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Soil Respiration in a Subtropical Mangrove Wetland in the Jiulong River Estuary, China
Pedosphere 23(5): 678–685, 2013 ISSN 1002-0160/CN 32-1315/P c 2013 Soil Science Society of China Published by Elsevier B.V. and Science Press
Soil Respiration in a Subtropical Mangrove Wetland in the Jiulong River Estuary, China∗1 JIN Liang1,2 , LU Chang-Yi1,∗2 , YE Yong1 and YE Gong-Fu3 1 College
of the Environment & Ecology, Xiamen University, Xiamen 361005 (China) University Tan Kah Kee College, Zhangzhou 363105 (China) 3 Fujian Institute of Forestry Science, Fuzhou 350002 (China) 2 Xiamen
(Received April 12, 2013; revised July 15, 2013)
ABSTRACT The diurnal and seasonal variations of soil respiration (SR) were studied at a subtropical mangrove wetland in the Jiulong River Estuary from May 2010 to April 2011. SR rates were measured continuously from 08:00 to 06:00 local time (24-h time system) on July 8–9 and October 3–4, 2010; and January 15–16 and April 11–12, 2011. Similar patterns in the diurnal variation of SR were observed on October 2–3 and April 11–12, with the maximum values at 14:00 and the minimum at 00:00. However, the diurnal dynamics of SR on July 8–9, 2010 and January 15–16, 2011 showed different patterns, with the maximum values at 08:00–10:00 on above sampling dates and the minimum at 22:00 on July 8 and at 04:00 on January 16. The daily mean values of SR approximated to the values measured at 08:00. SR fluctuated with distinct seasonal patterns. The seasonal variation was characterized by a mono-peak pattern, with the highest rate (6.18 μmol CO2 m−2 s−1 ) in July and the lowest rate (0.36 μmol CO2 m−2 s−1 ) in December. The results showed that the variation of SR in mangrove wetland was mainly controlled by soil temperature, and there was no significant correlation between SR and soil water content. It also implied that the model of SR in mangrove wetland should not only consider the effect of soil temperature, but also incorporate other factors, such as water level, precipitation, microbial activity and photosynthesis, which also could affect SR. Key Words:
controlling factors, Kandelia candel, microbial activity, neap tide, soil temperature
Citation: Jin, L., Lu, C. Y., Ye, Y. and Ye, G. F. 2013. Soil respiration in a subtropical mangrove wetland in the Jiulong River Estuary, China. Pedosphere. 23(5): 678–685.
Soil respiration (SR) is the primary pathway via which CO2 fixed by plants returns to the atmosphere (Chapin et al., 1996). On an annual scale, 60%–80% of ecosystem respiration or 40%–60% of gross primary production is contributed by SR (Raich and Schlesinger, 1992; Janssens et al., 2001). Due to the complex processes, with interactions and feedback among its components and influencing factors, SR is a major source of uncertainty in estimating the terrestrial carbon budget at ecosystem and larger scales (Dilly et al., 2000). Forecasts of SR changes with climate are obviously needed, but they remain highly uncertain (Denman et al., 2007). Therefore, it is important to obtain accurate estimates of SR and to understand the environmental controls on the underlying processes. Factors affecting SR include temperature (Lloyd and Taylor, 1994; Kirschbaum, 1995; Rustad et al., 2001; Davidson et al., 2006), soil water content (Hanson et al., 2000; Davidson et al., 2006; Jia et al., ∗1 Supported
2007), root exudation (Kuzyakov, 2002), photosynthesis (Cheng et al., 1996) and litterfall (DeForest et al., 2006; Chang et al., 2008). The response of respiration to temperature is reviewed by Kirschbaum (2006), with important conclusions that water and carbon substrate availability can limit SR, and those factors have complicated relationships with temperature. Rapid water input may cause a large pulse of SR (Lee et al., 2004). Conversely, respiration will be reduced in dry soils where conditions are suitable (Davidson et al., 1998; Baldocchi et al., 2006). The wetland plays a significant role in the global carbon cycle because it boasts the highest soil carbon storage among all ecosystems. Wetlands cover only about 1% of the earth’s surface, but soil carbon storage value for wetland ecosystems (about 450 Pg) is nearly 15% of overall terrestrial soil carbon storage (Sabine et al., 2004). Wetlands are responsible for a proportion of much greater biogeochemical fluxes between the land surface, the atmosphere and hydrologic system. The
by the National Natural Science Foundation of China (No. 41176092). author. E-mail: [email protected].
∗2 Corresponding
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mangrove forests occupy the interface between land and sea on sheltered tropical and subtropical coasts over a broad latitudinal range (Duke et al., 1998). They play important roles in sustaining tropical and subtropical coastal productivity and sequester large amounts of carbon below ground (Ewel et al., 1998; Chmura et al., 2003; Zhang et al., 2012). So mangrove wetland can be one of the most productive ecosystems in the world. Estuarine wetlands with excellent locations, abundant resources (Huang et al., 2006) and a complex and highly volatile ecosystem (Zhao et al., 2005) are mostly newly-developed wetlands, and usually severely affected by human activities (Lotze et al., 2006). Many studies have been conducted in wetlands to study the factors influencing SR (Deverel and Rojstaczer, 1996; Heinscha et al., 2004; Kutzbach et al., 2007; Zhou et al., 2009; Luo and Xing, 2010). In contrast, little research has been done on partitioning SR in mangrove wetland in estuaries (Alongi et al., 2005; Lovelock, 2008; Kristensen et al., 2008). The aims of this study were to i) describe the differences in the diurnal dynamics of SR among four seasons; and ii) analyze the main factors influencing the diurnal and seasonal variations of SR.
during summer and autumn. The mean salinity of open water adjacent to the forest is 17 g kg−1 . The dynamic and geomorphological processes of the wetland are profoundly influenced by the semi-diurnal tide with a mean tidal range of 4 m. The Kandelia candel mangrove forest in Fugong was rehabilitated in 1962. The current forest structure is described as follows: density 15 400 plants ha−1 , height 5.87 m, diameter at breast height 6.75 cm, and crown density 84.20% (Gu, 2011). Soil pH is 7.15. Soil salinity and soil organic carbon are 1.91 and 13.27 g kg−1 , respectively (Gu, 2011). The K. candel forest is distributed in the high intertidal zone (Fig. 2), and the width of the forest is about 30 m. In one month, the forest was inundated by high tides for only 6–8 days.
MATERIALS AND METHODS
Fig. 2
Study site
Soil respiration measurement
An experiment was performed in Fugong mangrove wetland (117◦ 55 E, 24◦ 24 N), which belongs to the Zhangzhou Mangrove Nature Reserve, located in the Jiulong River Estuary, Fujian Province, China (Fig. 1). This region is subject to the East Asia subtropical monsoon climate, with a mean annual temperature of 21 ◦ C ranging from −1 ◦ C in January to 39 ◦ C in July. The mean annual precipitation is approximately 1 371 mm, with 70% of the rainfall occur ring during May–September and a few typhoons occurring
SR rates were measured using an automated soilCO2 flux monitoring system (LI-8100, LI-COR, USA) equipped with a long-term chamber (Model 8100-101) that can be operated in the field and thus can provide SR data at a high temporal resolution. The LI-8100 soil-CO2 flux system measured CO2 concentration in a non-dispersive infrared gas analyzer. An integrated pump circulated the headspace air from the chamber to the analyzer in the closed state and the CO2 concentration data as well as the calculated flux rates were recorded in this system. Twelve of PVC soil collars (inner diameter 20 cm and height 10 cm) were divided into 6 groups on average and randomly arranged on a 30 m transect with 30 m spaces. The details describing sampling sites are shown in Fig. 2. The soil collars were inserted in the soil to a depth of 8 cm at each sampling point, one day before the measurements began. The soil collars were slightly inserted into the forest floor to prevent cutting of plant roots that were densely distributed in the organic layer. The border of the collar was carefully sealed from the outside with organic layer materials taken from the nearby forest floor. The tightness of the collar was checked each time before measurements. During the measurement, the moving
Fig. 1 Map of the study area in Fugong of the Jiulong River Estuary.
Sampling sites in Fugong mangrove wetland.
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dome covered the collar and the total volume of the chamber was 5 800 cm3 . The soil-CO2 flux monitoring system operated monthly from May 2010 to April 2011 and the SR was measured every 2 hours with 2 min closure of the chamber. Usually, SR was measured between 08:00 and 12:00 local time. To catch the diurnal pattern of SR, these were made continuously from 08:00 to 06:00 local time (24-h time system) on July 8–9 and October 3–4, 2010; and January 15–16 and April 11–12, 2011. All of the measurements were done during neap tides. Soil temperature was measured simultaneously with SR using a copper/constantan thermocouple penetration probe (Model 8100-201) inserted in the soil near each collar. Soil water content in the vicinity of the collars was monitored with ECH2 O soil moisture sensors (Decagon Devices Inc., Pullman, WA, USA). Soil temperature was measured continuously just below the surface at about 5 cm in the same sampling site as SR measurement. After all the measurements, 6 soil samples were taken from the profile of each sampling location for soil water content determination monthly. Statistical analysis Exponential regressions were used to evaluate the relationship between soil respiration and soil temperature. Linear regression model was used to describe the relationships between soil respiration and soil water content (Jabro et al., 2009). All statistical analyses were performed using SPSS 16.0 software. RESULTS Climate conditions The meteorological parameters recorded from May 2010 to April 2011 exhibited the patterns that were typical in the study area (Fig. 3). The annual precipitation for the study period amounted to 1 628 mm. In the East Asian rainy season (Meiyu season), the monthly precipitation was higher than 200 mm from May to June. In September, due to typhoons occurring, precipitation increased sharply with a maximum value of 755 mm. Mean monthly air temperature showed a typical seasonal pattern with the peak appearing in July. During the study period, the highest mean monthly air temperature was 30.8 ◦ C and the lowest was 9.9 ◦ C; the mean annual air temperature was 21 ◦ C. Diurnal variations of soil respiration Fig. 4 shows the diurnal variations of SR and soil
Fig. 3 Monthly precipitation and mean monthly air temperature from May 2010 to April 2011 in Fugong mangrove wetland.
temperature at the 5 cm depth on July 8–9 and October 2–3, 2010 and January 15–16 and April 11–12, 2011. The diurnal dynamics of SR were similar between October 2–3 and April 11–12, and they could be expressed as unimodal curves. SR reached a maximum at 14:00 and fell to the minimum at 00:00. However, on July 8–9, 2010 and January 15–16, 2011 the diurnal dynamics of SR showed different patterns, with the maximum values at 08:00–10:00 on above sampling dates and the minimum at 22:00 on July 8 and at 04:00 on January 16. During the study period, mean daily CO2 emission rates approximated to the values measured at 08:00 and 20:00. Thus, SR rates around 08:00 could be taken as mean daily CO2 emission rate. Soil respiration rate was highly associated with soil temperature (at 5 and 10 cm depth) on October 2–3 and April 11–12, and the variations of soil temperature at 5 cm depth rather than at 10 cm could better explain the variations in SR (Tabel I). As shown in Fig. 4, daily maximum value of SR occurred around the lowest tide time. Therefore, the water level may have an important influence on soil respiration. TABLE I Correlation coefficients between soil respiration rate and soil temperature at 5 and 10 cm depth on the four sampling dates Date
At 5 cm depth
July 8–9, 2010 October 2–3, 2010 January 15–16, 2011 April 11–12, 2011
0.151 0.860 0.420 0.839
(P (P (P (P
> 0.05) < 0.01) > 0.05) < 0.01)
At 10 cm depth 0.042 0.756 0.149 0.835
(P (P (P (P
> 0.05) < 0.01) > 0.05) < 0.01)
Seasonal variation of soil respiration An exponential function could explain most of the
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Fig. 4 Diurnal variations of soil respiration and soil temperature at 5 cm depth on (a) July 8–9, 2010 (lowest tide time: 10:20, 23:30); (b) October 2–3, 2010 (lowest tide time: 14:40, 03:00); (c) January 15–16, 2011 (lowest tide time: 16:00, 05:40); and (d) April 11–12, 2011 (lowest tide time: 13:00, 01:50) in Fugong mangrove wetland. Error bars represent standard errors of means (n = 12).
variations in SR with higher correlation with soil temperature at the 5 cm depth (R2 = 0.708, P < 0.001, n = 144) (Fig. 5a): SR = 0.103e0.119Ts
(1)
where SR is the soil respiration (μmol CO2 m−2 s−1 ), and Ts is the soil temperature at the 5 cm depth (◦ C). The effect of soil water content on SR was exami-
ned, and the result showed that soil water content only accounted for 6.1% of the seasonal variation of SR (Fig. 5b). To better understand the seasonal variation of SR, the SR values at 08:00 in each month (except July, October, January and April) were analyzed as the mean daily CO2 emission rate. During the whole study period, the SR rates increased from May to July and then decreased until March of next year. The results
Fig. 5 Soil respiration measured at 08:00 from 2010 to 2011 plotted against (a) soil temperature at 5 cm depth (P < 0.001, n = 144) and (b) soil water content at 10 cm depth (P < 0.05, n = 72).
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showed that SR exhibited a pronounced seasonal variation with a minimum value of 0.36 μmol CO2 m−2 s−1 in December and a maximum of 6.18 μmol CO2 m−2 s−1 in July (Fig. 6), in accordance with the minimum and maximum values (9.79 and 28.04 ◦ C, respectively) of soil temperature at the 5 cm depth. Annual mean CO2 emission rate during the entire study period was 1.72 μmol CO2 m−2 s−1 . Soil water content ranged between 335.5 g kg−1 on September 17 and 472.5 g kg−1 on June 6 over the whole study period (Fig. 7), correlating negatively with soil temperature.
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ever, the other seasons showed different dynamics, with the maximum values of SR occurring at 08:00–10:00, and the minimum values at 22:00 in summer and at 04:00 in winter. Soil temperature was an important environmental factor affecting the diurnal variations of SR. However, the variations of SR and soil temperature were not in-phase in different seasons in this study. The result showed that the water level may have an important influence on SR, especially in the low tide stage. Many studies have shown that SR increased with water-leveldrawdown, while water level and SR showed a significant negative correlation (Moore et al., 1998, Song et al., 2008). Due to the incompletely decomposition under anaerobic conditions, the organic matter in wetland could only produce little CO2 which is easily consumed in hydrolysis reaction. However, under aerobic conditions, the organic matter would be oxidized to CO2 and water (Martikainen et al., 1993). Therefore, the SR rates will increase in the condition of water level drawdown. At a regular changing water level (between 0 and 10 cm below the peat surface), CO2 emission at a low water level was 1.5 to 3 times higher than that at a high water level (Aerts and Ludwig, 1997). Seasonal variation of soil respiration and controlling factors
Fig. 6 Seasonal variations of soil respiration and soil temperature at 5 cm depth during the study period from 2010 to 2011. Error bars represent standard errors of means (n = 12).
Fig. 7 Variation of soil water content during the study period from 2010 to 2011. Error bars represent standard errors of means (n = 6).
DISCUSSION Diurnal variations of soil respiration The diurnal dynamics of SR were similar between spring and autumn, with the maximum value appearing at 14:00 and the minimum value at 00:00. How-
The SR of mangrove wetland in the Jiulong River Estuary fluctuated with distinct seasonal patterns. The SR rates recorded in the present study (0.36–6.18 μmol CO2 m−2 s−1 ) were similar with that recorded by Alongi et al. (2005) at the same area (2.55–6.01 μmol CO2 m−2 s−1 ). Comparing with previous studies, e.g., some mangroves in Caribbean, Australia and New Zealand (−0.25–2.97 μmol CO2 m−2 s−1 ) (Lovelock, 2008), reed wetlands in Yellow River Estuary, and Liaohe River Estuary (0.24–1.06 μmol CO2 m−2 s−1 ) (Luo and Xing, 2010), the SR of mangrove wetland in the Jiulong River Estuary was a little higher. There was a significant exponential relationship between SR and soil temperature during its season variations (Eq. 1). Exponential regressions have often been used to describe the relationship between SR and soil temperature at a seasonal scale when soil moisture or other factors are not limiting (Buchmann, 2000; Janssens and Pilegaard, 2003; Reth et al., 2004). It is clear that SR responds positively to temperature in a number of systems (Davidson et al., 1998; Fang and Moncrieff, 2001; Wiseman and Seiler, 2004; Han et al., 2007). A number of studies have shown that soil water content has a limited impact on SR rate, except under soil saturation or water deficits (Edwards, 1975;
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Hanson et al., 1993). The mangrove wetland is an area of land in which the soil is saturated either permanently or seasonally, so the soil water content remained high during the whole period. High soil water content would limit belowground biological activity, and SR was negative correlated with soil water content throughout the study period. A sharp increase in SR after rainfall events is observed in many studies (Holt et al., 1990; Rochette et al., 1991; Davidson et al., 2000; Liu et al., 2002), and this could account for the inter-annual variability of the soil carbon efflux (Rey et al., 2002). In this study, the same result was found. After the Meiyu precipitation, the SR increased sharply from June to July, with the soil temperature dropping, the SR decreased after July. Due to typhoon precipitation, SR stopped decreasing with the soil temperature in September. The seasonal variation of SR was also dependent on the phenological stages (Cheng et al., 1996; Fu et al., 2002). It was reported that seasonal patterns of soil CO2 efflux are driven by both photosynthate allocation to roots and current photosynthesis (H¨ ogberg et al., 2001), and have significant correlation with biotic variables, such as microbial activity (Cleveland et al., 2007; Dilly et al., 2011), leaf area index and root biomass (Shi et al., 2006). These biotic factors may influence SR by controlling root respiration, thus modifying the temperature response of SR. Increasing temperatures can activate dormant microbes and increase microbial species richness, which can potentially broaden the mineralizable carbon pools (Andrews et al., 2000), thus promoting microbial respiration. At the same time, increasing temperatures can also activate root respiration by influencing the photosynthesis of plants, and photosynthates translocated from the aboveground part of the plant. Furthermore, increasing soil temperature advances gas transmission in soil, and therefore accelerates gas exchange with the atmosphere (Tang et al., 2003). However, at high soil temperature, often in dwarf forests, SR declined with increasing temperature due to the activity of benthic photosynthetic microbial communities which are important in retaining respired carbon within the ecosystem (Lovelock, 2008). Therefore, SR decreased substantially after July when the temperature still remained high (Fig. 6). CONCLUSIONS Being a typical subtropical mangrove wetland, the Jiulong River Estuary study site had very unique characteristics of SR. The diurnal dynamics of SR varied among four seasons. Soil temperature was not the most important factor affecting diurnal variation of SR. The
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daily maximum value of SR occurred around the lowest tide time. The seasonal variation of SR revealed a mono-peak pattern which was primarily controlled by soil temperature. SR rate exponentially increased with increasing soil temperature. No significant correlation existed between SR and soil water content. Annual mean CO2 emission rate during the entire study period was 1.72 μmol CO2 m−2 s−1 . SR declined substantially with slowly declining temperature due to the activity of benthic photosynthetic microbial communities which were important in retaining respired carbon within the ecosystem. ACKNOWLEDGEMENTS We thank Mr. Pang Bo-Peng, Mr. Dong Ke-Zuan and Mr. Chen Shun-Yang from the College of Environment & Ecology, Xiamen University, China for their helps in the field sampling. The authors are indebted to Prof. J. Hodgkiss in the University of Hong Kong for English polishing. Thanks also to the anonymous reviewers for their valuable comments on the manuscript. REFERENCES Aerts, R. and Ludwig, F. 1997. Water-table changes and nutritional status affect trace gas emissions from laboratory columns of peatland soils. Soil Biol. Biochem. 29: 1691–1698. Alongi, D. M., Pfitzner, J., Trott, L. A., Tirendi, F. and Klumpp, D. W. 2005. Rapid sedimentation and microbial mineralization in mangrove forests of the Jiulongjiang Estuary, China. Estuar. Coast. Shelf S. 63: 605–618. Andrews, J. A., Matamala, R., Westover, K. M. and Schlesinger, W. H. 2000. Temperature effects on the diversity of soil heterotrophs and the δ 13 C of soil-respired CO2 . Soil Biol. Biochem. 32: 699–706. Baldocchi, D., Tang, J. W. and Xu, L. K. 2006. How switches and lags in biophysical regulators affect spatial-temporal variation of soil respiration in an oak-grass savanna. J. Geophys. Res. 111: G02008. Doi: 10.1029/2005JG000063. Buchmann, N. 2000. Biotic and abiotic factors controlling soil respiration rates in Picea abies stands. Soil Biol. Biochem. 32: 1625–1635. Chang, S. C., Tseng, K. H., Hsia, Y. J., Wang, C. P. and Wu, J. T. 2008. Soil respiration in a subtropical montane cloud forest in Taiwan. Agr. Forest Meteorol. 148: 788–798. Chapin, F. S., Zimov, S. A., Shaver, G. R. and Hobble, S. E. 1996. CO2 fluctuation at high latitudes. Nature. 383: 585–586. Cheng, W. X., Zhang, Q. L., Coleman, D. C., Carroll, C. R. and Hoffmann, C. A. 1996. Is available carbon limiting microbial respiration in the rhizosphere. Soil Biol. Biochem. 28: 1283–1288. Chmura, G. L., Anisfeld, S. C., Cahoon, D. R. and Lynch, J. C. 2003. Global carbon sequestration in tidal, saline wetland soils. Global Biogeochem. Cy. 17: 1111. Doi: 10.1029/ 2002GB001917. Cleveland, C. C., Nemergut, D. R., Schmidt, S. K. and Townsend, A. R. 2007. Increases in soil respiration following labile carbon additions linked to rapid shifts in soil microbial
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Soil Respiration in a Subtropical Mangrove Wetland in the Jiulong River Estuary, China∗1 JIN Liang1,2 , LU Chang-Yi1,∗2 , YE Yong1 and YE Gong-Fu3 1 College
of the Environment & Ecology, Xiamen University, Xiamen 361005 (China) University Tan Kah Kee College, Zhangzhou 363105 (China) 3 Fujian Institute of Forestry Science, Fuzhou 350002 (China) 2 Xiamen
(Received April 12, 2013; revised July 15, 2013)
ABSTRACT The diurnal and seasonal variations of soil respiration (SR) were studied at a subtropical mangrove wetland in the Jiulong River Estuary from May 2010 to April 2011. SR rates were measured continuously from 08:00 to 06:00 local time (24-h time system) on July 8–9 and October 3–4, 2010; and January 15–16 and April 11–12, 2011. Similar patterns in the diurnal variation of SR were observed on October 2–3 and April 11–12, with the maximum values at 14:00 and the minimum at 00:00. However, the diurnal dynamics of SR on July 8–9, 2010 and January 15–16, 2011 showed different patterns, with the maximum values at 08:00–10:00 on above sampling dates and the minimum at 22:00 on July 8 and at 04:00 on January 16. The daily mean values of SR approximated to the values measured at 08:00. SR fluctuated with distinct seasonal patterns. The seasonal variation was characterized by a mono-peak pattern, with the highest rate (6.18 μmol CO2 m−2 s−1 ) in July and the lowest rate (0.36 μmol CO2 m−2 s−1 ) in December. The results showed that the variation of SR in mangrove wetland was mainly controlled by soil temperature, and there was no significant correlation between SR and soil water content. It also implied that the model of SR in mangrove wetland should not only consider the effect of soil temperature, but also incorporate other factors, such as water level, precipitation, microbial activity and photosynthesis, which also could affect SR. Key Words:
controlling factors, Kandelia candel, microbial activity, neap tide, soil temperature
Citation: Jin, L., Lu, C. Y., Ye, Y. and Ye, G. F. 2013. Soil respiration in a subtropical mangrove wetland in the Jiulong River Estuary, China. Pedosphere. 23(5): 678–685.
Soil respiration (SR) is the primary pathway via which CO2 fixed by plants returns to the atmosphere (Chapin et al., 1996). On an annual scale, 60%–80% of ecosystem respiration or 40%–60% of gross primary production is contributed by SR (Raich and Schlesinger, 1992; Janssens et al., 2001). Due to the complex processes, with interactions and feedback among its components and influencing factors, SR is a major source of uncertainty in estimating the terrestrial carbon budget at ecosystem and larger scales (Dilly et al., 2000). Forecasts of SR changes with climate are obviously needed, but they remain highly uncertain (Denman et al., 2007). Therefore, it is important to obtain accurate estimates of SR and to understand the environmental controls on the underlying processes. Factors affecting SR include temperature (Lloyd and Taylor, 1994; Kirschbaum, 1995; Rustad et al., 2001; Davidson et al., 2006), soil water content (Hanson et al., 2000; Davidson et al., 2006; Jia et al., ∗1 Supported
2007), root exudation (Kuzyakov, 2002), photosynthesis (Cheng et al., 1996) and litterfall (DeForest et al., 2006; Chang et al., 2008). The response of respiration to temperature is reviewed by Kirschbaum (2006), with important conclusions that water and carbon substrate availability can limit SR, and those factors have complicated relationships with temperature. Rapid water input may cause a large pulse of SR (Lee et al., 2004). Conversely, respiration will be reduced in dry soils where conditions are suitable (Davidson et al., 1998; Baldocchi et al., 2006). The wetland plays a significant role in the global carbon cycle because it boasts the highest soil carbon storage among all ecosystems. Wetlands cover only about 1% of the earth’s surface, but soil carbon storage value for wetland ecosystems (about 450 Pg) is nearly 15% of overall terrestrial soil carbon storage (Sabine et al., 2004). Wetlands are responsible for a proportion of much greater biogeochemical fluxes between the land surface, the atmosphere and hydrologic system. The
by the National Natural Science Foundation of China (No. 41176092). author. E-mail: [email protected].
∗2 Corresponding
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mangrove forests occupy the interface between land and sea on sheltered tropical and subtropical coasts over a broad latitudinal range (Duke et al., 1998). They play important roles in sustaining tropical and subtropical coastal productivity and sequester large amounts of carbon below ground (Ewel et al., 1998; Chmura et al., 2003; Zhang et al., 2012). So mangrove wetland can be one of the most productive ecosystems in the world. Estuarine wetlands with excellent locations, abundant resources (Huang et al., 2006) and a complex and highly volatile ecosystem (Zhao et al., 2005) are mostly newly-developed wetlands, and usually severely affected by human activities (Lotze et al., 2006). Many studies have been conducted in wetlands to study the factors influencing SR (Deverel and Rojstaczer, 1996; Heinscha et al., 2004; Kutzbach et al., 2007; Zhou et al., 2009; Luo and Xing, 2010). In contrast, little research has been done on partitioning SR in mangrove wetland in estuaries (Alongi et al., 2005; Lovelock, 2008; Kristensen et al., 2008). The aims of this study were to i) describe the differences in the diurnal dynamics of SR among four seasons; and ii) analyze the main factors influencing the diurnal and seasonal variations of SR.
during summer and autumn. The mean salinity of open water adjacent to the forest is 17 g kg−1 . The dynamic and geomorphological processes of the wetland are profoundly influenced by the semi-diurnal tide with a mean tidal range of 4 m. The Kandelia candel mangrove forest in Fugong was rehabilitated in 1962. The current forest structure is described as follows: density 15 400 plants ha−1 , height 5.87 m, diameter at breast height 6.75 cm, and crown density 84.20% (Gu, 2011). Soil pH is 7.15. Soil salinity and soil organic carbon are 1.91 and 13.27 g kg−1 , respectively (Gu, 2011). The K. candel forest is distributed in the high intertidal zone (Fig. 2), and the width of the forest is about 30 m. In one month, the forest was inundated by high tides for only 6–8 days.
MATERIALS AND METHODS
Fig. 2
Study site
Soil respiration measurement
An experiment was performed in Fugong mangrove wetland (117◦ 55 E, 24◦ 24 N), which belongs to the Zhangzhou Mangrove Nature Reserve, located in the Jiulong River Estuary, Fujian Province, China (Fig. 1). This region is subject to the East Asia subtropical monsoon climate, with a mean annual temperature of 21 ◦ C ranging from −1 ◦ C in January to 39 ◦ C in July. The mean annual precipitation is approximately 1 371 mm, with 70% of the rainfall occur ring during May–September and a few typhoons occurring
SR rates were measured using an automated soilCO2 flux monitoring system (LI-8100, LI-COR, USA) equipped with a long-term chamber (Model 8100-101) that can be operated in the field and thus can provide SR data at a high temporal resolution. The LI-8100 soil-CO2 flux system measured CO2 concentration in a non-dispersive infrared gas analyzer. An integrated pump circulated the headspace air from the chamber to the analyzer in the closed state and the CO2 concentration data as well as the calculated flux rates were recorded in this system. Twelve of PVC soil collars (inner diameter 20 cm and height 10 cm) were divided into 6 groups on average and randomly arranged on a 30 m transect with 30 m spaces. The details describing sampling sites are shown in Fig. 2. The soil collars were inserted in the soil to a depth of 8 cm at each sampling point, one day before the measurements began. The soil collars were slightly inserted into the forest floor to prevent cutting of plant roots that were densely distributed in the organic layer. The border of the collar was carefully sealed from the outside with organic layer materials taken from the nearby forest floor. The tightness of the collar was checked each time before measurements. During the measurement, the moving
Fig. 1 Map of the study area in Fugong of the Jiulong River Estuary.
Sampling sites in Fugong mangrove wetland.
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dome covered the collar and the total volume of the chamber was 5 800 cm3 . The soil-CO2 flux monitoring system operated monthly from May 2010 to April 2011 and the SR was measured every 2 hours with 2 min closure of the chamber. Usually, SR was measured between 08:00 and 12:00 local time. To catch the diurnal pattern of SR, these were made continuously from 08:00 to 06:00 local time (24-h time system) on July 8–9 and October 3–4, 2010; and January 15–16 and April 11–12, 2011. All of the measurements were done during neap tides. Soil temperature was measured simultaneously with SR using a copper/constantan thermocouple penetration probe (Model 8100-201) inserted in the soil near each collar. Soil water content in the vicinity of the collars was monitored with ECH2 O soil moisture sensors (Decagon Devices Inc., Pullman, WA, USA). Soil temperature was measured continuously just below the surface at about 5 cm in the same sampling site as SR measurement. After all the measurements, 6 soil samples were taken from the profile of each sampling location for soil water content determination monthly. Statistical analysis Exponential regressions were used to evaluate the relationship between soil respiration and soil temperature. Linear regression model was used to describe the relationships between soil respiration and soil water content (Jabro et al., 2009). All statistical analyses were performed using SPSS 16.0 software. RESULTS Climate conditions The meteorological parameters recorded from May 2010 to April 2011 exhibited the patterns that were typical in the study area (Fig. 3). The annual precipitation for the study period amounted to 1 628 mm. In the East Asian rainy season (Meiyu season), the monthly precipitation was higher than 200 mm from May to June. In September, due to typhoons occurring, precipitation increased sharply with a maximum value of 755 mm. Mean monthly air temperature showed a typical seasonal pattern with the peak appearing in July. During the study period, the highest mean monthly air temperature was 30.8 ◦ C and the lowest was 9.9 ◦ C; the mean annual air temperature was 21 ◦ C. Diurnal variations of soil respiration Fig. 4 shows the diurnal variations of SR and soil
Fig. 3 Monthly precipitation and mean monthly air temperature from May 2010 to April 2011 in Fugong mangrove wetland.
temperature at the 5 cm depth on July 8–9 and October 2–3, 2010 and January 15–16 and April 11–12, 2011. The diurnal dynamics of SR were similar between October 2–3 and April 11–12, and they could be expressed as unimodal curves. SR reached a maximum at 14:00 and fell to the minimum at 00:00. However, on July 8–9, 2010 and January 15–16, 2011 the diurnal dynamics of SR showed different patterns, with the maximum values at 08:00–10:00 on above sampling dates and the minimum at 22:00 on July 8 and at 04:00 on January 16. During the study period, mean daily CO2 emission rates approximated to the values measured at 08:00 and 20:00. Thus, SR rates around 08:00 could be taken as mean daily CO2 emission rate. Soil respiration rate was highly associated with soil temperature (at 5 and 10 cm depth) on October 2–3 and April 11–12, and the variations of soil temperature at 5 cm depth rather than at 10 cm could better explain the variations in SR (Tabel I). As shown in Fig. 4, daily maximum value of SR occurred around the lowest tide time. Therefore, the water level may have an important influence on soil respiration. TABLE I Correlation coefficients between soil respiration rate and soil temperature at 5 and 10 cm depth on the four sampling dates Date
At 5 cm depth
July 8–9, 2010 October 2–3, 2010 January 15–16, 2011 April 11–12, 2011
0.151 0.860 0.420 0.839
(P (P (P (P
> 0.05) < 0.01) > 0.05) < 0.01)
At 10 cm depth 0.042 0.756 0.149 0.835
(P (P (P (P
> 0.05) < 0.01) > 0.05) < 0.01)
Seasonal variation of soil respiration An exponential function could explain most of the
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Fig. 4 Diurnal variations of soil respiration and soil temperature at 5 cm depth on (a) July 8–9, 2010 (lowest tide time: 10:20, 23:30); (b) October 2–3, 2010 (lowest tide time: 14:40, 03:00); (c) January 15–16, 2011 (lowest tide time: 16:00, 05:40); and (d) April 11–12, 2011 (lowest tide time: 13:00, 01:50) in Fugong mangrove wetland. Error bars represent standard errors of means (n = 12).
variations in SR with higher correlation with soil temperature at the 5 cm depth (R2 = 0.708, P < 0.001, n = 144) (Fig. 5a): SR = 0.103e0.119Ts
(1)
where SR is the soil respiration (μmol CO2 m−2 s−1 ), and Ts is the soil temperature at the 5 cm depth (◦ C). The effect of soil water content on SR was exami-
ned, and the result showed that soil water content only accounted for 6.1% of the seasonal variation of SR (Fig. 5b). To better understand the seasonal variation of SR, the SR values at 08:00 in each month (except July, October, January and April) were analyzed as the mean daily CO2 emission rate. During the whole study period, the SR rates increased from May to July and then decreased until March of next year. The results
Fig. 5 Soil respiration measured at 08:00 from 2010 to 2011 plotted against (a) soil temperature at 5 cm depth (P < 0.001, n = 144) and (b) soil water content at 10 cm depth (P < 0.05, n = 72).
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showed that SR exhibited a pronounced seasonal variation with a minimum value of 0.36 μmol CO2 m−2 s−1 in December and a maximum of 6.18 μmol CO2 m−2 s−1 in July (Fig. 6), in accordance with the minimum and maximum values (9.79 and 28.04 ◦ C, respectively) of soil temperature at the 5 cm depth. Annual mean CO2 emission rate during the entire study period was 1.72 μmol CO2 m−2 s−1 . Soil water content ranged between 335.5 g kg−1 on September 17 and 472.5 g kg−1 on June 6 over the whole study period (Fig. 7), correlating negatively with soil temperature.
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ever, the other seasons showed different dynamics, with the maximum values of SR occurring at 08:00–10:00, and the minimum values at 22:00 in summer and at 04:00 in winter. Soil temperature was an important environmental factor affecting the diurnal variations of SR. However, the variations of SR and soil temperature were not in-phase in different seasons in this study. The result showed that the water level may have an important influence on SR, especially in the low tide stage. Many studies have shown that SR increased with water-leveldrawdown, while water level and SR showed a significant negative correlation (Moore et al., 1998, Song et al., 2008). Due to the incompletely decomposition under anaerobic conditions, the organic matter in wetland could only produce little CO2 which is easily consumed in hydrolysis reaction. However, under aerobic conditions, the organic matter would be oxidized to CO2 and water (Martikainen et al., 1993). Therefore, the SR rates will increase in the condition of water level drawdown. At a regular changing water level (between 0 and 10 cm below the peat surface), CO2 emission at a low water level was 1.5 to 3 times higher than that at a high water level (Aerts and Ludwig, 1997). Seasonal variation of soil respiration and controlling factors
Fig. 6 Seasonal variations of soil respiration and soil temperature at 5 cm depth during the study period from 2010 to 2011. Error bars represent standard errors of means (n = 12).
Fig. 7 Variation of soil water content during the study period from 2010 to 2011. Error bars represent standard errors of means (n = 6).
DISCUSSION Diurnal variations of soil respiration The diurnal dynamics of SR were similar between spring and autumn, with the maximum value appearing at 14:00 and the minimum value at 00:00. How-
The SR of mangrove wetland in the Jiulong River Estuary fluctuated with distinct seasonal patterns. The SR rates recorded in the present study (0.36–6.18 μmol CO2 m−2 s−1 ) were similar with that recorded by Alongi et al. (2005) at the same area (2.55–6.01 μmol CO2 m−2 s−1 ). Comparing with previous studies, e.g., some mangroves in Caribbean, Australia and New Zealand (−0.25–2.97 μmol CO2 m−2 s−1 ) (Lovelock, 2008), reed wetlands in Yellow River Estuary, and Liaohe River Estuary (0.24–1.06 μmol CO2 m−2 s−1 ) (Luo and Xing, 2010), the SR of mangrove wetland in the Jiulong River Estuary was a little higher. There was a significant exponential relationship between SR and soil temperature during its season variations (Eq. 1). Exponential regressions have often been used to describe the relationship between SR and soil temperature at a seasonal scale when soil moisture or other factors are not limiting (Buchmann, 2000; Janssens and Pilegaard, 2003; Reth et al., 2004). It is clear that SR responds positively to temperature in a number of systems (Davidson et al., 1998; Fang and Moncrieff, 2001; Wiseman and Seiler, 2004; Han et al., 2007). A number of studies have shown that soil water content has a limited impact on SR rate, except under soil saturation or water deficits (Edwards, 1975;
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Hanson et al., 1993). The mangrove wetland is an area of land in which the soil is saturated either permanently or seasonally, so the soil water content remained high during the whole period. High soil water content would limit belowground biological activity, and SR was negative correlated with soil water content throughout the study period. A sharp increase in SR after rainfall events is observed in many studies (Holt et al., 1990; Rochette et al., 1991; Davidson et al., 2000; Liu et al., 2002), and this could account for the inter-annual variability of the soil carbon efflux (Rey et al., 2002). In this study, the same result was found. After the Meiyu precipitation, the SR increased sharply from June to July, with the soil temperature dropping, the SR decreased after July. Due to typhoon precipitation, SR stopped decreasing with the soil temperature in September. The seasonal variation of SR was also dependent on the phenological stages (Cheng et al., 1996; Fu et al., 2002). It was reported that seasonal patterns of soil CO2 efflux are driven by both photosynthate allocation to roots and current photosynthesis (H¨ ogberg et al., 2001), and have significant correlation with biotic variables, such as microbial activity (Cleveland et al., 2007; Dilly et al., 2011), leaf area index and root biomass (Shi et al., 2006). These biotic factors may influence SR by controlling root respiration, thus modifying the temperature response of SR. Increasing temperatures can activate dormant microbes and increase microbial species richness, which can potentially broaden the mineralizable carbon pools (Andrews et al., 2000), thus promoting microbial respiration. At the same time, increasing temperatures can also activate root respiration by influencing the photosynthesis of plants, and photosynthates translocated from the aboveground part of the plant. Furthermore, increasing soil temperature advances gas transmission in soil, and therefore accelerates gas exchange with the atmosphere (Tang et al., 2003). However, at high soil temperature, often in dwarf forests, SR declined with increasing temperature due to the activity of benthic photosynthetic microbial communities which are important in retaining respired carbon within the ecosystem (Lovelock, 2008). Therefore, SR decreased substantially after July when the temperature still remained high (Fig. 6). CONCLUSIONS Being a typical subtropical mangrove wetland, the Jiulong River Estuary study site had very unique characteristics of SR. The diurnal dynamics of SR varied among four seasons. Soil temperature was not the most important factor affecting diurnal variation of SR. The
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daily maximum value of SR occurred around the lowest tide time. The seasonal variation of SR revealed a mono-peak pattern which was primarily controlled by soil temperature. SR rate exponentially increased with increasing soil temperature. No significant correlation existed between SR and soil water content. Annual mean CO2 emission rate during the entire study period was 1.72 μmol CO2 m−2 s−1 . SR declined substantially with slowly declining temperature due to the activity of benthic photosynthetic microbial communities which were important in retaining respired carbon within the ecosystem. ACKNOWLEDGEMENTS We thank Mr. Pang Bo-Peng, Mr. Dong Ke-Zuan and Mr. Chen Shun-Yang from the College of Environment & Ecology, Xiamen University, China for their helps in the field sampling. The authors are indebted to Prof. J. Hodgkiss in the University of Hong Kong for English polishing. Thanks also to the anonymous reviewers for their valuable comments on the manuscript. REFERENCES Aerts, R. and Ludwig, F. 1997. Water-table changes and nutritional status affect trace gas emissions from laboratory columns of peatland soils. Soil Biol. Biochem. 29: 1691–1698. Alongi, D. M., Pfitzner, J., Trott, L. A., Tirendi, F. and Klumpp, D. W. 2005. Rapid sedimentation and microbial mineralization in mangrove forests of the Jiulongjiang Estuary, China. Estuar. Coast. Shelf S. 63: 605–618. Andrews, J. A., Matamala, R., Westover, K. M. and Schlesinger, W. H. 2000. Temperature effects on the diversity of soil heterotrophs and the δ 13 C of soil-respired CO2 . Soil Biol. Biochem. 32: 699–706. Baldocchi, D., Tang, J. W. and Xu, L. K. 2006. How switches and lags in biophysical regulators affect spatial-temporal variation of soil respiration in an oak-grass savanna. J. Geophys. Res. 111: G02008. Doi: 10.1029/2005JG000063. Buchmann, N. 2000. Biotic and abiotic factors controlling soil respiration rates in Picea abies stands. Soil Biol. Biochem. 32: 1625–1635. Chang, S. C., Tseng, K. H., Hsia, Y. J., Wang, C. P. and Wu, J. T. 2008. Soil respiration in a subtropical montane cloud forest in Taiwan. Agr. Forest Meteorol. 148: 788–798. Chapin, F. S., Zimov, S. A., Shaver, G. R. and Hobble, S. E. 1996. CO2 fluctuation at high latitudes. Nature. 383: 585–586. Cheng, W. X., Zhang, Q. L., Coleman, D. C., Carroll, C. R. and Hoffmann, C. A. 1996. Is available carbon limiting microbial respiration in the rhizosphere. Soil Biol. Biochem. 28: 1283–1288. Chmura, G. L., Anisfeld, S. C., Cahoon, D. R. and Lynch, J. C. 2003. Global carbon sequestration in tidal, saline wetland soils. Global Biogeochem. Cy. 17: 1111. Doi: 10.1029/ 2002GB001917. Cleveland, C. C., Nemergut, D. R., Schmidt, S. K. and Townsend, A. R. 2007. Increases in soil respiration following labile carbon additions linked to rapid shifts in soil microbial
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