Variations in Temperature Sensitivity (Q10) of CH4 Emission from a Subtropical Estuarine Marsh in Southeast China

Chun Wang; Derrick Y. F. Lai; Chuan Tong; Weiqi Wang; Jiafang Huang; Chongsheng Zeng

doi:10.1371/journal.pone.0125227

Abstract

Understanding the functional relationship between greenhouse gas fluxes and environmental variables is crucial for predicting the impacts of wetlands on future climate change in response to various perturbations. We examined the relationships between methane (CH₄) emission and temperature in two marsh stands dominated by the Phragmites australis and Cyperus malaccensis, respectively, in a subtropical estuarine wetland in southeast China based on three years of measurement data (2007–2009). We found that the Q₁₀ coefficient of CH₄ emission to soil temperature (Q_s10) from the two marsh stands varied slightly over the three years (P > 0.05), with a mean value of 3.38 ± 0.46 and 3.89 ± 0.41 for the P. australis and C. malaccensis stands, respectively. On the other hand, the three-year mean Q_a10 values (Q₁₀ coefficients of CH₄ emission to air temperature) were 3.39 ± 0.59 and 4.68 ± 1.10 for the P. australis and C. malaccensis stands, respectively, with a significantly higher Q_a10 value for the C. malaccensis stand in 2008 (P < 0.05). The seasonal variations of Q₁₀ (Q_s10 and Q_a10) differed among years, with generally higher values in the cold months than those in the warm months in 2007 and 2009. We found that the Q_s10 values of both stands were negatively correlated with soil conductivity, but did not obtain any conclusive results about the difference in Q₁₀ of CH₄ emission between the two tidal stages (before flooding and after ebbing). There were no significant differences in both Q_s10 and Q_a10 values of CH₄ emission between the P. australis stand and the C. malaccensis stands (P > 0.05). Our results show that the Q₁₀ values of CH₄ emission in this estuarine marsh are highly variable across space and time. Given that the overall CH₄ flux is governed by a suite of environmental factors, the Q₁₀ values derived from field measurements should only be considered as a semi-empirical parameter for simulating CH₄ emissions.

Citation: Wang C, Lai DYF, Tong C, Wang W, Huang J, Zeng C (2015) Variations in Temperature Sensitivity (Q₁₀) of CH₄ Emission from a Subtropical Estuarine Marsh in Southeast China. PLoS ONE 10(5): e0125227. https://doi.org/10.1371/journal.pone.0125227

Academic Editor: Xuhui Zhou, Fudan University, CHINA

Received: August 30, 2014; Accepted: March 23, 2015; Published: May 28, 2015

Copyright: © 2015 Wang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

Data Availability: All relevant data are within the paper.

Funding: This work was financially supported by the National Science Foundation of China (Grant No: 40671174 and 41071148), the Program for Innovative Research Team in Fujian Normal University IRTL1205), Research Grants Council of the Hong Kong Special Administrative Region, China (CUHK458913), and The Chinese University of Hong Kong (SS12434). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Methane is a greenhouse gas that is 34 times more potent than carbon dioxide on a 100-year time scale and hence plays an important role in global climate change [1]. Natural wetlands in particular are the single largest global CH₄ source [2]. The global interannual variability of CH₄ emissions are primarily driven by fluctuations of CH₄ emissions from natural marshes, which on average emitted 177–284 Tg CH₄ yr^-1 during the period of 2000–2009 [1]. While numerous researchers have examined CH₄ dynamics in northern peatlands [3–7], relatively little has been done in the coastal and estuarine wetland ecosystems [8–10]. It is essential to develop a thorough understanding of the relationships between various environmental factors and CH₄ emissions from estuarine wetlands in order to accurately predict the impacts of natural and anthropogenic perturbations on CH₄ release, as well develop appropriate management strategies to minimize the potential adverse climatic impacts of wetlands.

The net CH₄ emission from wetland soil is a reflection of the balance between CH₄ production, oxidation and transport. Temperature is in general a major factor governing wetland CH₄ emission to the atmosphere [6, 11, 12], although some researchers have reported a weak correlation between CH₄ emission and temperature [13, 14]. The Q₁₀ coefficient has been commonly used to describe the temperature response of various microbial-mediated processes by standardizing temperature-related differences in reaction rates to proportional changes per 10°C rise in temperature. It is also considered to be one of the most important parameters used to assess the apparent temperature sensitivity of both soil respiration and ecosystem respiration [15–19]. However, few studies thus far have reported on the Q₁₀ of wetland CH₄ emission [6, 20, 21].

As soil respiration is widely regarded to be related exponentially to temperature, an exponential function is often used to determine the Q₁₀ of soil and ecosystem respirations. A number of studies have shown that Q₁₀ of soil respiration is not constant during the year, and that Q₁₀ tends to decrease with increasing temperature in both forest [22, 23]and grassland ecosystems [24]. Yet, it is not known whether Q₁₀ of CH₄ emission from wetland ecosystems will exhibit a similar pattern. In estuarine wetlands, tidal flow is a unique and important physical process that can influence various biogeochemical processes. While CH₄ emission from a tidal marsh was found to vary among different tidal stages [25], there is hitherto a lack of studies that compare Q₁₀ of CH₄ emission in tidal marshes among different tidal stages and different years. It is believed that a better understanding of Q₁₀ variations for both carbon dioxide and CH₄ fluxes could significantly improve our knowledge on the carbon balance of coastal estuarine wetland ecosystems [26].

In this study, we measured CH₄ fluxes continuously over a 3-year period from two stands dominated by Phragmites australis and Cyperus malaccensis, respectively, in a tidal marsh in southeast China to address the following objectives: (1) to examine the relationship between CH₄ emission and temperature in the two marsh stands; (2) to determine the seasonal and interannual variability of Q₁₀ of CH₄ emission from this tidal marsh; (3) to investigate the influence of two tidal stages (before flooding and after ebbing) on the Q₁₀ value of CH₄ emission; and (4) to elucidate on the influence of different vegetation on the Q₁₀ value of CH₄ emission.

Materials and Methods

The study was conducted in a tidal marsh at the Shanyutan wetland (26°00′36″–26°03′42″N, 119°34′12″–119°40′40″E, Fig 1) in the Min River estuary of Fujian Province in southeast China, with a total area 3120 ha (Fig 1). The climate of this subtropical region is warm and wet, with a mean annual temperature of 19.6°C and a mean annual precipitation of approximately 1,350 mm. Semi-diurnal tides are typical in the coastal area [27]. The soil surface is submerged for about 7 h over a 24 h cycle. There is normally between 10 and 150 cm of water above the soil surface at high tide. At other times the soil surface is completely exposed to air.

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Fig 1. Location of the sampling sites.

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The study site was located in the midwest section of the Shanyutan wetland, with C. malaccensis and P.australis (Cav.) Trin as the dominant plant species. We randomly selected two monoculture marsh stands dominated by C. malaccensis and P.australis, respectively, with almost identical environmental conditions for flux measurements. The characteristics of the two stands are shown in Table 1. Vegetation and soil properties were determined in 2007. In three replicate quadrats (50 x 50 cm) of both the P. australis and C. malaccensis stands, the above-ground and belowground (0–60 cm depth) biomass were measured every two months, and every season, respectively. All biomass was oven-dried at 80°C to constant mass and weighed. Soil total organic carbon (TOC) content (0–50 cm depth) was measured via wet combustion of sediments in H₂SO₄/K₂Cr₂O₇ [27,28].

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Table 1. Vegetation and soil properties of the two marsh stands dominated by P. australis and C. malaccensis, respectively.

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The closed, static chamber technique [29] was used to measure CH₄ emission from the two stands during two tidal stages in which the soil surface was exposed (i.e. before flooding, BF; after ebbing, AE). The maximum height of C. malaccensis was approximately 1.5 m, and the height of P. australis ranged from 1.6 to 1.8 m. The chambers consisted of three parts: a stainless steel bottom collar (50 cm length × 50 cm width x 30 cm height) and two individual PVC chambers (50 cm length × 50 cm width), with the lower and upper sections being 120 cm and 50 cm tall, respectively, for the P. australis stand, and 100 cm and 50 cm tall, respectively, for the C. malaccensis stand. The bottom collar was inserted permanently into the marsh sediment, with 2 cm left protruding above the sediment surface, while the PVC chambers were then placed on top of the collar during flux measurement. PVC chambers are commonly used in measuring wetland CH₄ fluxes since they are opaque and can reduce overheating of the chamber headspace over the deployment period. However, a recent study suggested that the use of opaque chambers could lead to underestimation of CH4 fluxes from plants that transport gases actively through convection (e.g. Phragmites spp.) [30]. The top chamber was equipped with an electric fan to ensure a complete mixing of air inside the chamber headspace. Also, in the hot summer, the chamber top was covered by cotton quilts during flux measurements to keep the temperature inside within -0.8°C to 1.2°C of the ambient level. A wooden boardwalk was installed permanently throughout the three years of study to facilitate access to the measurement sites without causing significant disturbance during sampling.

Monthly CH₄ flux measurements were made from January 2007 to December 2009, with the exception of February in these three years (owing to the Chinese Lunar New Year). Three replicate chambers separated by about 5 m were deployed in each marsh stand for gas sampling. All samples were taken on the days between the spring and neap tides (i.e. the third or fourth day after the largest spring tide). On these dates, the sampling sites began to flood at 10:00 am (Beijing time) and the soil was exposed to air again after ebb tide at about 1:30 pm. Chambers were deployed at 9:00 am (one hour before the beginning of flooding), and at approximately 3:00 pm (1.5 h after the end of the ebb tide) to determine the CH₄ fluxes at two different tidal stages in a single day (before flooding, BF, and after ebbing, AE). To measure CH₄ fluxes, three gas samples inside the chamber headspace were collected at 30-min intervals by 100 ml polypropylene syringes equipped with a three-way stopcock.

On each sampling date, one set of environmental variables was measured for each plant stand. Soil temperature, pH and redox potential at a depth of 10 cm were measured using a Eh/pH/temperature meter (IQ Scientific Instruments, USA), while soil conductivity (mS·cm^-1) was measured using an electrical conductivity meter (2265FS, Spectrum Technologies Inc., USA). Air temperature (1.5 m above ground) was measured by a pocket weather meter (Kestrel-3500, USA).

Methane concentrations in the gas samples were determined using a gas chromatograph (Shimadzu GC-2010, Japan) equipped with a FID detector within 48 h after sampling. The column and detector temperatures were set at 60°C and 130°C, respectively, with nitrogen as the carrier gas at a flow rate of 20 ml min^-1. The gas chromatograph was calibrated with gas standards containing 1.01, 7.99, and 50.5 μl CH₄ l^-1, respectively, on a monthly basis (i.e. every time when gas samples were analyzed). CH₄ emission into the atmosphere was estimated by linear regression of the change in headspace CH₄ gas concentrations with time [6]. The fluxes were rejected and removed from the analysis when the R² value of the linear regression was smaller than 0.90 [31].

We calculated the Q₁₀ value of CH₄ emission based on the exponential function that was commonly used to determine Q₁₀ of soil and ecosystem respiration [24] as well as CH₄ flux [6, 21], which was given as follows: (1) where F is CH₄ efflux (mg m^-2 h^-1), t is the air temperature or soil temperature measured at 10 cm depth, and a and b are regression coefficients (b is also called the temperature reaction coefficient).

The Q₁₀ value was then calculated as: (2) where Q_s10 and Q_a10, are the Q₁₀ values based on soil and air temperatures, respectively.

The entire data set of each year was divided into two groups for analysis based on the timing of data collection, with one group in the warm months (warmer period between April to September) and the other in the cold months (colder period between January to March, and October to December). We determined the Q₁₀ values of CH₄ emission separately for these two groups of data. We also calculated the Q₁₀ values of CH₄ emission for the two different tidal stages.

All statistical analyses were performed using SPSS 16.0 software (SPSS Inc., Chicago, Illinois). The differences in vegetation, soil properties, and Q₁₀ between the two marsh sites dominated by P. australis and C. malaccensis were tested using the paired-sample T test. The relationships between Q_s10 values and other soil parameters were tested using the Pearson correlation analysis. We tested for any significance differences in Q₁₀ among different years and seasons from the two stands using one-way ANOVA with Tukey’s post-hoc test.

Results

Relationship Between CH₄ Flux and Temperature

Variations of soil and air temperature from the P. australis and C. malaccensis marshes during 2007 to 2009 are shown in Fig 2. In the three years of our study, annual mean CH₄ emissions from the P. australis stand ranged from 5.26 ± 0.67 to 6.41 ± 0.94 mg m^-2 h^-1, with minimum and maximum fluxes of 0.10 and 61.40 mg m^-2 h^-1, respectively. For the C. malaccensis stand, annual mean CH₄ emissions ranged from 0.84 ± 0.12 to 2.97 ± 0.65 mg m^-2 h^-1, with minimum and maximum fluxes of 0.01 and 27 mg m^-2 h^-1, respectively. The temporal variation of CH₄ fluxes from the P. australis stand and the C. malaccensis stand had been reported previously [27]. CH₄ emission from the P. australis stand was significantly higher than that of the C. malaccensis stand (P < 0.05, Fig 3). The relationship of CH₄ emissions with both soil temperatures at a depth of 10 cm and air temperature could be described significantly by the exponential function (P < 0.01, Fig 3). Except in 2009, the percentage variance in CH₄ emission explained by air or soil temperature was greater for the C. malaccensis stand compared to the P. australis counterpart (Fig 3).

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Fig 2. Monthly mean soil temperature (°C) at 10 cm depth or air temperature (°C) in the two marsh stands from 2007 to 2009.

Data of soil (air) temperature was missing in April 2007 due to instrument failure.

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Fig 3. Relationships between CH₄ emission (mg m^-2 h^-1) and soil temperature (°C) at 10 cm depth or air temperature (°C) in the two marsh stands from 2007 to 2009 as described by the exponential function (P < 0.05).

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Inter-annual Variations in Q₁₀ Values

The Q_s10 values of CH₄ emission from the two marsh stands showed little inter-annual variations in the three study years (P > 0.05, Fig 4). Annual mean Q_s10 values of CH₄ emission from P. australis stand were 3.41 ± 0.29, 4.07 ± 1.33 and 2.67 ± 0.45 in 2007, 2008 and 2009, respectively, while those from C. malaccensis stand were 3.96 ± 0.53, 4.26 ± 0.73 and 3.45 ± 1.04, respectively. In general, the Q_s10 values from the P. australis stand was lower than that of the C. malaccensis stand (P > 0.05). On the other hand, for Q_a10 of CH₄ emissions, the values from C. malaccensis stand were significantly higher in 2008 compared to the other two years (P < 0.05), while that from P. australis stand were not distinct different (P > 0.05). In 2007–2009, annual mean Q_a10 of CH₄ emission from P. australis stand was 3.06 ± 0.04, 4.78 ± 1.58 and 2.35 ± 0.27, respectively, while that from the C. malaccensis stand was 3.02 ± 0.24, 8.26 ± 2.09 and 2.76 ± 0.69, respectively. The annual mean CH₄ fluxes from the two stands were also highest in 2008, with values of 6.41 ± 0.94 and 2.97 ± 0.65 mg m^-2 h^-1 for the P. australis and C. malaccensis stands, respectively. The variations in Q_s10 and Q_a10 of the two stands among these three years were consistent with CH₄ emission, except for the Q_s10 of the P. australis stand (Figs 4 and 5).

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Fig 4. Interannual variations of Q_s10 values (solid triangle), CH₄ emission (open circle) and soil temperatures at 10 cm depth (solid circle) in the two marsh stands from 2007 to 2009.

Error bars represent 1 standard error of the means.

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Fig 5. Interannual variations of Q_a10 values (solid triangle), CH₄ emission (open circle) and air temperatures (solid circle) in the two marsh stands from 2007 to 2009.

Error bars represent 1 standard error of the means.

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Seasonal Variations in Q₁₀ Values

For the two marsh stands, both Q_s10 and Q_a10 generally exhibited a distinct difference between the warm and cold months except in 2009 (Fig 6). In 2007, both Q_s10 and Q_a10 of CH₄ emission from the two marsh stands were considerably lower in the warm months compared to those in the cold months (P < 0.05, Fig 6), particularly for the Q_a10 of CH₄ emission from the P. australis stand (P < 0.05, Fig 6). In 2009, both Q_s10 and Q_a10 from the C. malaccensis stand were also slightly lower in the warm months (P > 0.05), but the seasonal difference was less discernible for the P. australis stand (P > 0.05, Fig 6). In contrast, the Q_s10 values of CH₄ emission from the two stands in 2008 were significantly higher in the warm months than in the cold months (P < 0.05).

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Fig 6. Q_s10 and Q_a10 of CH₄ emissions from the two marsh stands in the warm months and cold months from 2007 to 2009.

Values are represented by means of triplicates ± 1 standard error. Significant differences in Q_s10 or Q_a10 (P < 0.05) between the two periods are indicated by different letters.

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Difference in Q₁₀ Values Between Two Tidal Stages

Fig 7 shows the mean Q_s10 and Q_a10 of CH₄ emission from the two marsh stands in two tidal stages (before flooding and after ebbing) over three years. In 2007, we found significantly lower Q_s10 and Q_a10 of CH₄ emission from the P. australis stand before flooding (BF) compared to those after ebbing (AE) (P < 0.05), while for the C. malaccensis stand, the difference was not statistically significant between the two tidal stages (P > 0.05). In 2008, the Q_s10 and Q_a10 values of both stands were higher during BF and AE, respectively, yet the difference was only statistically significant for the Q_s10 value in the C. malaccensis stand (P < 0.05). In 2009, no significant difference in both Q_s10 and Q_a10 values were observed between the two tidal stages in the two stands (P > 0.05), although we observed considerably higher mean values during AE compared to BF in the C. malaccensis stand.

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Fig 7. Q_s10 and Q_a10 of CH₄ emission from the two marsh stands in two tidal stages (before flooding and after ebbing) from 2007 to 2009.

Values are represented by means of triplicates ± 1 standard error. Significant differences in Q_s10 or Q_a10 (P < 0.05) between the two tidal stages are indicated by different letters.

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Relationships between Q_s10 values and other soil parameters

The Q_s10 values were not significantly different among the three years of study in both marsh stands (P > 0.05). Therefore, the Q_s10 values in the three different years trial could be treated as replicates of the stands. Correlation analysis shows that the Q_s10 of both stands were negatively correlated with soil conductivity, but positively correlated with soil redox potential (Table 2). The Q_s10 of CH₄ emission from the P. australis stand was positively correlated with soil pH, while an opposite relationship was observed in the C. malaccensis stand (Table 2).

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Table 2. Pearson correlation coefficients between Q_s10 of CH₄ emissions and soil properties from the two marsh stands.

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Discussion

Relationship Between CH₄ Flux and Temperature

In our study, the annual mean CH₄ emission ranged from 5.26 ± 0.67 to 6.41 ± 0.94 mg m^-2 h^-1 for the P. australis stand, and 0.84 ± 0.12 to 2.97 ± 0.65 mg m^-2 h^-1 for the C. malaccensis stand, which was consistent with previous findings of a lower CH₄ emission associated with a higher salinity condition [32]. This was likely a result of the high availability of electron acceptors (e.g. sulfate, nitrate) in seawater that completely eliminated methanogens and shifted the dominant anaerobic pathways of organic carbon mineralization [33,34]. Moreover, we found that CH₄ emission rate in our tidal wetland study site was lower than that in a tidal freshwater marsh from the Daoqingzhou wetland upstream of the Minjiang estuary, China, but within the range reported in the estuarine wetlands in the Yangtze River in China and Sundarban in India [35,36] (Table 3). The exponential model expressed the relationships between CH₄ emission and temperature fairly well (Fig 3), which was consistent with findings in a boreal forest wetland in Saskatchewan Canada [37] and a high P. australis marsh of the Wuliangsu Lake, Inner Mongolia, northern China [38]. Temperature governs soil biogeochemical processes directly by altering microbial metabolism which is largely driven by enzymatic kinetics, or indirectly by controlling substrate availability [39–41]. Numerous studies [37, 42–44] have demonstrated a positive relationship between CH₄ emission and temperature as a result of the increased C availability at higher temperatures. Meanwhile, the influence of temperature on CH₄ emission is very complex as the overall CH₄ emission from wetland soils to the atmosphere is a net result of CH₄ production, oxidation, and transport, which could be independently controlled by temperature or other factors such as precipitation, soil carbon input amount and quality, soil texture, etc. [40,41].

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Table 3. Summary of methane emission rates from estuarine wetlands reported in previous studies.

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Inter-annual Variations in Q₁₀ Values

Understanding the response of soil biogeochemical processes to a warmer world is critical for predicting short-term and long-term changes in the cycling of soil carbon and nitrogen. Field measurements of both the magnitude and temperature sensitivity of CH₄ emission are important for understanding methane dynamics in wetlands. We observed the highest Q₁₀ values of CH₄ emission from the tidal marsh stands dominated by P. australis and C. malaccensis in 2008, with the Q_s10 values of 4.07 ± 1.33 for the P. australis stand and 4.26 ± 0.73 for the C. malaccensis stand, and the Q_a10 values of 4.78 ± 1.58 for the P. australis stand and 8.26 ± 2.09 for the C. malaccensis stand, respectively (Figs 4 and 5). The higher temperature sensitivity of CH₄ emission from both stands in 2008 was likely the result of a higher soil temperature in 2008 than the other two years (Fig 4), which could speed up the dissolution and diffusion of substrates [41,42]. At the same time, the annual mean CH₄ fluxes from the two stands were found to be highest in 2008. Interannual variability of Q₁₀ was not significant among the three years in both stands (P > 0.05), except for Q_a10 in the C. malaccensis stand with significantly higher value in 2008. The high temporal and spatial heterogeneity of soil metabolism might have partly masked some possible differences in mean Q_s10 values of the two stands among years [40]. Updegraff et al. [45] found a large variation in Q₁₀ of CH₄ production potential among the soils of northern wetlands, ranging from Q₁₀ values of 1.98 in sedge meadow to 16.2–28.0 in various peat soils to a depth of 1 m, which implied a strong temperature-substrate interaction influencing methanogenic metabolism. In a review of the potential rate of CH₄ production, Segers [46] reported a high variability of Q₁₀ for methanogenesis in wetland soils, with an overall mean of 4.1 ± 0.4 and a range of 2–28 and 1.5–6.4 for minerotrophic and oligotrophic peat soils, respectively. A very wide range of Q₁₀ of CH₄ production between 1 and 35 has been observed in some acid mire soils [47]. Valentine et al. [48] found that the higher Q₁₀ coefficients (1.7 to 4.7) observed for methanogenesis in peat slurries were related to the lower lignin to nitrogen ratios.

Seasonal Variations in Q₁₀ Values

We found that the Q₁₀ values (both of the Q_s10 and Q_a10 values) of CH₄ emission for the P. australis stand and the C. malaccensis stand were higher in the cold months than those in the warm months during 2007 and 2009, which was consistent with the findings of previous studies [16;22–24;49], with the exception of Q_a10 values from the P. australis stand. The Q₁₀ value reflects the apparent temperature sensitivity of the underlying microbial processes involved in CH₄ production. Temperature has been found to govern microbial populations more strongly at lower temperatures [16, 49]. Temperature affects both production and turnover of extracellular enzymes in soils [50], and thus possibly indirectly alters the Q_s10 values of CH₄ emission. The Q₁₀ value of Methanosarcina barkeri, which was able to metabolize both acetate and H₂-CO₂ in the production of CH₄, was found to range from 1.3 to 4 [51], while methanogenic bacteria in rice paddy soils had a Q₁₀ value of up to 12 [52]. The large variation of CH₄ production could be due to the anomalous temperature behavior of the methanogens themselves as well as the interactions between several distinct microbial processes [46]. Dunfield et al. [53] reported a higher Q₁₀ value for CH₄ production (5.3–16) compared to that of CH₄ oxidation (1.4–2.1) in some northern peat soils which suggested that the Q₁₀ of the overall CH₄ emission may be further affected by the different temperature responses of methanogens and methanotrophs due to different enzymatic processes. Several studies also have indicated that the temperature sensitivity of extracellular enzymes varied seasonally [54,55]. In this study, the seasonal pattern of Q₁₀ values (both Q_s10 and Q_a10) of CH₄ emission for the two stands in 2008 was opposite to that observed in 2007 and 2009 (Fig 6). Unfortunately, we cannot provide a credible explanation for this variability because we did not have any information regarding the influence of different temperature ranges on methanogen populations to provide further insights regarding the causes for the seasonal variations in Q₁₀ values of CH₄ emission during the three years.

Difference in Q₁₀ Values Between Two Tidal Stages

We did not obtain any conclusive results whether there was a consistent difference in the Q₁₀ of CH₄ emission between the two tidal stages (BF and AE) (Fig 7). A considerable temporal variation in CH₄ emission was found, with a higher flux during BF in some months but a greater emission during AE in some other months. In a 4-year study, Chang and Yang [8] also showed that the monthly CH₄ emissions were sometimes higher during BF, whereas in other months, they were higher during AE. This inherently high temporal variability of CH₄ emission during BF and AE would further add to the difficulty of examining the influence of tidal stages on the temperature sensitivity of CH₄ emission in the two marsh stands. Salinity is an important stressor factor in coastal marshes through its effects primarily on ionic strength and the microbial pathway of soil carbon mineralization [33]. Neubauer [34] found that the Q₁₀ of CH₄ emission were comparatively lower in the added salt plots (Q₁₀ = 1.6–2.5) than that in the added fresh plots (Q₁₀ = 3.2–3.5) at Brookgreen Gardens tidal freshwater marsh, USA. In our study, the Q_s10 values of both stands were negatively correlated with soil conductivity, although statistically not significant (P > 0.05) (Table 2). The annual mean soil conductivity was 3.58–4.29 mS cm^-1, with no significant difference between BF and AE (P > 0.05). Soil pH is another major variable that could govern the ionization of organic molecules, as well as the activity and function of enzymes [56]. Min et al. [56] found that the C-acquiring β-glucosidase (βGase) activity was higher in more alkaline conditions regardless of soil temperature, but the temperature sensitivity of βGase was higher at pH 4.5. In our study, we found lower soil pH values in the two stands during AE than at BF, although the range of annual mean was small (6.44–6.78) and some of the differences were not significant statistically. Soil redox potential could also profoundly affect CH₄ production and emission from wetland soils as methanogens are anaerobic microorganisms, but we found no significant correlation between soil redox potential and the Q_s10 of CH₄ emission in both stands during BF and AE (P > 0.05). Overall, our results suggest that the temporal and spatial variations of soil properties may exert little influence on the Q₁₀ of CH₄ emission over the short term between the two tidal stages.

Difference in Q₁₀ Values Between Two Marsh Stands

It is known that some wetland plants capable of convective transport substantially influence CH₄ emission by providing a pathway for gases through aerenchyma [57]. Simultaneously, aerenchyma tissues of wetland plants could transport oxygen to the anaerobic root zone [30]. In our study, we found the CH₄ fluxes from the P. australis stand were higher than those from the C. malaccensis stand, which could be attributed to a better developed aerenchyma system in P. australis. However, it is hard to extrapolate this effect of wetland vegetation to temperature sensitivity (Q₁₀ values) of CH₄ emission owing to the complicated biogeochemical processes. It is possible that CH₄ emission induced by convective transport in wetland plants is susceptible to changes in the local micro-environment (e.g. air temperature and relative humidity) [58]. Alternatively, wetland plants physiological functions (such as transpiration, photosynthesis and respiration) may also contribute to the CH₄ metabolic processes [30]. Song et al. [6] found significant difference in Q₁₀ values of CH₄ emission between the Carex lasiocarpa and Calamagrostis angustifolia marshes of the Sanjing Plain, northeastern China (2.50 vs. 1.90). In our study, we also found lower mean Q₁₀ values (Q_s10 and Q_a10) of CH₄ emission for the P. australis stand when compared with the C. malaccensis stand, albeit the difference was not significant. No significant differences in the annual Q₁₀ values (Q_s10 and Q_a10) of CH₄ emission were found among the three study years for both stands (P > 0.05), with the exception of Q_a10 for the C. malaccensis stand (P < 0.05) (Figs 4 and 5). Meanwhile, the Q_s10 values of CH₄ emission determined in our tidal wetlands were found to be higher than those in the freshwater marshes in the Sanjiang Plain of northeast China (2.67–4.26 vs. 2.49), which suggests a stronger positive climatic feedback to warming in the subtropical brackish marshes compared to the freshwater counterparts in the temperate region. On the other hand, the Q_s10 values in the peat bogs of Moorehouse Nature Reserve in North Pennines, UK as well as the paddy fields in Hangzhou and Taoyuan of China were higher than those in our estuarine marshes (5.2–5.93, Table 4), which might be related to differences in root exudation, methanotrophic communities, etc. that deserve further investigation.

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Table 4. Summary of Q_s10 values of methane emissions from different types of wetlands reported in previous studies.

https://doi.org/10.1371/journal.pone.0125227.t004

Conclusions

In summary, we found that CH₄ emission from the two tidal marsh stands in the Min River estuary increased exponentially with both soil and air temperatures. Both Q_s10 and Q_a10 exhibited a strong seasonal pattern, yet the variations were not consistent among different years. We also observed differences in Q₁₀ of CH₄ emission between the two tidal stages, with the pattern being quite variable from one year to the other. Meanwhile, we found a lower Q₁₀ values (Q_s10 and Q_a10) of CH₄ emission for the P. australis stand compared with the C. malaccensis stand, although the difference was not statistically significant.

Although measurements in the field has the advantage of being more realistic than laboratory assays, our results suggest that the Q₁₀ values of CH₄ emission derived from field data should generally be regarded as a semi-empirical fitting parameter for simple models only as the fluxes determined reflect a combination of a number of processes (e.g. substrate production, methane production, oxidation and transmission). Q₁₀ is actually only an indicator of the apparent temperature sensitivity, with the actual fluxes in the field being affected by a suite of factors like temperature, root biomass quantity and activity, moisture conditions, and perhaps other unknown variables. In view of the large variability of the temperature response of CH₄ emissions over space and time, a longer-term monitoring with more frequent measurements might be necessary to obtain a better understanding of the variations of Q₁₀ values. Given the paucity of data on Q₁₀ of CH₄ emission from the subtropical region, our findings provided some useful data on the temperature sensitivity to better predict the response of CH₄ emission to future climate change.

Acknowledgments

This work was financially supported by the National Science Foundation of China (Grant No: 40671174 and 41071148), the Program for Innovative Research Team in Fujian Normal University (IRTL1205), Research Grants Council of the Hong Kong Special Administrative Region, China (CUHK458913), and The Chinese University of Hong Kong (SS12434). We thank Cong-Ping Yan, Lu-Ying Lin, Bo Lei, An E, Ji Lia, Chun Yao, Ze-Qiong Liu, Zhi-Qiang Hu for their field assistance. We would also like to thank the anonymous reviewers for their valuable comments that have substantially improved our manuscript.

Author Contributions

Conceived and designed the experiments: CW CT CZ. Performed the experiments: WW JH. Analyzed the data: CW DYFL. Wrote the paper: CW CT DYFL.

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Figures

Abstract

Introduction

Materials and Methods

Results

Relationship Between CH4 Flux and Temperature

Inter-annual Variations in Q10 Values

Seasonal Variations in Q10 Values

Difference in Q10 Values Between Two Tidal Stages

Relationships between Qs10 values and other soil parameters

Discussion

Relationship Between CH4 Flux and Temperature

Inter-annual Variations in Q10 Values

Seasonal Variations in Q10 Values

Difference in Q10 Values Between Two Tidal Stages

Difference in Q10 Values Between Two Marsh Stands

Conclusions

Acknowledgments

Author Contributions

References

Relationship Between CH₄ Flux and Temperature

Inter-annual Variations in Q₁₀ Values

Seasonal Variations in Q₁₀ Values

Difference in Q₁₀ Values Between Two Tidal Stages

Relationships between Q_s10 values and other soil parameters

Relationship Between CH₄ Flux and Temperature

Inter-annual Variations in Q₁₀ Values

Seasonal Variations in Q₁₀ Values

Difference in Q₁₀ Values Between Two Tidal Stages

Difference in Q₁₀ Values Between Two Marsh Stands