Effect of Scirpus mariqueter on nitrous oxide emissions from a subtropical monsoon estuarine wetland


  • Zhongjie Yu,

    1. School of Resources and Environment Science, East China Normal University, Shanghai, China
    2. Department of Earth and Environmental Sciences, Rutgers, State University of New Jersey, Newark, New Jersey, USA
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  • Yangjie Li,

    1. School of Resources and Environment Science, East China Normal University, Shanghai, China
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  • Huanguang Deng,

    1. School of Resources and Environment Science, East China Normal University, Shanghai, China
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  • Dongqi Wang,

    Corresponding author
    1. School of Resources and Environment Science, East China Normal University, Shanghai, China
    2. Department of Oceanography and Coastal Sciences, School of the Coast and Environment, Louisiana State University, Baton Rouge, Louisiana, USA
      Corresponding author: D. Wang, School of Resources and Environment Science, East China Normal University, Shanghai, 3663 North Zhongshan Rd., Shanghai, 200062, China. (dqwang@geo.ecnu.edu.cn)
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  • Zhenlou Chen,

    1. School of Resources and Environment Science, East China Normal University, Shanghai, China
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  • Shiyuan Xu

    1. School of Resources and Environment Science, East China Normal University, Shanghai, China
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Corresponding author: D. Wang, School of Resources and Environment Science, East China Normal University, Shanghai, 3663 North Zhongshan Rd., Shanghai, 200062, China. (dqwang@geo.ecnu.edu.cn)


[1] The effects of the wetland plant Scirpus mariqueter on nitrous oxide (N2O) emissions in Yangtze estuary, China, were investigated using an in situ static chamber technique. Field measurements spanned the entire growing season (May to October) and encompassed a wide range of weather conditions typical of the subtropical monsoon climate of this region. Simultaneous measurement of carbon dioxide (CO2) and anatomical measurements were conducted to experimentally determine the gas transport mechanisms of S. mariqueter on N2O flux. S. mariqueter had a significant effect on N2O flux. Based on the comparison of light-dark and clipped-unclipped gas flux, N2O flux was negatively correlated with NEE (p < 0.0001) and NPP (p < 0.001) under light conditions when S. mariqueter was present but positively with temperatures in the dark condition or when S. mariqueter was clipped. Besides the plant uptake corresponding to the N2O negative flux in light chamber, it is reasonable to assume that because of the limitation of nitrate in sediment, coupled nitrification-denitrification is the main process of N2O producing. O2 transported into the S. mariqueter rhizosphere during photosynthesis stimulated denitrifier also would consume the N2O and would be induced to the N2O diffusing from atmosphere into sediment. Although photosynthetic activity of S. mariqueter attenuated N2O flux significantly over the course of the entire study period, creating a net sink for atmospheric N2O under light condition, the marsh of Chongming Island Dongtan wetland was a net source of atmospheric N2O during the active S. mariqueter growth phase (averaged flux was 98.3 μg N2O m−2 h−1).

1. Introduction

[2] Wetlands receiving increased nitrogen loading are considered as net source of N2O [Moseman-Valtierra et al., 2011]. Previous studies showed that uncertainties in the estimate of wetland greenhouse gas fluxes is partially owing to the spatial and temporal variability of measured rates within and across wetland types [e.g., Kammann et al., 1998; Bergström et al., 2007]. Many wetland plants develop an extensive system of internal gas spaces or lacunae to adapt to waterlogged conditions [Schuette et al., 1994], by supporting aerobic soil microbial processes and gas exchange [Jackson and Armstrong, 1999]. It has been confirmed by numerous studies that wetland plants can play an important role on CH4 transport, oxidation and production by serving as a conduit in facilitating the CH4 flux [Van der Nat et al., 1998], releasing O2 into rhizophere through radial oxygen loss [Armstrong and Armstrong, 1990] and providing substrates for methanogenesis as labile carbon in root exudates [Joabsson et al., 1999].

[3] Whereas numerous studies have been conducted to investigate the effects of plants on CH4 emission from wetland ecosystems, similar studies of N2O emission have not been widely or systematically conducted [Chen et al., 1997; Rusch and Rennenberg, 1998; Pihlatie et al., 2005]. In wetland environments, the flux of N2O from soil/sediment to the atmosphere is the net result of N2O production, further reduction to N2, and transport interception [Chen et al., 1997]. Some wetland plants, such as rice (Oryza sativa L.) [Mosier et al., 1990], Pontederia cordata L., and Juncus effusus L. [Reddy et al., 1989], functioned as conduits for N2O transport. The efflux of O2 from plant roots may promote nitrification of NH4+, with the NO3 formed serving as substrate for denitrification [Bodelier et al., 1996], and at the same time more N2O would be produced in promoted nitrification [Wrage et al., 2001]. Based on the treatments of elevated CO2 concentration and nitrogen fertilization, Kettunen et al. [2005] reported the potential of Phleum pratense to increase the N2O production via easily decomposable root exudates [Kettunen et al., 2005]. However, only a few long-term studies have been conducted on the dynamics of plant-dependent N2O flux under field conditions, many of the controlling factors have not been identified, including the relationship between N2O emission and plant productivity.

[4] Scirpus mariqueter, an endemic species in the subtropical monsoon estuarine and coastal zone of China, is a long-lived rhizomatous, corm-forming herb growing predominantly in intertidal marshes (mudflats) of the Yangtze estuary [Sun et al., 2001]. The role of S. mariqueter in the regulation of N2O fluxes, which it is important for determining the function of wetlands as sources and sinks of N2O in this area, has not been determined. Our objective for the study was to investigate how S. mariqueter affects the variability and magnitude of N2O fluxes from the Yangtze estuarine wetland and to explore the relationship between the N2O fluxes and plant productivity (or the photosynthetic activity). This was accomplished through examination of S. mariqueter structural features combined with measurement of N2O fluxes in dark and light enclosures in clipped or unclipped vegetation plots. Our approach was designed to provide a comprehensive means for determining the mechanism of gas transport through S. mariqueter and the relationship between plant productivity and N2O fluxes.

2. Methods and Materials

2.1. Physical Setting of Study Area

[5] The Yangtze estuary is located in a typical subtropical monsoon area characterized by four distinct seasons (spring, summer, autumn and winter). Because of the abundant sediment supply from the Yangtze River [Chen and Zhong, 1998], the delta front continues to extend seaward rapidly. Dongtan wetland of Chongming Island (CD) is the largest and most completely developed wetland in the Yangtze estuary, which has about 100 km2 of tidelands (as shown in Figure 1), composed of natural high, middle, and low tidal flats. S. mariqueter is the dominant native plant in middle tidal flat (marsh). Sampling location, the marsh, is not submerged during the neap tide and submerged for several hours during the spring tide [Wang et al., 2009]. The growing season for S. mariqueter generally occurs from late April through early November with the most active growth occurring during the summer months. All the aboveground shoots die off at the end of the growing season, whereas underground parts (i.e., corm and rhizome) persist for several years [Sun et al., 2001].

Figure 1.

Map of sampling site.

2.2. Experimental Design and Gas Fluxes

[6] Nonsteady state chamber composed by two parts, base and cover chamber was used to investigated N2O fluxes and the effects of S. mariqueter. The base is 5 cm height and 30 cm diameter and has a 3 cm height and 1.5 cm width U shape groove, is made from 1 mm stainless steel plat. Because of the tide cycling, if the base is previously installed in the marsh, there will be much particles settling down in the base. So we sharpened the blade of the end of base, making it could cut into the sediment with little disturbance. Two kind Cover chambers (50 cm net height × 30 cm ID), dark (opaque) and light (transparent), made from 0.4 mm thickness iron sheet and 3 mm thickness Perspex cylinder were adopted. Dark chamber was covered by an insulating layer and aluminum foil to insulate and reduce heat transmission and reflect light. Sampling port with three way valve, electric fan, thermometer, and pressure port were installed on every chamber. All the connections were made “air tight” and sealed using silicon rubber. During sampling, the bases were installed on the sediment surface about 15 to 1/2 h before sampling, and then chambers were fixed on the base and sealed by water in the U shape groove.

[7] Gas flux samples were collected under both light and dark chambers within the S. mariqueterdominated zone, monthly from May to October 2004. In May, samples were collected one time in the morning, and four times in June at the morning and afternoon. From June to September, we took eight time measurement of flux from dawn to dusk every 1 1/2 h. Immediately after installing each chamber and again after 30 min, a 180 ml gas sample was drawn using a syringe with a three-way airtight valve, which was injected into a gas sampling bag, (A plastic bag plated with Aluminum inside, which is inert to the air and has a screw vent port with septum. Air sample could be injected into bag by syringe.). The clipping procedure was conducted monthly from July to October at the study site.S. mariqueter plants within six 40 × 40 cm plots were carefully cut and removed, leaving about 1 cm stubble, without disturbing the surface sediment. The sampling procedure was detailed by Wang et al. [2009].

[8] Gaseous flux (F) was calculated as the concentration change of the gases in chamber during sampling time (μg N2O m−2 h−1 or mg CO2 m−2 h−1).By comparing N2O fluxes in chambers under light versus dark conditions, the variability in flux resulting from plant respiration and gross photosynthetic activity was assessed. Comparing N2O fluxes in chambers with and without the presence of aboveground vegetation allowed us to weigh the contribution of S. mariqueteron gas transfer from the soil-plant system. Net ecosystem exchange (NEE) was equivalent to the inverse of CO2 flux in light unclipped conditions. Positive values of NEE indicated net fixation of atmospheric CO2 by S. mariqueter community. Net primary production (NPP) in light chambers, defined as the difference between gross primary production and autotrophic respiration [Lovett et al., 2006], was calculated by subtracting the dark clipped CO2 flux (respiration of sediment and microbial) from the light unclipped CO2 flux (NEE).Gas samples were analyzed by gas chromatography (HP5890II) equipped with ECD [Wang et al., 2009]. Analysis was performed within 3 days of sampling.

2.3. Vegetation and Environmental Parameters

[9] Vegetation samples were collected during each sampling events from seven 50 × 50 cm randomly placed quadrats at 3–5 m spacing. In each quadrat, the aboveground portion of S. mariqueter was cut, and the height and stem density of the vegetation was recorded. Biomass and environmental parameters, including the Air temperature, ground temperature, photosynthetically active radiation, the density and height of S. mariqueter community, and organic carbon content and median grain size of sediment were measured and presented by Wang et al. [2009, Table 1].

2.4. Anatomical Studies

[10] For anatomical characterization of S. mariqueter, transverse and longitudinal sections of corms, stems, and leaves were dissected by hand using fresh material. The sample pieces were dehumidified in a mixture of 3% glutaraldehyde, 1.5% acrolein and 1.5% paraformaldehyde in phosphate buffer (pH 6.8), dehydrated in acetone and then dried in a critical point dryer. They were examined by scanning electron microscopy.

2.5. Data Analysis

[11] N2O flux from each treatment was calculated by averaging the three replicates for each sampling time. The data of environmental parameter used in correlation analysis and regression analysis with N2O fluxes are in Table 1 of Wang et al. [2009], the simultaneous research focusing on methane emission.

3. Results

3.1. Anatomical Characterization of S. Mariqueter

[12] By using scanning electron microscopy, intercellular gas spaces were observed in all vegetative parts of S. mariqueter (see Figure 2). In the transverse section of the corm, intercellular gas spaces were found to be well developed in the proportionally large cortex and central cylinder, with hexagonal packing arrangements. Stellate parenchyma surrounding the central cylinder showed high porosity, with no aerenchyma. In the transverse section of the aerial stem, large aerenchyma was visible, embedded regularly in the outer cortex, while the complete inner cortex was formed by cortical gas spaces. In the leaves, lysigenous-like aerenchyma were observed in the cortex parenchyma. The structure was narrow, symmetrically arranged and not as extensive as those in the stem. In addition, stomata were located primarily on the longitudinal section of leaf epidermis.

Figure 2.

Transverse and longitudinal section of vegetative organs of S. mariqueter observed by scanning electron microscopy. (a) Corm, (b) stem, (c) leaf, (d) aerenchymas in stem, (e) and leaf surface showing stomatas arranged in row. Legend: ae, aerenchyma; cc, central cylinder; cp, cortex parenchyma; en, endoderm; ex, exodermis; sp, stellate parenchyma; vb, vascular bundle.

3.2. Seasonal Variation of Nitrous Oxide Fluxes

[13] N2O concentration in the headspace of chamber is ambient, about from 300 to 360 ppbv. During the study period, monthly averaged N2O flux under light conditions ranged from −76.3 ± 57.4 μg N2O m−2 h−1 to 36.5 ± 65.4 μg N2O m−2 h−1. Except for in June, CD was a sink for atmospheric N2O with a maximum absorption flux of −76.3 ± 57.4 μg N2O m−2 h−1 measured in August (Table 1). There was no significant correlation between temperatures and N2O flux in the light enclosures. However, PAR was significantly correlated with light N2O flux (p < 0.01), indicating that the photosynthetic activity of S. mariqueter, which was closely correlated with PAR, apparently affected the seasonal variation of N2O flux. During June, CD became a source of atmospheric N2O, corresponding to low PAR levels measured during that month. Overall, monthly N2O absorption (negative flux) rate increased along with the growth of S. mariqueter, and decreased when plants senesced. On a monthly basis, the differences in N2O flux between light and dark chambers were significant (p < 0.05 in May and June, p < 0.001 in July, August, September, and October). In contrast to the N2O fluxes under light conditions, N2O flux in the dark chambers was a source of atmospheric N2O during the whole growing season, highlighting the relationship between photosynthetic activity of S. mariqueter and inhibition of N2O flux. Furthermore, significant positive correlations were found between N2O flux and temperatures (AT and SGT, p < 0.01) in dark chambers.

Table 1. Seasonal Variation in N2O Flux (μg N2O m−2 h−1) in Clipped and Nonclipped Treatments (μg N2O m−2 h−1)a
 LightDarkLight (Clipped)Dark (Clipped)
  • a

    Values are means and standard deviation of sequential measurements performed during monthly sampling events. Standard deviation represents variation during each sampling.

May−67.4 ± 14.6730 ± 19.2--
Jun.36.5 ± 65.4107 ± 50.0--
Jul.−42.6 ± 52.0246 ± 36.880.9 ± 68.2110 ± 69.3
Aug.−76.3 ± 57.4152 ± 25.1130 ± 41.6129 ± 18.6
Sep.−75.1 ± 65.9139 ± 23.1135 ± 41.6125 ± 30.1
Oct.−16.2 ± 24.447.2 ± 2.3535.8 ± 9.7643.1 ± 9.33

3.4. Nitrous Oxide Fluxes of Clipping Treatment

[14] Compared with N2O fluxes in unclipped light chambers, cutting the aboveground part of S. mariqueter under light conditions enhanced N2O emission in all months (p < 0.001). Cutting the aboveground part of S. mariqueter in the dark chambers significantly attenuated the N2O fluxes in July (p < 0.001) and August (p < 0.05). However, substantial attenuation of N2O flux occurred only in July, when flux decreased by about 55% in the clipped dark chambers compared to the nonclipped dark chambers. N2O flux in both light and dark clipped chambers exhibited a similar temperature-induced diurnal pattern during the four month period, with peak emission observed during late afternoon when the 10 cm GT were usually highest (seeFigure 3).

Figure 3.

Diurnal change of N2O fluxes in light and dark chambers in the unclipped and clipped treatments. Bars represent standard deviation of the triple duplicates.

3.5. Nitrous Oxide Flux at Wetlands

[15] N2O emission from wetland research was token on at many kinds of typical wetland around the world (see Figure 4). Reported data show that N2O flux at wetland has a large range from negative value to positive (from about −32.4 to 1292 μg N2O m−2 h−1), while wetland is the source of the atmosphere on the whole (see Table 2). In our research, although in light chamber marsh was a sink of atmospheric N2O, the S. mariqueter marsh was a net source of atmospheric N2O, with an average N2O emission rate of 98.3 μg N2O m−2 h−1 during the principal growing season from May to October. It is interesting that N2O flux in Arctic and Antarctic area is higher. The budget of global N2O emission from wetland need a detail spatial data, and the data also need to be considered the effect of radiation.

Figure 4.

Map of N2O fluxes research locations of the world.

Table 2. N2O Emission Flux at Some Typical Areas Around the Worlda
NumberLocation characterFlux (μg N2O m−2 h−1)Reference
  • a

    The data were converted with same unit according the data in every research.

1Subarctic tundra79.2–1292[Repo et al., 2009]
2Peatland−1.25–8.33[Regina et al., 1996]
3Intertidal mud flat1.79[Middelburg et al., 1995]
4Intertidal saltmarsh and mudflats14[Kenny et al., 2004]
5Intertidal saltmarsh and mudflats11.5[Kenny et al., 2004]
6Coastal mash35.5[Schiller and Hastie, 1994]
 Coastal fen121.0 
7Riparian Forest11.2 ± 1.77[Ullah and Moore, 2011]
 Wetland17.8 ±3.01–48.3 ±18.6 
8Intertidal salt marsh−1.33 ±0.88[Moseman-Valtierra et al., 2011]
9Salt marsh5.56[Smith et al., 1983]
 Brackish marsh8.61 
 Fresh marsh9.87 
10Mangrove3.36–218[Corredor et al., 1999]
11Freshwater marsh65 ± 37[Zhang et al., 2007]
12Mangrove17.1–33.3[Krithika et al., 2008]
13Subtropical mangrove−2–14[Kreuzwieser et al., 2003]
14Subtropical mangrove−4–65[Allen et al., 2007]
15Temperate mangrove and salt marsh15.7[Livesley and Andrusiak, 2012]
16Antarctic tundra−32.4–135[Zhu et al., 2008]
17Antarctic tundra0.6 ± 1.7–1.1 ± 2.2[Zhu et al., 2005]
18Antarctic lakeshore soils52.5–132[Gregoricha et al., 2006]
19Subtropical intertidal salt marsh98.3This study

4. Discussion

4.1. Gas Transport Mechanism in S. Mariqueter

[16] Researchers had demonstrated that mechanisms of gas transport commonly employed by wetland plants include molecular diffusion, characterized by migration of gas molecules along a concentration gradient, and convective flow in response to a pressure differential [Armstrong et al., 1992; Brix et al., 1992]. Previous studies have demonstrated significant differences in plant-mediated CH4 fluxes under dark versus light conditions [Whiting and Chanton, 1996; Van der Nat and Middelburg, 2000], when wetland plants were the primary conduits facilating CH4emission via convective throughflow and stomata-controlled transport [Van der Nat and Middelburg, 1998]. Significantly attenuated CH4 emission rates have been observed when aboveground portions of the vegetation were clipped under light conditions, because the capacity for pressurized transport was eliminated [Van der Nat and Middelburg, 2000]. However, there can be significant increase in CH4 flux under dark conditions when the stem or the leaf is cut, if diffusion is the primary transport mechanism in the wetland plant, and especially diffusion had been limited by the resistance of the aboveground portion of the plant [Schimel, 1995].

[17] Although many studies focused on CH4 transport by wetland plants, the effects of plant on N2O emission have not been extensively studied, both of these gases, are soluble in water, so they can be transported concurrently within wetland plants by convective throughflow or diffusion. Some studies have reported that wetland plants can affect N2O fluxes by acting as a transport conduit [Reddy et al., 1989; Mosier et al., 1990], influencing nitrification-denitrification processes in the rhizosphere [Reddy et al.,1989; Bodelier et al., 1996; Kettunen et al., 2005], and/or producing N2O by photosassimilation of NO2 in the leaves [Smart and Bloom, 2001].

[18] Same as many other wetland plants, S. mariqueter possesses abundant intercellular gas space in the stem and leaf tissues (see Figures 2b–2d), indicating that convective throughflow is likely, particularly when an intensive pressure differential exists. In the previous research on CH4 emission, when the transpiration was higher, molecular diffusion and convective gas flow were the two main mechanisms of CH4 transport in S. mariqueter plants [Wang et al., 2009]. In July, when S. mariqueter was exuberant and PAR and temperature were relatively high, higher gas transport efficiency via convective throughflow was expected. Cutting the aboveground portion of S. mariqueter significantly decreased the CH4 fluxes in light chambers [Wang et al., 2009], because the capacity for pressurized transport has been eliminated [Van der Nat and Middelburg, 2000]. But in light chambers, clipping the aboveground portion of S. mariqueter significantly enhanced N2O flux compared with the unclipped chambers (p < 0.001) (see Figure 3), there was no observable of the transportation of N2O by convective throughflow. On the other hand, N2O fluxes in the unclipped dark were also significantly higher than those in light chambers (p < 0.001), suggesting that S. mariqueter photosynthetic activity significantly decreased the N2O emission.

[19] A microscopic anatomical evaluation of S. mariqueter revealed that cortical gas spaces occupied the full cortex (see Figure 2a), suggesting low resistance on transporting gas from root to stem and leaf. Such a configuration generally has little effect on gas diffusion [Schuette et al., 1994; Sorrell et al., 1997], although the potential diffusion resistance at the transition between the rhizosphere and the root aerenchyma was unknown. Based on the previous research in which molecular diffusion became the primary transport mechanism when S. mariqueter began to senesce, clipping the aboveground portion of S. mariqueter enhanced CH4 emission indicating the resistance of stems and leaves [Wang et al., 2009], suggesting that aboveground portion of vegetation was a factor regulating CH4 diffusion [Schimel, 1995]. While cutting of the aboveground portion of S. mariqueter significantly decreased the N2O flux in dark chamber (p < 0.001) especially in July and August, It was clear that gas transport by S. mariqueter was not the primary factor governing N2O emission in wetland. Therefore, the S. mariqueter transport function was to a degree influenced by its other physiological activities, such as production of root exudates and oxygenation of the rhizosphere.

4.2. Effect of S. mariqueter on Nitrous Oxide Fluxes

[20] Compared to CH4, there is not a large amount of research on plant-dependent N2O flux from wetland ecosystems, including information on the relationship between N2O flux and plant productivity. In the study of nitrogen loading in a freshwater marsh from Sanjiang plain, North China, Zhang et al. [2007] proposed that Deyeuxia angustifolia had the potential to increase the production of N2O by supplying easily decomposable root exudates, which enhance microbial activity in soil. Based on a significant correlation between N2O flux and aboveground biomass, they inferred that a large fraction of N2O flux was facilitated by Deyeuxia angustifolia via the transpiration stream [Zhang et al., 2007]. However, in other studies, there was no correlation between plant characteristics and N2O flux [Chen et al., 1997; Müller, 2003]. Yan et al. [2000] further concluded that N2O is mainly transported by diffusion through the soil surface rather than through plants [Yan et al., 2000].

[21] In our study, the effect of S. mariqueter on N2O flux was relatively distinct and straightforward. By comparing N2O flux in light and dark chambers, we conclude that the photosynthetic activity of S. mariqueter attenuated N2O flux significantly during the entire study period (see Table 1 and Figure 3). With the exception of June, monthly averaged N2O absorption rate varied with the growth of S. mariqueter. Significant positive correlations were found between N2O emission in dark chambers and temperature; conversely, there was a significant negative correlation between N2O flux and PAR under light conditions (p < 0.01). Furthermore, clipping the aboveground part of S. mariqueter in light chambers greatly enhanced N2O emission during each monthly measurements. On the other hand, there was no significant difference in N2O flux between clipped and unclipped dark chambers. We interpret these results as follows: PAR governed the photosynthetic rate and growth of S. mariqueter; consequently, a significant inhibitory effect on N2O emission was imposed by the S. mariqueter community. Scatterplots of diurnal N2O flux in light unclipped chambers versus NEE and NPP show the significant negative correlation between N2O flux and NEE and NPP (see Figure 5), the regression curve of N2O fluxes and NEE, NPP was described by the linear function: N2O flux (μg N2O m−2 h−1) = −0.2790 × NEE (mg CO2 m−2 h−1) − 2.0345 (R2 = 0.7758, p < 0.0001), N2O flux (μg N2O m−2 h−1) = −0.1224 × NPP (mg CO2 m−2 h−1) + 24.546 (R2 = 0.4211, p < 0.001).

Figure 5.

Diurnal gas fluxes in light chamber in unclipped treatments, plotted against net ecosystem exchange (NEE) and net primary production (NPP). Bars represent standard deviation of the triple duplicates.

[22] N2O production in freshwater marshes was clearly limited by nitrogen deficiency [Zhang et al., 2007]. Under field conditions, concentrations of inorganic nitrogen compounds are usually low in the root zone in the growing season due to plant uptake of nitrogen [Bodelier et al., 1996; Van der Nat et al., 1997]. The growth of S. mariqueter might suppress N2O emission by taking up nitrogen in sediment, which could directly inhibit the N2O production by diminishing the substrate for nitrification and denitrification. When denitrifiers and nitrifiers in the sediment were suffering the NO3 limitation, they would consume the N2O diffusing from the atmosphere [Frasier et al., 2010]. Although this process is poorly understood, some researches found that N2O was consumed by the soil [Chapuis-Lardy et al., 2007; Peichle et al., 2010; Ullah and Moore, 2011].On the other hand, Zhang et al. [2007] assumed that plant uptake can reduce some N2O, most likely by taking up available nitrogen. Furthermore, our explanation is also in agreement observations on Spartina alterniflora and Phragmites australis reported by Cheng et al. [2007] in experimental mesocosms using plants and soils from the Jiuduansha salt marsh in the Yangtze River estuary.

[23] Beside the competition between S. mariqueter and microbes for nitrogen, O2 is transported and diffused into S. mariqueterrhizosphere during photosynthesis. It effectively increases the aerobic-anaerobic surface area and influences anaerobic metabolism in the wetland soil [Megonigal et al., 2004]. In another research report [Wang et al., 2009], CH4 flux in light chamber was higher than in dark chamber from July to September, but there were no significant difference in July and August, and in October, CH4 flux in light chamber was slightly lower than in dark chamber. Photosynthesis of the plant or the O2 transported into sediment did not inhibit methanogenesis process greatly because more organic materials would also be transported into root and exuded [Zhang et al., 2007]. Denitrification is often tightly coupled to nitrification in the high redox area [Kettunen et al., 2005] that predominates in the rhizosphere, while methanogenesis dominates at lower reducer environment only when other electron acceptors are almost exhausted. Basing on this spatial distribution, it is reasonable to assume that the denitrification is more sensitive to the rhizospheric O2 delivery.

[24] In sediment, because of nitrate limitation coupled nitrification-denitrification was the main process of N2O production [Moseman-Valtierra et al., 2011]. LaMontagne et al. [2003] found that there was a higher N2O uptake rates in the opaque chamber deployed on macroalgae covered sediments, and benthic N2O sink can be explained by a close coupling of nitrification and denitrification [LaMontagne et al., 2003]. When coupled nitrification provides the nitrate for denitrifier, N2O uptake can occur [van Raaphorst et al., 1992], denitrifiers would consume N2O during hypoxic conditions [Usui et al., 2001]. When S. mariqueter photosynthesized under light conditions, more O2 was released from the root to sediment meeting the demand of nitrification, stimulated denitrifier consumed the N2O inducing to it diffusing from atmosphere into sediment. While in the dark chambers, although denitrification process would be slowed down because of the nitrate limitation, the consumption was decreased quickly and there was a net N2O production from denitrification. On the other hand, the stimulation of CH4 production by root exudates of S. mariqueter [Wang et al., 2009] indicates that the root exudates should also fuel the denitrifiers resulting in greater denitrification rate [Zhang et al., 2007] and more N2O consumption.

[25] From July to October, under light conditions, besides the diffusing into marsh sediment directly, N2O could diffuse with O2 from the stomata to the rhizosphere when S. mariqueter photosynthesized and the stomata were open, where it was consumed by coupled nitrify denitrification [Vieten et al., 2008; Moseman-Valtierra et al., 2011]. Under dark conditions, molecular diffusion was not the main transporting mechanism of N2O emission. Clipping the aboveground portion of S. mariqueter had no obviously effect N2O flux, facilitating N2O diffusing from rhizosphere to atmosphere. In July, the flux in clipped light and dark chambers was significantly lower than in unclipped dark chambers (p < 0.001, Figure 3), indicating that the positive effect of respiration of S. mariqueter on N2O emission exceeding the negative effect by the resistance of leaf and stem on N2O diffusion. But there was no significant difference between flux in unclipped dark chambers and clipped light and dark chambers from August to October (Figure 3). N2O diffusing out or into by molecular diffusion method through intercellular gas space was depended on its gradient between rhizosphere and atmosphere. The transport of N2O by S. mariqueter is not only simple molecular diffusion but the result associated with the complex effects of nitrogen cycling in rhizosphere. More detailed studies on N2O transport and its production and consumption in the rhizosphere via nitrification and denitrification process are needed in order to fully understand such effects.

5. Conclusion

[26] Wetland plant has not only the physical effect on N2O transporting and diffusing by facilitating it emission from sediment to atmosphere or providing a pass way which N2O diffuse into rhizosphere with O2 when there is a concentration gradient because of N2O consumption in sediment, it also control N2O production and consumption by influencing the biogeochemical processes in sediment. Under light condition, competition with the microbe for nitrogen and directly using of N2O, and providing O2 and decomposable organic carbon for nitrifiers and denitrifier are the two main mechanisms inducing the N2O absorption. While in the dark chamber, the higher N2O emission flux indicated that Yangtze estuarine wetland is a net source of atmospheric N2O; it is must to carefully consider the temporal and spatial change of N2O flux in calculating N2O budget in an area.


[27] We thank the anonymous reviewers and associate editor who aided in the development and improvement of this paper. We also would like to thank William DeBusk for his helpful comments and editorial corrections and Lei Wang for his help in world map drawing. This work was jointly supported by the National Natural Science Foundation of China (grants 40903049 and 40971259), the Ministry of Environmental Protection of China and Ministry of Housing and Urban-Rural Development of China (grant 2009ZX07317-006), the Ministry of Science and Technology of China (grant 2010BAK69B15), the Science and Technology Department of Shanghai (grants 10JC1404300 and 10dz1200602), and the Fundamental Research Funds for the Central Universities.