL of the liquor were used to measure the decrease in Ti3+ concentration during the 6 h using a spectrophotometer at the wavelength of 527 nm. The concentration of the Ti3+ citrate solution was estimated according to the standard curve, which was obtained from a serial dilution of Ti3+ citrate solutions with known concentrations. The root oxygen release rate (μmol O2/h/plant) was calculated based on the decrease in the concentration of Ti3+ in the solution as described by Kludze et al. (1994). All the operations were conducted a box flushed with the inert gas of N2.
3.2. Performance of nutrient removal in IVCW Nutrient removal performance was showed in Fig. 3. TOC removal was highly and consistently efficient in all IVCW systems, ranging from 76.34 ± 10.83% to 94.99 ± 0.32%. TP removal ranged from 46.66 ± 5.66% to 89.76 ± 3.50% and TP average removal in the A. calamus wetland, S. validus wetland and C. indica wetland were 68.70%, 57.67%, and 57.41%, respectively. TP removal of A. calamus wetland was significantly higher than that of S. validus wetland and C. indica wetland (P < 0.05) (Table S8). The TP efficiencies of three wetlands varied with seasons: summer > autumn or spring > winter. The TP efficiencies of A. calamus and C. indica wetlands in summer were significantly higher than that in Autumn and Winter (P < 0.05) (Tables S1 and S3). The average TOC removal efficiencies were very high (76.34 ± 10.83%–94.99 ± 0.32%), and The average TOC removal of the A. calamus wetland were higher than those of the S. validus wetland (p > 0.05) (Table S9), with the lowest efficiencies observed for the C. indica wetland. The TOC seasonal removal efficiencies of three plant wetlands were not significant different (p > 0.05) (Tables S1, S2 and S3). The NH4+-N removal in the C. indica wetland (ranging from 30.63 ± 3.61 to 60.93 ± 3.58, average 49.7%) was higher than that in the A. calamus wetland (18.82 ± 4.95–68.78 ± 9.29, average 41.3%), followed by the S. validus wetland (29.58 ± 3.80–53.68 ± 4.66, average 40.4%). The NH4+-N removal in three wetlands had not significant difference (p > 0.05) (Table S10). The TN removal was highest in the C. indica wetland (ranging from 31.7 ± 2.99% to 40.23 ± 4.15%, average 36.3%), followed by the A. calamus wetland (24.10 ± 2.50–41.81 ± 3.99, average 35.1%)，and then by the S. validus wetland (23.21 ± 3.72%-38.58 ± 1.33%, average 32.2%). The TN removal only in S. validus and C. indica wetland showed a significant difference (P < 0.05) (Table S11). The NH4+-N removal and TN removal efficiencies in three wetlands had a similar seasonal variation tendency: summer > autumn or spring > winter. The values of nitrogen removal in summer were significantly different with those in winter (P < 0.05) (Tables S1, S2 and S3). Positive significant relationships between TN removal efficiency, NH4+-N removal efficiency and N2O fluxes from the three wetlands were found in this study (p < 0.05). Moreover, there were no relationship between TOC removal efficiency and N2O fluxes from the wetlands. Significant relationships between TP removal and N2O fluxes were found in the A. calamus wetland (p < 0.05) but not in the C. indica wetland and S. validus wetland. In this study, K1 was N2O fluxes/TN removal efficiency and K2 was N2O fluxes/NH4+-N removal efficiency. Lower values of K1 and K2 for a wetland mean that this system emits less N2O than other wetlands for per unit of TN and NH4+-N removed. The K1 and K2 of A. calamus were higher than C. indica, followed by S. validus (Fig. 4). All the values in three species had a significant difference (P < 0.05) (Tables S12 and S13).
2.5. Statistical analysis The statistical analysis was carried out using SPSS 21 and Origin 2015. Spearman correlation was used to analyze correlations between N2O fluxes and air temperature, nutrient removal efficiencies, and ROL for the wetland plants. The term flux is used for both positive and negative gas exchanges. Positive fluxes represent gas emission, while negative fluxes are used for consumption. When p < 0.05, correlations and difference were considered statistically significant and p < 0.01 was defined as highly significant. One-way ANOVE followed by LSD was conducted to test the difference of different species parameters. The N2O fluxes between down-flow chamber and up-flow chamber were analyzed by independent sample t-test. Pearson correlation was conducted between ROL and nitrogen removal. 3. Results 3.1. Changes N2O fluxes from IVCW The variation of N2O emission from IVCW systems during the experimental period is illustrated in Fig. 2. The N2O fluxes from A. calamus wetland, C. indica wetland and S. validus wetland ranged from 0.05 ± 0.01 to 1.80 ± 0.34, 0.08 ± 0.00 to 0.62 ± 0.20, and 0.03 ± 0.00 to 0.27 ± 0.01 mg N2O-N/m2/h, respectively. N2O fluxes from the three plant wetlands varied seasonally. The N2O fluxes were higher in summer than in spring and fall, and there had lowest N2O fluxes in winter. In the A. calamus and S. validus wetland, The N2O fluxes in summer had a significant different with those in winter (P < 0.05) (Tables S1 and S2). In the C. indica wetland, the N2O fluxes in summer had a significant different with those in Autumn, Spring, and Winter (P < 0.05) (Table S3). Significant differences in N2O fluxes were found among different CWs with various plant species in this study. The A. calamus wetland emitted much higher N2O than the C. indica wetland (P < 0.05), and the S. validus wetland has the lowest emissions. N2O fluxes of the A. 3
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Fig. 2. The monthly average N2O fluxes from three planted wetlands and the relationships with air temperature.
between 0 ± 0.02 and 1.54 ± 0.24 μmol O2/h/plant. The average ROL was 2.13 μmol O2/h/plant for C. indica, 1.84 μmol O2/h/plant for A. calamus, followed by 0.66 μmol O2/h/plant for S. validus. The average ROL of C. indica and A. calamus were much higher than the average ROL of S. validus (P < 0.05) (Table S14). The present study analyzed the ROL of three wetland plants and the N2O fluxes from the wetlands. The results indicated that ROL of wetland plants was positively correlated with N2O fluxes, and can be an indicator to predict N2O fluxes. Pearson correlation was conducted between ROL and TN removal, and NH4+-N removal. The results were shown as Tables S15, S16, and S17. ROL of three plants had a very significant correlation with TN removal, and NH4+-N removal (P < 0.01). TN removal also had a very significant correlation with NH4+-N removal (P < 0.01).
3.3. Radial oxygen loss ROL of the three wetland plants was affected greatly by seasonal conditions (Fig. 5). The highest ROL of the plants appeared in summer, followed by autumn, and then by spring, while lowest values were observed in winter. The ROL of A. calamus and S. validus in summer had a significant difference with ROL in Winter and Spring (P < 0.05) (Tables S1 and S2). The ROL of the C. indica in summer had a significant difference with ROL in Winter, Autumn and Spring (P < 0.05) (Table S3). During the measurement period from July of 2016 to May of 2017, ROL of A. calamus and C. indica ranged from 0.05 ± 0.11 to 3.13 ± 0.25 μmol O2/h/plant and 0.47 ± 0.14–5.04 ± 0.67 μmol O2/h/plant, respectively, whereas S. validus was relative steady
4
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Fig. 3. Nutrient removal efficiencies by three wetlands grown with different plant species (p < 0.05 means a significant correlation between nutrient removal efficiencies and N2O fluxes, p < 0.01 means an extremely significant correlation between nutrient removal efficiencies and N2O fluxes).
4. Discussion
which meant A. calamus's roots had large surface area for nitrification bacteria and denitrification bacteria inhabiting. In addition, large biomass was beneficial for plants transmit gas. Most of N2O producing by roots was transmitted into air through plants (Chang et al., 1998). It was reported that plants release N2O, and the foliage released the highest N2O compared with stem and root (Huang et al., 1992). It could be speculated that A. calamus with luxuriant foliage was beneficial to N2O release. The maximum value (1.8000 ± 0.34 mg N2O-N/m2/h from the down-flow cell of A. calamus wetland in August) measured in this study was higher than the value (0.03 mg N2O-N/m2/h) in a natural ecosystem reported by Saggar et al. (2007), and similar with the value measured in wastewater treatment CWs (1.37 mg N2O-N/m2/h) reported by Wu et al. (2009), but greatly lower than the value
The average N2O fluxes of the A. calamus wetland, C. indica wetland, and S. validus wetland were 0.52, 0.32 and 0.12 mg N2O-N/m2/h, respectively, which indicated that the three plant wetlands functioned as N2O sources during the whole monitoring period. A. calamus wetland reached the highest N2O fluxes (P < 0.05), while S. validus wetland got the lowest (P < 0.05). We concluded that N2O fluxes from constructed wetlands can be decreased significantly through proper selection of plant species. It was reported that stronger root system and higher under-ground biomass of wetland plants have higher removal of nitrogen and phosphorus (Anderson et al., 1994). A. calamus's root was strong and has high above-ground biomass and underground biomass,
Fig. 4. K1 and K2 of three wetlands grown with different plant species (K1: N2O fluxes/TN removal efficiency; K2: N2O fluxes/NH4+-N removal efficiency). 5
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Fig. 5. ROL of three wetland plants and the relationships with average N2O fluxes (ROL: radial oxygen loss).
(1272.73 mg N2O-N/m2/h) measured in a sewage treatment plant (Benckiser et al., 1996). Tian (2016) reported N2O fluxes from −0.01 to 0.20 mg N2O-N/m2/h in IVCWs, similar with the values recorded in this study. The N2O fluxes were higher in summer than in spring and fall, and there had lowest N2O fluxes in winter perhaps due to the plants withering and low microorganism activity in winter. The high temperature in summer led to abundant nitrifying bacteria and denitrifying bacteria, and could result in more N2O emission. Our results indicated that temperature had an important effect on the N2O emission in CWs, which is in agreement with other reports (Zhang et al., 2005). Significantly higher N2O fluxes during the summer season than during winter was found by Søvik et al. (2006). On the other hand, it is well recognized that temperature affects plant photosynthesis and plant biomass directly, and thus increases organic matter and gas transportation, which have positive effects on N2O fluxes (Zhao et al., 2016). High temperatures within certain range where the enzymes are stable and maintain high activity may contribute to biological process in the denitrification (Firestone, 1983). Therefore, it is possible to speculate on the N2O fluxes by measured air temperatures. The N2O fluxes from the down-flow cells were found to be higher than the fluxes from the up-flow cells due to more nutrients in the down-flow cells. The N2O fluxes in A. calamus wetland and S. validus wetland had significant difference between down-flow chamber and upflow chamber (P < 0.05). Johansson et al. (2010) and Mander et al. (2003) both reported that there were higher N2O emission rates at water inlets than those at the water outlets. More NO3− in the downflow cell, which are available for the denitrification process, may contribute to higher N2O emission rates compared to the up-flow cell (Wu, 2014). The removal efficiencies of TN and NH4+-N in the IVCW of this study were relatively low, which agrees with the study results of an approximately 30% removal efficiency using wetlands to reduce N from wastewater following the conventional secondary treatment (Andersen et al., 2003). However, the N removal efficiencies in this study were lower than those reported in studies of Andersen et al. (2003). The low efficiencies might have resulted from a higher hydraulic loading rate (330 mm/d) used in the present study as compared to theirs (18–100 mm/d). It was also reported that high hydraulic loading rates could result in low nutrient removal efficiencies (Karpuzcu and Stringfellow, 2012). It was probably that hydraulic loading rate resulted in anaerobic situation and it could affect nitrification that transformed NH4+-N to NO3−. The results in Tables S1, S2, and S3 showed that both of NH4+-N removal and TN removal efficiencies had significant difference between summer and winter (P < 0.05). The NH4+-N removal and TN removal efficiencies had a similar seasonal variation tendency: summer > autumn or spring > winter, which agreed well with other reported results (Bastviken et al., 2009; Spieles
and Mitsch, 1999). This significant seasonal variation of nitrogen removal efficiency could be primarily attributed to the annual growing cycle of the plants and the sensitiveness of nitrification and denitrification to environmental conditions particularly temperatures. TP removal efficiencies were primarily achieved through soil adsorption and plant uptake (Inamori et al., 2007). The TP removal efficiencies of the three planted wetlands were highest in the summer, which could be explained by the peak biomasses in the summer. Starting in September, plants began to lose leaves, and the accumulated phosphorus start to be released from the fallen leaves. A resultant sharp decrease in phosphorus removal efficiency was thus observed in the autumn and winter. The wetland plants started to absorb more phosphorus in the second spring due to the plant growth (Fig. 3). TOC removal had low correlation with seasons (P > 0.05), this may be because microorganisms rather than plants in the IVCWs largely contributed to the TOC removal (Reddy and D'Angelo, 1997). TOC removal was very high, and also had no significant difference with species (P > 0.05). Glucose in the waste water was easily consumed, with single organic composition. Higher N2O fluxes and NH4+-N and TN removal efficiencies were obtained in the A. calamus and C. indica wetlands compared to the S. validus wetland (Figs. 2 and 3), suggesting that A. calamus and C. indica wetlands had higher N removal efficiencies with potentially larger contribution to global warming. We assume that nitrification and denitrification were responsible for N2O production, with the highest rates in summer and the lowest in winter. N2O can be produced through nitrification (conversion of ammonia to nitrate) and denitrification (conversion of nitrate to N2) (Colliver and Stephenson, 2000). S. validus wetland had the lowest K1 and K2 values (P < 0.05). It proved that S. validus wetland had the lowest global warming potential in terms of N2O fluxes per unit of TN and NH4+-N removed. Hence, we can preferentially choose S. validus as a waste water treatment plant in the IVCW for removing TN and NH4+-N while minimizing N2O fluxes. Plants transfer oxygen to the root system through aerenchyma. The present results showed ROL of C. indica (average 2.13 μmol O2/h/plant) was higher than A. calamus (average 1.84 μmol O2/h/plant), followed by S. validus (average 0.66 μmol O2/h/plant). S. validus got the lowest ROL (P < 0.05). These variations were consistent with the highest aboveground and belowground biomass of C. indica, followed by A. calamus, and then by S. validus. Broad leaves were in favor of photosynthesis and absorbing oxygen in the atmosphere. Plants used aerenchyma to transmit oxygen to the root system, which informed ROL. It has been reported that there were significant differences in ROL among different plant species (Li et al., 2011). It was found that Phragmites australis had high value of ROL at 5.27 μmol O2/h/plant, followed by Typha orientalis Presl at 4.78 μmol O2/h/plant, and Arundo donax at 3.46 μmol O2/h/plant (Wang, 2015). A previous study showed ROL of Phragmites australis > Typha orientalis Presl > Scirpus validus Vahl 6
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Appendix A. Supplementary data
(Wu, 2014). Remarkable seasonal variation in ROL in IVCWs systems was observed, with summer > autumn > spring > winter. The high temperature and abundant light in summer favored plant growth and thus the highest value of ROL in a year. In autumn, decreasing air temperature and decreasing light resulted in ROL of plants gradually decreased. In winter, the low temperature (7 to 11 °C) and low light led to plant root system being in dormancy with almost zero ROL. In spring, plants were in growing period, and ROL of plants increased gradually. Previous studies showed that ROL reached maximum values in summer or autumn due to the highest photosynthetic rates and growth rates (Cheng et al., 2014). We found three species' ROL had a significant correlation with TN removal and NH4+-N removal (P < 0.01) (Tables S15, S16 and S17), this could be nitration needs oxygen, and ROL provided oxygen for nitration reaction. Up to now, little work has been done directly on the correlation between ROL and N2O fluxes from wetlands. We also found that ROL was positively correlated with N2O fluxes (p < 0.05), and ROL of wetland plants was one of the most important influencing factors of N2O fluxes, suggesting that the oxidizing capacity in anaerobic environment is important for N2O emissions. The complicated nitrogen cycle in wetlands is discussed in detail by Reed et al. (1988). Nitrification and denitrification are the major nitrogen removal processes. N2O production through denitrification was been identified as the significant pathway under aerobic conditions. The last step of denitrification, in term of the conversion of N2O to N2, was easily disrupted by oxygen and led to incomplete denitrification and N2O emission (Colliver and Stephenson, 2000). Higher ROL may increase more oxygen release to the surrounding water and reduce denitrification, which might resulted in the higher N2O/N2 ratios. Hence, ROL from wetland plants could be applied to predict N2O fluxes approximately (Fig. 5), according to the formulas. To adapt to the anaerobic environment with low redox potentials, wetland plants have developed an efficient strategy releasing oxygen from roots to oxidize the rhizosphere. The oxidizing capacity played an important role in surviving the anaerobic environment.
Supplementary data to this article can be found online at https:// doi.org/10.1016/j.ecoleng.2019.105644. References Andersen, D.C., Sartoris, J.J., Thullen, J.S., Reusch, P.G., 2003. The effects of bird use on nutrient removal in a constructed wastewater-treatment wetland. Wetlands 23, 423–435. Anderson, T.A., Cuthie, E.A., Walton, B.T., 1994. Bioremediation in the rhizosphere. Environ. Sci. Technol. 27, 2630–2636. Bastviken, S.K., Weisner, S.E.B., Thiere, G., Svensson, J.M., Ehde, P.M., Tonderski, K.S., 2009. Effects of vegetation and hydraulic load on seasonal nitrate removal in treatment wetlands. Ecol. Eng. 35, 946–952. Benckiser, G., Eilts, R., Linn, A., Lorch, H.J., Sümer, E., Weiske, A., Wenzhöfer, F., 1996. N2O emissions from different cropping systems and from aerated, nitrifying and denitrifying tanks of a municipal waste water treatment plant. Biol. Fert. Soils 23, 257–265. Chang, C., Janzen, H.H., Nakonechny, E.M., Cho, C.M., 1998. Nitrous oxide emission through plants. 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Investigating CH4 and N2O emissions from eco-engineering wastewater treatment processes using constructed wetland microcosms. Process Biochem. 42, 363–373. Inamori, R., Wang, Y., Yamamoto, T., Zhang, J., Kong, H., Xu, K., Inamori, Y., 2008. Seasonal effect on N2O formation in nitrification in constructed wetlands. Chemosphere 73, 1071–1077. IPCC, 2014. Climate change 2014: synthesis report. In: Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Johansson, A.E., Klemedtsson, Å.K., Klemedtsson, L., Svensson, B.H., 2010. Nitrous oxide exchanges with the atmosphere of a constructed wetland treating wastewater. Tellus Ser. B Chem. Phys. Meteorol. 55, 737–750. Karpuzcu, M.E., Stringfellow, W.T., 2012. Kinetics of nitrate removal in wetlands receiving agricultural drainage. Ecol. Eng. 42, 295–303. Kludze, H.K., Delaune, R.D., Patrick, W.H., 1994. 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Biogeochemical indicators to evaluate pollutant removal efficiency in constructed wetlands. Water Sci. Technol. 35, 1–10. Reed, S.C., Crites, R.W., Middlebrooks, E.J., 1988. Natural systems for waste management and treatment. McGraw-Hill 22, 35–38. Saggar, S., Hedley, C.B., Giltrap, D.L., Lambie, S.M., 2007. Measured and modeled estimates of nitrous oxide emission and methane consumption from a sheep-grazed pasture. Agric. Ecosyst. Environ. 122, 357–365. Soda, S., Ike, M., Ogasawara, Y., Yoshinaka, M., Mishima, D., Fujita, M., 2007. Effects of light intensity and water temperature on oxygen release from roots into water lettuce rhizosphere. Water Res. 41, 487–491. Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K., Tignor, M., Miller, H., 2007. Climate change 2007: the physical science basis. In: Contribution of Working Group I to the Fourth 16 Assessment Report of the Intergovernmental Panel on Climate Change. Computational Geometry 2007. pp. 1–21. 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5. Conclusions In this study, N2O fluxes from A. calamus, S. validus and C. indica wetlands, ranging from 0.05 ± 0.01 to 1.80 ± 0.34, 0.08 ± 0.00 to 0.62 ± 0.20, and 0.03 ± 0.00 to 0.27 ± 0.01 mg N2O-N/m2/h, respectively, and had a similar seasonal variations tendency: summer > autumn > spring > winter. The N2O fluxes from the down-flow cells were higher than those from the up-flow cells due to more nutrients in the down-flow cells. The S. validus wetland was more efficient in mitigating N2O fluxes and removing TN and NH4+-N. N2O fluxes had significant correlation with NH4+-N and TN removal efficiencies and ROL of the three wetland plants. On the whole, these results provided insight in seasons, temperatures, the plant species and ROL in relation to the N2O fluxes from IVCWs systems and can be utilized in future efforts to reduce N2O fluxes.
Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments This work is financially supported by the National Natural Science Foundation of China (No. 51308127). 7
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of purification effect on eutrophic water by Canna indica L., Iris tectorum, Lythrum salicaria L. and Iris pseudacorus. J. Anhui Univ. (Nat. Sci. Ed.) 40, 98–108. Zhang, J.B., Song, C.C., Yang, W.Y., 2005. Cold season CH4, CO2 and N2O fluxes from freshwater marshes in northeast China. Chemosphere 59, 1703–1705. Zhao, Z., Chang, J., Han, W., Wang, M., Ma, D., Du, Y., Qu, Z., Chang, S.X., Ge, Y., 2016. Effects of plant diversity and sand particle size on methane emission and nitrogen removal in microcosms of constructed wetlands. Ecol. Eng. 95, 390–398.
Wang, Q., 2015. Study on the Mechanism of Radial Oxygen Loss Affected Pollutant Removal in Constructed Wetlands. ShanDong university. Wu, H., 2014. Cyclic Processes of Carbon, Nitrogen and Phosphorus in Constructed Wetlands and Its Environmental Effects. ShanDong university. Wu, J., Zhang, J., Jia, W., Xie, H., Gu, R.R., Li, C., Gao, B., 2009. Impact of COD/N ratio on nitrous oxide emission from microcosm wetlands and their performance in removing nitrogen from wastewater. Bioresour. Technol. 100, 2910–2917. Wu, S.J., Chen, H.J., Xu, X.L., Ma, X.L., Yang, J., Wang, S.P., Liang, W.Y., 2016. Analysis
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Influences of plant species and radial oxygen loss on nitrous oxide fluxes in constructed wetlands ⁎
Xuyao Jianga, Yunfei Tiana, Xiyan Jia, Changyu Lub, , Jibiao Zhanga, a b
T
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Department of Environmental Science and Engineering, Fudan University, Shanghai 200433, PR China Department of Water Resource and Environment, Hebei Geo University, Shijiazhuang 050031, PR China
A R T I C LE I N FO
A B S T R A C T
Keywords: Constructed wetlands N2O fluxes Radial oxygen loss Correlations Significant difference
Constructed wetlands have been used as a green technology to treat wastewaters for several decades. However, constructed wetlands are considered to be great sources of nitrous oxide, a potent greenhouse gas contributing to global warming. Plants play an important role in the nitrogen cycling in wetland ecosystems. To investigate the effects of wetland plants on nitrous oxide fluxes through radial oxygen loss and nutrient removal, integrated vertical flow constructed wetlands were used and planted with three wetland plants (Canna indica L. (C. indica), Acorus calamus L. (A. calamus) and Scirpus validus Vahl (S. validus)). The results showed that integrated vertical flow constructed wetlands were significant sources of nitrous oxide fluxes. However, the nitrous oxide fluxes from the C. indica, A. calamus and S. validus wetlands differed substantially, ranging from 0.05 ± 0.01 to 1.80 ± 0.34, 0.08 ± 0.00 to 0.62 ± 0.20, and 0.03 ± 0.00 to 0.27 ± 0.01 mg N2O-N/m2/h, respectively, and had a similar tendency of seasonal variations: summer > autumn > spring > winter. The nitrous oxide fluxes from the down-flow cells were higher than those from the up-flow cells in every season. Among the three plant species, S. validus was most efficient in removing total nitrogen and ammonium nitrogen while minimizing nitrous oxide fluxes, and could be utilized preferentially as wetland plant. The radial oxygen loss of species has a seasonal tendency: summer > autumn > spring > winter. The nitrous oxide fluxes had positive significant correlations with temperatures, ammonium nitrogen and total nitrogen removal efficiencies and radial oxygen loss. These results contributed to linear prediction and reduction for nitrous oxide fluxes in constructed wetlands.
1. Introduction
contributes to global warming. A CW consists of a mosaic of aerobic and anaerobic microsites where nitrification and denitrification could occur at the same time (Mander et al., 2014). Therefore, N2O emissions are highly variable under different environmental conditions. A literature review by (Mander et al., 2014) indicated that average N2O fluxes in various types of CWs was 1.40–1.97 mg N2O-N/m2/h, and can be influenced by many physical, hydrological and operational factors such as dissolved oxygen (DO), hydraulic retention time, water depth, inflow loading, influent C/N ratio, climate and vegetation. Therefore, to maximise the environmental benefits of CWs as a sustainable wastewater treatment technology, improved understanding of the factors regulating N2O emissions in the treatment processes are necessary for the design of best CW systems. The selection of plants is important in wetland system. Climate, terrain, and human landscape should also be considered. Secondly, strong purification capacity and pollution tolerance of plants were important. It was reported that C. indica, A. calamus and other plants
Nitrous oxide (N2O) accounted for around 6% of the total anthropogenic greenhouse gases, and its concentration in the atmosphere is increasing by 0.2–0.3% per year (IPCC, 2014). N2O in the atmosphere from human activities are approximately equal to that from natural systems. N2O remains in the atmosphere for almost 114 years, and destructs stratosphere (Solomon et al., 2007). Constructed wetlands (CWs) have been widely used for wastewater treatment because of their many advantages including easy operation, low cost and less maintenance (Inamori et al., 2008). The aerobic and anaerobic conditions in CWs are in favor of nutrients removal, especially for nitrogen (N). Effective conversion of N pollutants to gaseous products through nitrification and denitrification was essential for sustainable operation of the system. However, substantial N2O emissions can occur in CWs (Mander et al., 2003), which poses a serious environmental concern as their accumulation in the atmosphere can
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Corresponding authors. E-mail addresses: [email protected] (C. Lu), [email protected] (J. Zhang).
https://doi.org/10.1016/j.ecoleng.2019.105644 Received 31 October 2018; Received in revised form 3 September 2019; Accepted 30 October 2019 Available online 13 November 2019 0925-8574/ © 2019 Elsevier B.V. All rights reserved.
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Roots of Canna and A. calamus were stronger and thicker than others. C. indica and A. calamus leaves' superficial areas were bigger than that of S. validus, which was beneficial to compare ROL, gas emission, and pollutant removal among different plants. Each IVCW was grown with one plant species, at a density of 20 plants/m2 for A. calamus and C. indica, and 20 clusters/m2 for S. validus. Plant seedlings of A. calamus, C. indica and S. validus were obtained from ShangHai AiDe Garden Limited. Synthetic domestic wastewater was employed in the experiment for minimizing the variation in the concentrations of influent pollutants. Specially, the characteristics of the influents were total organic carbon (TOC) 64–84 mg/L, total nitrogen (TN) 50–59 mg/L, ammonia nitrogen (NH4+-N) 20–28 mg/L, total phosphorus (TP) 4–6 mg/L. The IVCW systems were flushed with fresh wastewater once per week, at a hydraulic loading of 330 mm/d.
had high removal of nitrogen and phosphorus (Wu et al., 2016). In addition, flourishing root was one of the factors when selecting wetland plants. Flourishing roots could release much root exudate, which was beneficial for microbial transformation, root biodegradation, and purification capacity of wetlands (Anderson et al., 1994). Roots had important effect on holding the soil, keeping plants and microorganisms vigorous. The root exudates positively influenced the microbial abundance of denitrifying bacteria. Oxygen availability was of great importance to the growth and reproduction of bacteria involved in the nitrogen cycling, especially nitrification and denitrification (Coleman et al., 2001; Pauldaniel et al., 2008). N2O can be produced through a number of different pathways, both chemical and biochemical, during anoxic denitrification and aerobic nitrification (Coleman et al., 2001; Pauldaniel et al., 2008). Plant roots can release oxygen (O2) into their surrounding soil and are a primary oxygen source in the wetland matrix (Soda et al., 2007). The phenomenon that wetland plant roots release oxygen through aerenchyma to rhizosphere is known as “radial oxygen loss (ROL)” (Kludze et al., 1994). As a result of ROL, aerobic and anoxic zones can occur concurrently around the rhizosphere, with the coexistence of aerobic, anaerobic and facultative microorganisms. Therefore, ROL is one of the most important functional characteristics of wetland plants (Cheng et al., 2014). The relationship between ROL and N2O fluxes in constructed wetlands have not been systematically researched. The objectives of this study were to: (Andersen et al., 2003) investigate the seasonal changes on N2O fluxes from the integrated vertical flow constructed wetlands (IVCWs) under three typical plant species, and influence of plant pieces and temperatures on N2O fluxes (Anderson et al., 1994) assess the relationship between N2O fluxes and nutrient removal from the wetlands, and (Bastviken et al., 2009) explore the relationship between N2O fluxes and ROL of the plants.
2.2. Gas sample collection and measurement Gas sampling was conducted using closed chambers. The chambers were made of polymethyl methacrylate with a dimension of 50 cm × 50 cm × 50 cm. The stainless steel base had a dimension of 50 cm × 50 cm × 30 cm. The base was inserted into the soil in each cell to a depth of 10 cm in advance, 30 min before sampling. There was a fan inside the chamber to mix the air. The gases emitted from the treatment cells were trapped by the chamber, and sampled from the air outlet in the middle of the top panel using a 50-ml syringe with a threeway valve. Gas sampling of three plant wetlands were carried out simultaneously. Four gas samples were collected at 0, 20, 40 and 60 min after closure of each chamber between 9:00 and 10:00 am after 48 h of waste water intake. The gas sampling was conducted three times a month. Then the data were used to calculate standard deviation. The sampling campaigns were conducted in summer (July and August of 2016), autumn (September, October, and November of 2016), winter (December of 2016 and January of 2017) and spring (April and May of 2017). Air temperature was recorded before and after air sample collection. To minimize any effects of weather in emissions, samples were taken on both sunny and cloudy days. The air samples were analyzed with a gas chromatograph (Agilent Technologies 7890B, USA) equipped with an electron capture detector (ECD) running at 300 °C. The fluxes were calculated by linear model from the change of gas concentration in the chamber with time over a 60 min period (n = 4) using the following formula as described by Wu et al. (2009):
2. Materials and methods 2.1. Construction of the wetland Three IVCWs were constructed and installed in the campus of Fudan University, Shanghai, China. Shanghai has a subtropical monsoon climate, with an annual average temperature of approximately 17 °C. Two parallel pilot-scale IVCW cells consisting of a down-flow cell (75 cm ∗ 90 cm ∗ 90 cm) and an up-flow cell (75 cm ∗ 90 cm ∗ 90 cm) connected in series, were constructed (Fig. 1). The down-flow cell was filled, from bottom to top, with 20 cm of large gravel (φ = 30–50 mm), 20 cm of small gravel (φ = 10–20 mm), 20 cm of fine sand and 10 cm of soil. The up-flow cell was constructed similarly, but with only 10 cm of fine sand for water falling. Three species of macrophytes, C. indica, A. calamus and S. validus, with different leaves superficial area and roots' thickness, were transplanted into the surface soil on May 20th, 2016.
J=
dc M P T0 28 ∙ ∙ ∙ ∙H∙ dt V0 P0 T 44
(1)
where J is flux (mg N2O-N/m /h); dc/dt is the slope of the gas concentration vs. time plot (mm3/m3/h); M is the N2O mole; P is the atmosphere pressure (Kpa); T is the absolute temperature (K); V0, P0, T0 are volume, absolute temperature and pressure under standard conditions, respectively; and H is chamber height above water surface (m). The monthly average emission rate was calculated by averaging all the N2O fluxes in each month. 2
2.3. Water sampling and analysis Influent and effluent of the cells were sampled to evaluate nutrients transformation and treatment performance, about 50 mL/per sample. The effluent samples were taken from the outlets at the end of every waste water flushing event, three times a month from July of 2016 to May of 2017, immediately before each gas sampling event. Water sampling was conducted three times a month. Then the data were used to calculate standard deviation. The water samples were analyzed for TOC, TP, TN, and NH4+-N. TP and NH4+-N were determined using the methods described by Walter (1989). TOC and TN were measured using a liquid TOC/TN analyser (TOC-L CPH, Shimadzu, Japan). The nutrient removal efficiency was calculated as:
Fig. 1. Diagram of the integrated vertical flow constructed wetlands. 2
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Ce ⎞ × 100 R = ⎛1 − Ci ⎠ ⎝
calamus wetland and S. validus wetland were significantly different (P < 0.05) (Table S4). The annual average N2O emissions for A. calamus, C. indica, and S. validus were 0.52, 0.32 and 0.12 mg N2O-N/m2/ h, respectively. The fluxes from the down-flow cell were higher than the fluxes from the up-flow cell in every season (A. calamus (p < 0.05), C. indica (p < 0.05), S. validus (p > 0.05)) (Tables S5, S6, and S7). Positive correlation was detected between N2O fluxes from the three wetlands and air temperature (p < 0.05). Thus, the N2O fluxes of IVCWs could be predicted approximately from air temperature with the formulas shown in Fig. 2.
(2)
where R is the removal efficiency (%) for a pollutant; Ci and Ce are, respectively, the concentrations of a pollutant in the influent and effluent (mg/L). The monthly mean removal efficiency of a nutrient was calculated as the average value of the nutrient removal efficiencies in the month. 2.4. Radial oxygen loss ROLs of plants were determined in an indoor laboratory of Fudan university in summer (July and August of 2016), autumn (September, October, and November of 2016), winter (December of 2016 and January of 2017) and spring (April and May of 2017) in three replicates for calculating standard deviation. The plants were carefully separated from the soil. The roots were coated with paraffin oil to inhibit contamination by atmospheric O2 and were put in a Ti3+ citrate solution in a flask for 6 h from 9:00 am to 3:00 pm on 15th of every month. The solution was previously purged with N2 gas for 30 min to remove dissolved O2. At the end of the incubation, the flask was lightly shaken to ensure the color liquor well-mixed. Then, 5 mL of the liquor were used to measure the decrease in Ti3+ concentration during the 6 h using a spectrophotometer at the wavelength of 527 nm. The concentration of the Ti3+ citrate solution was estimated according to the standard curve, which was obtained from a serial dilution of Ti3+ citrate solutions with known concentrations. The root oxygen release rate (μmol O2/h/plant) was calculated based on the decrease in the concentration of Ti3+ in the solution as described by Kludze et al. (1994). All the operations were conducted a box flushed with the inert gas of N2.
3.2. Performance of nutrient removal in IVCW Nutrient removal performance was showed in Fig. 3. TOC removal was highly and consistently efficient in all IVCW systems, ranging from 76.34 ± 10.83% to 94.99 ± 0.32%. TP removal ranged from 46.66 ± 5.66% to 89.76 ± 3.50% and TP average removal in the A. calamus wetland, S. validus wetland and C. indica wetland were 68.70%, 57.67%, and 57.41%, respectively. TP removal of A. calamus wetland was significantly higher than that of S. validus wetland and C. indica wetland (P < 0.05) (Table S8). The TP efficiencies of three wetlands varied with seasons: summer > autumn or spring > winter. The TP efficiencies of A. calamus and C. indica wetlands in summer were significantly higher than that in Autumn and Winter (P < 0.05) (Tables S1 and S3). The average TOC removal efficiencies were very high (76.34 ± 10.83%–94.99 ± 0.32%), and The average TOC removal of the A. calamus wetland were higher than those of the S. validus wetland (p > 0.05) (Table S9), with the lowest efficiencies observed for the C. indica wetland. The TOC seasonal removal efficiencies of three plant wetlands were not significant different (p > 0.05) (Tables S1, S2 and S3). The NH4+-N removal in the C. indica wetland (ranging from 30.63 ± 3.61 to 60.93 ± 3.58, average 49.7%) was higher than that in the A. calamus wetland (18.82 ± 4.95–68.78 ± 9.29, average 41.3%), followed by the S. validus wetland (29.58 ± 3.80–53.68 ± 4.66, average 40.4%). The NH4+-N removal in three wetlands had not significant difference (p > 0.05) (Table S10). The TN removal was highest in the C. indica wetland (ranging from 31.7 ± 2.99% to 40.23 ± 4.15%, average 36.3%), followed by the A. calamus wetland (24.10 ± 2.50–41.81 ± 3.99, average 35.1%)，and then by the S. validus wetland (23.21 ± 3.72%-38.58 ± 1.33%, average 32.2%). The TN removal only in S. validus and C. indica wetland showed a significant difference (P < 0.05) (Table S11). The NH4+-N removal and TN removal efficiencies in three wetlands had a similar seasonal variation tendency: summer > autumn or spring > winter. The values of nitrogen removal in summer were significantly different with those in winter (P < 0.05) (Tables S1, S2 and S3). Positive significant relationships between TN removal efficiency, NH4+-N removal efficiency and N2O fluxes from the three wetlands were found in this study (p < 0.05). Moreover, there were no relationship between TOC removal efficiency and N2O fluxes from the wetlands. Significant relationships between TP removal and N2O fluxes were found in the A. calamus wetland (p < 0.05) but not in the C. indica wetland and S. validus wetland. In this study, K1 was N2O fluxes/TN removal efficiency and K2 was N2O fluxes/NH4+-N removal efficiency. Lower values of K1 and K2 for a wetland mean that this system emits less N2O than other wetlands for per unit of TN and NH4+-N removed. The K1 and K2 of A. calamus were higher than C. indica, followed by S. validus (Fig. 4). All the values in three species had a significant difference (P < 0.05) (Tables S12 and S13).
2.5. Statistical analysis The statistical analysis was carried out using SPSS 21 and Origin 2015. Spearman correlation was used to analyze correlations between N2O fluxes and air temperature, nutrient removal efficiencies, and ROL for the wetland plants. The term flux is used for both positive and negative gas exchanges. Positive fluxes represent gas emission, while negative fluxes are used for consumption. When p < 0.05, correlations and difference were considered statistically significant and p < 0.01 was defined as highly significant. One-way ANOVE followed by LSD was conducted to test the difference of different species parameters. The N2O fluxes between down-flow chamber and up-flow chamber were analyzed by independent sample t-test. Pearson correlation was conducted between ROL and nitrogen removal. 3. Results 3.1. Changes N2O fluxes from IVCW The variation of N2O emission from IVCW systems during the experimental period is illustrated in Fig. 2. The N2O fluxes from A. calamus wetland, C. indica wetland and S. validus wetland ranged from 0.05 ± 0.01 to 1.80 ± 0.34, 0.08 ± 0.00 to 0.62 ± 0.20, and 0.03 ± 0.00 to 0.27 ± 0.01 mg N2O-N/m2/h, respectively. N2O fluxes from the three plant wetlands varied seasonally. The N2O fluxes were higher in summer than in spring and fall, and there had lowest N2O fluxes in winter. In the A. calamus and S. validus wetland, The N2O fluxes in summer had a significant different with those in winter (P < 0.05) (Tables S1 and S2). In the C. indica wetland, the N2O fluxes in summer had a significant different with those in Autumn, Spring, and Winter (P < 0.05) (Table S3). Significant differences in N2O fluxes were found among different CWs with various plant species in this study. The A. calamus wetland emitted much higher N2O than the C. indica wetland (P < 0.05), and the S. validus wetland has the lowest emissions. N2O fluxes of the A. 3
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Fig. 2. The monthly average N2O fluxes from three planted wetlands and the relationships with air temperature.
between 0 ± 0.02 and 1.54 ± 0.24 μmol O2/h/plant. The average ROL was 2.13 μmol O2/h/plant for C. indica, 1.84 μmol O2/h/plant for A. calamus, followed by 0.66 μmol O2/h/plant for S. validus. The average ROL of C. indica and A. calamus were much higher than the average ROL of S. validus (P < 0.05) (Table S14). The present study analyzed the ROL of three wetland plants and the N2O fluxes from the wetlands. The results indicated that ROL of wetland plants was positively correlated with N2O fluxes, and can be an indicator to predict N2O fluxes. Pearson correlation was conducted between ROL and TN removal, and NH4+-N removal. The results were shown as Tables S15, S16, and S17. ROL of three plants had a very significant correlation with TN removal, and NH4+-N removal (P < 0.01). TN removal also had a very significant correlation with NH4+-N removal (P < 0.01).
3.3. Radial oxygen loss ROL of the three wetland plants was affected greatly by seasonal conditions (Fig. 5). The highest ROL of the plants appeared in summer, followed by autumn, and then by spring, while lowest values were observed in winter. The ROL of A. calamus and S. validus in summer had a significant difference with ROL in Winter and Spring (P < 0.05) (Tables S1 and S2). The ROL of the C. indica in summer had a significant difference with ROL in Winter, Autumn and Spring (P < 0.05) (Table S3). During the measurement period from July of 2016 to May of 2017, ROL of A. calamus and C. indica ranged from 0.05 ± 0.11 to 3.13 ± 0.25 μmol O2/h/plant and 0.47 ± 0.14–5.04 ± 0.67 μmol O2/h/plant, respectively, whereas S. validus was relative steady
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Fig. 3. Nutrient removal efficiencies by three wetlands grown with different plant species (p < 0.05 means a significant correlation between nutrient removal efficiencies and N2O fluxes, p < 0.01 means an extremely significant correlation between nutrient removal efficiencies and N2O fluxes).
4. Discussion
which meant A. calamus's roots had large surface area for nitrification bacteria and denitrification bacteria inhabiting. In addition, large biomass was beneficial for plants transmit gas. Most of N2O producing by roots was transmitted into air through plants (Chang et al., 1998). It was reported that plants release N2O, and the foliage released the highest N2O compared with stem and root (Huang et al., 1992). It could be speculated that A. calamus with luxuriant foliage was beneficial to N2O release. The maximum value (1.8000 ± 0.34 mg N2O-N/m2/h from the down-flow cell of A. calamus wetland in August) measured in this study was higher than the value (0.03 mg N2O-N/m2/h) in a natural ecosystem reported by Saggar et al. (2007), and similar with the value measured in wastewater treatment CWs (1.37 mg N2O-N/m2/h) reported by Wu et al. (2009), but greatly lower than the value
The average N2O fluxes of the A. calamus wetland, C. indica wetland, and S. validus wetland were 0.52, 0.32 and 0.12 mg N2O-N/m2/h, respectively, which indicated that the three plant wetlands functioned as N2O sources during the whole monitoring period. A. calamus wetland reached the highest N2O fluxes (P < 0.05), while S. validus wetland got the lowest (P < 0.05). We concluded that N2O fluxes from constructed wetlands can be decreased significantly through proper selection of plant species. It was reported that stronger root system and higher under-ground biomass of wetland plants have higher removal of nitrogen and phosphorus (Anderson et al., 1994). A. calamus's root was strong and has high above-ground biomass and underground biomass,
Fig. 4. K1 and K2 of three wetlands grown with different plant species (K1: N2O fluxes/TN removal efficiency; K2: N2O fluxes/NH4+-N removal efficiency). 5
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Fig. 5. ROL of three wetland plants and the relationships with average N2O fluxes (ROL: radial oxygen loss).
(1272.73 mg N2O-N/m2/h) measured in a sewage treatment plant (Benckiser et al., 1996). Tian (2016) reported N2O fluxes from −0.01 to 0.20 mg N2O-N/m2/h in IVCWs, similar with the values recorded in this study. The N2O fluxes were higher in summer than in spring and fall, and there had lowest N2O fluxes in winter perhaps due to the plants withering and low microorganism activity in winter. The high temperature in summer led to abundant nitrifying bacteria and denitrifying bacteria, and could result in more N2O emission. Our results indicated that temperature had an important effect on the N2O emission in CWs, which is in agreement with other reports (Zhang et al., 2005). Significantly higher N2O fluxes during the summer season than during winter was found by Søvik et al. (2006). On the other hand, it is well recognized that temperature affects plant photosynthesis and plant biomass directly, and thus increases organic matter and gas transportation, which have positive effects on N2O fluxes (Zhao et al., 2016). High temperatures within certain range where the enzymes are stable and maintain high activity may contribute to biological process in the denitrification (Firestone, 1983). Therefore, it is possible to speculate on the N2O fluxes by measured air temperatures. The N2O fluxes from the down-flow cells were found to be higher than the fluxes from the up-flow cells due to more nutrients in the down-flow cells. The N2O fluxes in A. calamus wetland and S. validus wetland had significant difference between down-flow chamber and upflow chamber (P < 0.05). Johansson et al. (2010) and Mander et al. (2003) both reported that there were higher N2O emission rates at water inlets than those at the water outlets. More NO3− in the downflow cell, which are available for the denitrification process, may contribute to higher N2O emission rates compared to the up-flow cell (Wu, 2014). The removal efficiencies of TN and NH4+-N in the IVCW of this study were relatively low, which agrees with the study results of an approximately 30% removal efficiency using wetlands to reduce N from wastewater following the conventional secondary treatment (Andersen et al., 2003). However, the N removal efficiencies in this study were lower than those reported in studies of Andersen et al. (2003). The low efficiencies might have resulted from a higher hydraulic loading rate (330 mm/d) used in the present study as compared to theirs (18–100 mm/d). It was also reported that high hydraulic loading rates could result in low nutrient removal efficiencies (Karpuzcu and Stringfellow, 2012). It was probably that hydraulic loading rate resulted in anaerobic situation and it could affect nitrification that transformed NH4+-N to NO3−. The results in Tables S1, S2, and S3 showed that both of NH4+-N removal and TN removal efficiencies had significant difference between summer and winter (P < 0.05). The NH4+-N removal and TN removal efficiencies had a similar seasonal variation tendency: summer > autumn or spring > winter, which agreed well with other reported results (Bastviken et al., 2009; Spieles
and Mitsch, 1999). This significant seasonal variation of nitrogen removal efficiency could be primarily attributed to the annual growing cycle of the plants and the sensitiveness of nitrification and denitrification to environmental conditions particularly temperatures. TP removal efficiencies were primarily achieved through soil adsorption and plant uptake (Inamori et al., 2007). The TP removal efficiencies of the three planted wetlands were highest in the summer, which could be explained by the peak biomasses in the summer. Starting in September, plants began to lose leaves, and the accumulated phosphorus start to be released from the fallen leaves. A resultant sharp decrease in phosphorus removal efficiency was thus observed in the autumn and winter. The wetland plants started to absorb more phosphorus in the second spring due to the plant growth (Fig. 3). TOC removal had low correlation with seasons (P > 0.05), this may be because microorganisms rather than plants in the IVCWs largely contributed to the TOC removal (Reddy and D'Angelo, 1997). TOC removal was very high, and also had no significant difference with species (P > 0.05). Glucose in the waste water was easily consumed, with single organic composition. Higher N2O fluxes and NH4+-N and TN removal efficiencies were obtained in the A. calamus and C. indica wetlands compared to the S. validus wetland (Figs. 2 and 3), suggesting that A. calamus and C. indica wetlands had higher N removal efficiencies with potentially larger contribution to global warming. We assume that nitrification and denitrification were responsible for N2O production, with the highest rates in summer and the lowest in winter. N2O can be produced through nitrification (conversion of ammonia to nitrate) and denitrification (conversion of nitrate to N2) (Colliver and Stephenson, 2000). S. validus wetland had the lowest K1 and K2 values (P < 0.05). It proved that S. validus wetland had the lowest global warming potential in terms of N2O fluxes per unit of TN and NH4+-N removed. Hence, we can preferentially choose S. validus as a waste water treatment plant in the IVCW for removing TN and NH4+-N while minimizing N2O fluxes. Plants transfer oxygen to the root system through aerenchyma. The present results showed ROL of C. indica (average 2.13 μmol O2/h/plant) was higher than A. calamus (average 1.84 μmol O2/h/plant), followed by S. validus (average 0.66 μmol O2/h/plant). S. validus got the lowest ROL (P < 0.05). These variations were consistent with the highest aboveground and belowground biomass of C. indica, followed by A. calamus, and then by S. validus. Broad leaves were in favor of photosynthesis and absorbing oxygen in the atmosphere. Plants used aerenchyma to transmit oxygen to the root system, which informed ROL. It has been reported that there were significant differences in ROL among different plant species (Li et al., 2011). It was found that Phragmites australis had high value of ROL at 5.27 μmol O2/h/plant, followed by Typha orientalis Presl at 4.78 μmol O2/h/plant, and Arundo donax at 3.46 μmol O2/h/plant (Wang, 2015). A previous study showed ROL of Phragmites australis > Typha orientalis Presl > Scirpus validus Vahl 6
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Appendix A. Supplementary data
(Wu, 2014). Remarkable seasonal variation in ROL in IVCWs systems was observed, with summer > autumn > spring > winter. The high temperature and abundant light in summer favored plant growth and thus the highest value of ROL in a year. In autumn, decreasing air temperature and decreasing light resulted in ROL of plants gradually decreased. In winter, the low temperature (7 to 11 °C) and low light led to plant root system being in dormancy with almost zero ROL. In spring, plants were in growing period, and ROL of plants increased gradually. Previous studies showed that ROL reached maximum values in summer or autumn due to the highest photosynthetic rates and growth rates (Cheng et al., 2014). We found three species' ROL had a significant correlation with TN removal and NH4+-N removal (P < 0.01) (Tables S15, S16 and S17), this could be nitration needs oxygen, and ROL provided oxygen for nitration reaction. Up to now, little work has been done directly on the correlation between ROL and N2O fluxes from wetlands. We also found that ROL was positively correlated with N2O fluxes (p < 0.05), and ROL of wetland plants was one of the most important influencing factors of N2O fluxes, suggesting that the oxidizing capacity in anaerobic environment is important for N2O emissions. The complicated nitrogen cycle in wetlands is discussed in detail by Reed et al. (1988). Nitrification and denitrification are the major nitrogen removal processes. N2O production through denitrification was been identified as the significant pathway under aerobic conditions. The last step of denitrification, in term of the conversion of N2O to N2, was easily disrupted by oxygen and led to incomplete denitrification and N2O emission (Colliver and Stephenson, 2000). Higher ROL may increase more oxygen release to the surrounding water and reduce denitrification, which might resulted in the higher N2O/N2 ratios. Hence, ROL from wetland plants could be applied to predict N2O fluxes approximately (Fig. 5), according to the formulas. To adapt to the anaerobic environment with low redox potentials, wetland plants have developed an efficient strategy releasing oxygen from roots to oxidize the rhizosphere. The oxidizing capacity played an important role in surviving the anaerobic environment.
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5. Conclusions In this study, N2O fluxes from A. calamus, S. validus and C. indica wetlands, ranging from 0.05 ± 0.01 to 1.80 ± 0.34, 0.08 ± 0.00 to 0.62 ± 0.20, and 0.03 ± 0.00 to 0.27 ± 0.01 mg N2O-N/m2/h, respectively, and had a similar seasonal variations tendency: summer > autumn > spring > winter. The N2O fluxes from the down-flow cells were higher than those from the up-flow cells due to more nutrients in the down-flow cells. The S. validus wetland was more efficient in mitigating N2O fluxes and removing TN and NH4+-N. N2O fluxes had significant correlation with NH4+-N and TN removal efficiencies and ROL of the three wetland plants. On the whole, these results provided insight in seasons, temperatures, the plant species and ROL in relation to the N2O fluxes from IVCWs systems and can be utilized in future efforts to reduce N2O fluxes.
Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments This work is financially supported by the National Natural Science Foundation of China (No. 51308127). 7
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