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Temporal controls on dissolved organic carbon biodegradation in subtropical rivers: Initial chemical composition versus stoichiometry
Science of the Total Environment 651 (2019) 3064–3069
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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Temporal controls on dissolved organic carbon biodegradation in subtropical rivers: Initial chemical composition versus stoichiometry Rong Mao a,b, Siyue Li a,⁎ a b
Research Center for Eco-hydrology, Chongqing Institute of Green and Intelligent Technology, Chinese Academy of Sciences, Chongqing 400714, China Key Laboratory of Silviculture, Co-Innovation Center of Jiangxi Typical Trees Cultivation and Utilization, College of Forestry, Jiangxi Agricultural University, Nanchang 330045, China
H I G H L I G H T S
G R A P H I C A L
A B S T R A C T
• Greater DTN and DTP concentrations were observed in wet season than in dry season. • DOM had greater HIX, and lower FI values in wet season than in dry season. • DOM biodegradation remained unchanged across seasons. • DOM biodegradation negatively related to DOC:DTP and DTN:DTP ratios in dry season. • DOM biodegradation negatively correlated with HIX in wet season.
a r t i c l e
i n f o
Article history: Received 19 July 2018 Received in revised form 12 October 2018 Accepted 15 October 2018 Available online 16 October 2018 Editor: Kevin V. Thomas Keywords: Biodegradability Carbon dioxide production Nutrient availability Riverine C cycle The Three Gorges Reservoir area
a b s t r a c t Dissolved organic carbon (DOC) plays an indispensable role in biogeochemical cycles and ecosystem services in rivers. However, little is known about the seasonal variations of DOC biodegradation in subtropical rivers. Here, we investigated the concentrations of DOC, dissolved total nitrogen (DTN), and dissolved total phosphorus (DTP), humification index (HIX), fluorescence index (FI), and DOC biodegradation in 57 rivers in the dry and wet seasons in the Three Gorges Reservoir area, China, and the aims were to clarify the temporal changes in DOC biodegradation and its driving factors in these subtropical rivers. Compared with dry season, DTN and DTP concentrations, and HIX value were greater, and FI value was lower in the wet season. However, DOC biodegradation remained unchanged across the two sampling seasons. Further, DOC biodegradation negatively correlated with DOC:DTP ratio, DTN:DTP ratio, and FI in the dry season, but only with HIX in the wet season. These findings emphasis that, despite unchanged DOC biodegradation, the key factors driving DOC biodegradation shift from C: N:P stoichiometry in the dry season to initial chemical composition in the wet season in subtropical rivers. Our results regarding the temporal patterns of DOC biodegradation and the underlying mechanisms bear important implications for a better understanding of C dynamics in subtropical river ecosystems. © 2018 Elsevier B.V. All rights reserved.
1. Introduction
⁎ Corresponding author at: Chongqing Institute of Green and Intelligent Technology (CIGIT), Chinese Academy of Sciences (CAS), 266, Fangzheng Avenue, Shuitu High-tech Park, Beibei, Chongqing 400714, China. E-mail address: [email protected] (S. Li).
https://doi.org/10.1016/j.scitotenv.2018.10.220 0048-9697/© 2018 Elsevier B.V. All rights reserved.
Riverine ecosystems are a fundamental component of global carbon (C) cycle, because they are important agents in modulating the transfer of organic matter from the lands to the oceans, and act as a substantial source of greenhouse gases to the atmosphere at local to global scales (Cole et al., 2007; Aufdenkampe et al., 2011; Raymond et al., 2013). In
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these ecosystems, dissolved organic carbon (DOC) is the largest pools of transported organic C, and provides the main substrates for aquatic microorganisms, especially heterotrophic bacteria (Volk et al., 1997; Balcarczyk et al., 2009; Schiller et al., 2017). Accordingly, microbial process of DOC, i.e., DOC biodegradation, accounts for a large proportion of aquatic metabolism, and is key to C cycling and greenhouse gas fluxes in riverine ecosystems (Judd et al., 2006; Cole et al., 2007; Lambert et al., 2015). In rivers, DOC is primarily derived from autochthonous and terrigenous organic matter, and is a highly heterogeneous pool of a vast diversity of soluble organic compounds with varying lability (Hosen et al., 2014). Thus, the biodegradability of DOC is largely influenced by the intrinsic properties, such as the initial chemical composition (Balcarczyk et al., 2009; Mann et al., 2012) and C:nutrient stoichiometry (Wickland et al., 2012; Mao et al., 2017). In general, DOC biodegradation differs across seasons because of the marked differences in DOC sources and associated C quality and nutrient availability in temperate and arctic rivers (Holmes et al., 2008; Wickland et al., 2012; Abbott et al., 2014; Shin et al., 2016). For example, Wickland et al. (2012) have pointed that DOC biodegradation was greatest during winter (35–53%), and decreased into spring (17–38%) and summer (3–36%) in the Yukong River and its tributaries in Alaska, USA. Moreover, the mechanisms underlying the seasonal patterns of DOC biodegradation are still inconclusive in these rivers, and may vary with DOC sources, chemical composition and background nutrient concentrations (Holmes et al., 2008; Wickland et al., 2012; Abbott et al., 2014; Hosen et al., 2014). Unfortunately, the temporal variations of DOC biodegradation in tropical and subtropical rivers have not been well studied. Considering the critical roles of riverine ecosystems in regulating C and nutrient cycles from regional to global scales, it is urgent to clarify the shifts in DOC biodegradation and its driving factors across seasons in the tropical and subtropical rivers. The Three Gorges Reservoir is built on the upper reach of the Yangzte River of China, and is regarded as one of the largest hydropower dams in the world. The Three Gorge Reservoir catchment is located in the subtropical East Asia summer monsoon region that is characterized by the distinctive dry season (from October to April) and wet season (from May to September) (Zhao et al., 2010). In our preliminary study, DOC biodegradation is believed to be limited by P availability in the river networks in the Three Gorges Reservoir region (Mao et al., 2017). However, the temporal variations of DOC biodegradation and its influencing factors are still unclear due to the lack of empirical studies, which could limit our full understanding of C budget in this catchment and even the Yangtze River. Here, we investigated DOC biodegradation, DOC, dissolved total nitrogen (DTN), and dissolved total phosphorus (DTP) concentrations, humification index (HIX), and fluorescence index (FI) in the dry and wet seasons in 57 rivers in the Three Gorges Reservoir catchment, China. The specific objectives were to (1) assess the temporal variations of DOC biodegradation using a laboratory incubation experiments, and (2) identify the possible mechanisms controlling DOC biodegradation across the two sampling seasons.
2. Materials and methods 2.1. Study sites This study was conducted in the Three Gorges Reservoir catchment (28°44′–31°40′N, 106°10′–111°10′E) located in south-central China. The Three Gorges Reservoir is a typical valley-type reservoir, and the total catchment area is approximately 56,000 km2 (Zhao et al., 2010). The water level (above sea level) fluctuates between 145 m and 175 m following the normal operation of the Three Gorges Dam in 2010. When the water level reaches 175 m, the surface area of the Three Gorges Reservoir is approximately 1084 km2 with 660 km in length. Mean annual temperature of the study sites is 15–19 °C, and
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mean annual precipitation is 1250 mm (70% falling in May– September) (Wu et al., 2004). 2.2. Sample collection and measurements In this study, water samples were collected from 57 tributaries of the Yangtze rivers in the dry season (from late October to early November 2015) and wet season (from late June to early July 2016) in the Three Gorges Reservoir catchment. During each sampling season, we collected one water sample per river, resulting in a total of 114 water samples. The selected rivers cover the majority of the tributaries of the Yangtze River in this region. The detailed descriptions of the sampling sites are shown in Fig. 1 and Supplementary material. In each river, three water samples were collected 10 cm below the water surface in the center of the river channel and then mixed to form a homogenized sample. In total, 2-L running water was sampled per river and stored in acid-washed plastic containers. Water samples were filtered with pre-combusted glass fiber filters (GF/F 47 mm, 0.7μm, Whatman) on the sampling day, stored in the dark at 4 °C in the refrigerator, and then transported on ice to the laboratory within five days of water collection (Vonk et al., 2015). DOC biodegradation experiment was started immediately when the water samples were transported to the laboratory, and the measurements of DOC, DTN, and DTP concentrations, and DOC fluorescence properties were completed within seven days of water collection. DOC concentration was measured by the high-temperature catalytic oxidation method on a total organic carbon analyzer (TOC-5000, Shimadzu, Japan), and DTN and DTP concentrations were measured by the hydrazine reduction method and the molybdenum blue method on a continuous-flow autoanalyzer (AA3, Seal Analytical, Germany) following peroxodisulfate oxidation, respectively (Ebina et al., 1983). The detection limits for DOC, DTN, and DTP concentrations were 4 μg L−1, 6 μg L−1, and 3 μg L−1, respectively. In this study, the stoichiometric ratios among DOC, DTN, and DTP are mass ratios. Fluorescence excitation-emission matrices (EEMs) were measured on the filtered river samples at room temperature using a Hitachi F7000 fluorescence spectrometer (Hitachi High Technologies, Japan). Meanwhile, a sample of Milli-Q deionized water was used as a blank. The fluorescence intensity was measured at excitation wavelengths ranging from 220 to 400 nm at 2-nm increments and at emission wavelengths ranging from 250 to 500 nm at 2-nm increments. When necessary, water samples were diluted to avoid inner filter effects. EEMs were corrected for instrument optics, inner filter corrected, Raman area normalized at excitation 350 nm, Raman normalized blank subtracted, and multiplied by the dilution factor, and were reported in Raman Units (O'Donnell et al., 2016). In this study, FI and HIX were used to describe DOC sources and chemical characteristics, respectively. FI is the ratio of the emission fluorescence intensities at 450 nm and 500 nm at the excitation wavelength 370 nm, and is used to identify the sources of DOC in aquatic ecosystems (McKnight et al., 2001). HIX is calculated as the ratio of the area under the emission spectra 435–480 nm divided by 300–445 nm at excitation wavelength 254 nm, which can assess the humification degree of DOC (Zsolnay et al., 1999; Fellman et al., 2010); humification is related to the increase in the aromatic character of the molecules and the possible increments in the conjunction degree in unsaturated aliphatic chains (Fuentes et al., 2006). DOC biodegradation was measured using a laboratory incubation method described by Wickland et al. (2012) and Vonk et al. (2015). Specifically, 50 mL of water was added to 250-mL glass bottles, and then the bottles were sealed and capped with Teflon-lined stoppers and crimp seals. We established five bottles for each water sample; three bottles were incubated at 20 °C in the dark to measure the biodegradability of DOC, and another two bottles were used to determine the initial dissolved inorganic C (DIC) concentration (Wickland et al., 2012). In addition, three bottles with 50 mL Milli-Q deionized water were included as references. Because 0.7-μm filter could permit sufficient microbes to
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Fig. 1. Location of the sampling site in the Three Gorges Reservoir Region, China.
pass through it (Vonk et al., 2015), we did not add inoculum to the water samples in this study. On days 2, 6, 12, 18, 30, and 42, approximately 10-mL headspace gas was sampled, and then CO2 concentration in the headspace gas was assessed on a gas chromatograph (Agilent 7890A, Agilent Technologies, USA). Following gas sampling, the bottles were refreshed with CO2-free air for 10 min and then sealed. During the incubation, we shook the water samples every two days to ensure aerobic conditions. On day 42, the final DIC concentration in the water samples was measured following CO2 analyses. DOC biodegradation was calculated based on the initial and final DIC contents in the water and the cumulative headspace CO2 production, and was expressed as the percent of the initial DOC concentration. 2.3. Statistical analyses For the selected 57 rivers, paired-t-test was used to examine the differences in water parameters between dry and wet seasons. Relationships between DOC biodegradation and the stoichiometric ratios of DOC, DTN, and DTP, or DOC fluorescence properties were tested with the nonlinear regression analyses. The statistical analyses were conducted using the SPSS statistical software (v. 13.0), and a statistical significant level of 0.05 was accepted. 3. Results DOC concentration did not differ between dry and wet seasons (p = 0.681; 12.1 and 12.4 mg L−1, respectively), whereas DTN (p = 0.026) and DTP (p b 0.001) concentrations were significantly higher in the wet season (4.16 mg L−1 and 99.9 μg L−1, respectively) than in the dry season (3.48 mg L−1 and 67.8 μg L−1, respectively) (Fig. 2). As a consequence, C:P (p b 0.001) and N:P (p b 0.001) ratios were significantly lower in the wet season (157 and 49.3, respectively) than in the dry season (293 and 91.8, respectively) (Fig. 2). However, there was no significant difference in C:N ratio between dry and wet seasons (p = 0.730).
DOC fluorescence properties varied significantly with sampling seasons (Table 1). Specifically, FI was significantly greater in the dry season than in the wet season (p b 0.001), while HIX exhibited a reverse seasonal change trend (p b 0.001, Table 1). DOC biodegradation showed no significant difference between dry and wet seasons (p = 0.951; 24.5% and 24.6%, respectively) (Table 1). However, the dynamics of cumulative CO2 production during 42-day incubation period differed across the two sampling seasons (Fig. 3). Cumulative CO2 production in the dry season (16.9%) was greater than that in the wet season (13.4%) in the first 18 days (all p b 0.001), whereas there was no significant difference in cumulative CO2 production between dry and wet seasons by the end of incubation (Fig. 3). When all data were pooled together, DOC biodegradation did not correlate significantly with C:N ratio, C:P ratio, N:P ratio, FI, and HIX (Figs. 4 and 5). However, DOC biodegradation negatively correlated with the initial C:P ratio (R2 = 0.749, p b 0.001), N:P ratio (R2 = 0.469, p b 0.001) and FI (R2 = 0.307, p b 0.001) in the dry season, but showed a negative relationship with HIX (R2 = 0.477, p b 0.001) in the wet season (Figs. 4 and 5). 4. Discussion In contrast to temperate and arctic rivers (Holmes et al., 2008; Wickland et al., 2012; Hosen et al., 2014), DOC biodegradation remained constant across the two sampling seasons in these subtropical rivers, although DTN and DTP concentrations and HIX in the wet season were greater than that in the dry season (Table 1 and Fig. 2). These inconsistences among the rivers might be caused by the spatial differences in seasonality of nutrient availability and initial chemical composition (Balcarczyk et al., 2009; Hosen et al., 2014). For example, DOC biodegradation was observed to be greater in the winter and early spring than the other seasons in arctic rivers as a result of high N availability and labile DOC chemical composition (Holmes et al., 2008; Mann et al., 2012; Wickland et al., 2012). In this study, DTN and DTP concentrations
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Fig. 2. Temporal variations of dissolved organic carbon (DOC), dissolved total nitrogen (DTN), and dissolved total phosphorus (DTP) concentrations and their ratios in subtropical rivers.
increased from dry season to wet season, but HIX exhibited an opposite seasonal change trend in these subtropical rivers. Abbott et al. (2014) observed that increased nutrient availability only enhanced labile DOC biodegradation, and did not affect recalcitrant DOC biodegradation in arctic rivers. Accordingly, one possible mechanism responsible for unchanged DOC biodegradation across the two sampling seasons was the counteractive effect between nutrient availability and DOC quality. Nevertheless, our finding clearly indicates that the seasonal patterns of DOC biodegradation in subtropical rivers differ with that in temperate and arctic rivers. Considering that DOC biodegradation is primarily driven by the aquatic heterotrophic microorganisms (Cole et al., 2007; Vonk et al., 2015), further studies regarding the temporal variations of microbial community structure and metabolic efficiency are needed to fully understanding of the unchanged DOC biodegradation across seasons in subtropical rivers. In subtropical rivers, the biodegradability of DOC is generally believed to be limited by P availability (Mao et al., 2017). However, we only observed the negative relationship between DOC biodegradation and DOC:DTP ratio or DTN:DTP ratio in the dry season (Fig. 2). Moreover, DOC biodegradation declined with elevating HIX in the wet season in these rivers (Fig. 3). In temperate rivers, Hosen et al. (2014) also found that DOC biodegradation negatively correlated with HIX only in spring and summer. These results confirmed that, despite unchanged DOC biodegradation, the key factors influencing DOC biodegradation might differ across seasons in riverine ecosystems. In the present study, such temporal shift in controls of DOC biodegradation might be caused by substantial differences in P availability and associated C:N:P stoichiometric ratios across the two sampling seasons (Abbott et al., 2014). In the wet season, P availability probably did not become a growth-limiting mineral nutrient for heterotrophic microorganisms due to the greater DTP concentration and associated lower DOC:DTP
ratio in subtropical rivers (Fig. 2). These indicated that, with increasing DTP concentration, the initial chemical composition would be an overriding driver of DOC biodegradation in subtropical rivers. In these subtropical rivers, FI declined from dry season to wet season, whereas HIX exhibited a reverse seasonal pattern (Table 1). In general, FI is used to distinguish DOC which is derived from terrestrial (low FI ~ 1.2) or microbial (high FI ~ 1.8) sources (McKnight et al., 2001; Huguet et al., 2009), and HIX is used as an indicator of the extent of humification of DOC, with higher values indicating an increasing degree of humification (Zsolnay et al., 1999; Fellman et al., 2010). These changes in fluorescence properties all point to seasonal shift in DOC sources and associated chemical composition in the subtropical rivers. Compared with wet season, the greater FI value (1.89) in the dry season indicated that DOC was primarily derived from extracellular release and leachate from aquatic bacteria and algae other than from terrestrial plant and soil organic matter (Fellman et al., 2010), and thus had a lower degree of humification or aromaticity (Balcarczyk et al., 2009). Indeed, the relative abundance of aromatic compounds or humic-like components in DOC was observed to be the highest during the wet
Table 1 Temporal variations of humification index (HIX), fluorescence index (FI), and dissolved organic carbon (DOC) biodegradation in subtropical rivers. Parameters
Dry season
Wet season
p value
FI HIX DOC biodegradation
1.89 (0.05) 1.68 (0.15) 24.5 (0.6)
1.63 (0.02) 3.96 (0.20) 24.6 (0.9)
b0.001 b0.001 0.951
Values are means and data in the brackets are standard error (n = 57).
Fig. 3. Cumulative CO2 production during 42-day incubations. The data represent the mean value, the error bars are the standard error (n = 57), and ns and *** indicate p N 0.05 and p b 0.001 between dry and wet seasons, respectively.
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Fig. 4. Relationships between dissolved organic matter (DOC) biodegradation and the initial stoichiometric ratios among dissolved organic carbon (DOC), dissolved total nitrogen (DTN), and dissolved total phosphorus (DTP).
season in tropical rivers (Seidel et al., 2016) and temperate rivers (Fellman et al., 2009). Both DTN and DTP concentrations were observed to be greater in the wet season than in the dry season, despite an unchanged DOC concentration across the two sampling seasons (Fig. 2). Previous studies also found elevated DTN, and DTP concentrations in the rivers during high rainfall in the subtropical East Asian monsoon region (Hao et al., 2017; Ran et al., 2017) and other regions (Cauwet and Sidorov, 1996; Parr et al., 2015). In this hilly region, high precipitation in the wet season probably increased N and P exports to rivers by enhanced surface runoff and leaching (Li et al., 2009; Li and Bush, 2015). Consequently, DTN and DTP concentrations were higher in the wet season than in the dry season in these rivers. In the riverine ecosystems, the amounts of DTN and DTP are the key nutrient elements influencing water chemistry and eutrophication (Hao et al., 2017; Ran et al., 2017). Therefore, these results would help to uncover the temporal variations of water quality in the subtropical rivers in the Three Gorges Reservoir area. In the Three Gorges Reservoir area, increased P loading to the rivers will be continued because of the extensive fertilizer use for maintaining crop yields (Ran et al., 2017). In this study, DOC biodegradation remained constant, although DTP increased by 50% from dry season to wet season (Table 1 and Fig. 2). This implies that, in the context of P eutrophication, microbial decomposition of DOC is constrained by the initial chemical composition, and DOC biodegradation may not be accelerated as previously predicted in subtropical rivers (Mao et al., 2017). The fate of DOC in river ecosystems is either transported downstream or emitted to the atmosphere as greenhouse gases through
microbial decomposition (Cole et al., 2007). Our results suggest that increased P loading would not cause substantial influences on DOC dynamics and alter regional C budget in the aquatic networks in the Three Gorges Reservoir area. Generally, labile DOC compounds are believed to have short turnover times ranging from hours to a few days, and thus DOC biodegradation is strongly recommended to be measured immediately following water sampling (Vonk et al., 2015; Kamjunke et al., 2017). In this study, we initiated the laboratory incubation experiment to assess DOC biodegradation after the filtered water samples were kept in darkness at a low temperature (4 °C) for approximately five days, because rapid incubation setup was not feasible at these remote field sites. Because of the lack of empirical studies, the effect of cold storage on aquatic microbial composition was still unknown. However, Lee et al. (2007) observed that soil microbial biomass and structure were unaffected by 28-day cold storage at 4 °C in forests and agricultural lands. Moreover, previous studies have reported that short-term cold storage at 4 °C had minor effects on DOC quantity and absorbance properties for freshwater samples (Peacock et al., 2015; Marlen and Dominik, 2018). Accordingly, we assumed that cold storage for about five days would produce negligible influences on DOC biodegradation, although this pretreatment method could underestimate DOC biodegradation. Nonetheless, the results of this study could be helpful for the assessment of temporal pattern of DOC biodegradation in the subtropical rivers of the Three Gorges Reservoir area. Meanwhile, we propose that additional studies are urgently needed to clarify the effects of water sample storage on DOC biodegradation in aquatic ecosystems.
Fig. 5. Relationships between dissolved organic matter (DOC) biodegradation and DOC fluorescence properties.
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Seidel, M., Dittmar, T., Ward, N.D., Krusche, A.V., Richey, J.E., Yager, P.L., Medeiros, P.M., 2016. Seasonal and spatial variability of dissolved organic matter composition in the lower Amazon River. Biogeochemistry 131, 281–302. Shin, Y., Lee, E.J., Jeon, Y.J., Hur, J., Oh, N.H., 2016. Hydrological changes of DOC composition and biodegradability of rivers in temperate monsoon climates. J. Hydrol. 540, 538–548. Volk, C.J., Volk, C.B., Kaplan, L.A., 1997. Chemical composition of biodegradable dissolved organic matter in streamwater. Limnol. Oceanogr. 42, 39–44. Vonk, J.E., Tank, S.E., Mann, P.J., Spencer, R.G.M., Treat, C.C., Striegl, R.G., Abbott, B.W., Wickland, K.P., 2015. Biodegradability of dissolved organic carbon in permafrost soils and aquatic systems: a meta-analysis. Biogeosciences 12, 6915–6930. Wickland, K.P., Aiken, G.R., Butler, K., Dornblaser, M.M., Spencer, R.G.M., Striegl, R.G., 2012. 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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Temporal controls on dissolved organic carbon biodegradation in subtropical rivers: Initial chemical composition versus stoichiometry Rong Mao a,b, Siyue Li a,⁎ a b
Research Center for Eco-hydrology, Chongqing Institute of Green and Intelligent Technology, Chinese Academy of Sciences, Chongqing 400714, China Key Laboratory of Silviculture, Co-Innovation Center of Jiangxi Typical Trees Cultivation and Utilization, College of Forestry, Jiangxi Agricultural University, Nanchang 330045, China
H I G H L I G H T S
G R A P H I C A L
A B S T R A C T
• Greater DTN and DTP concentrations were observed in wet season than in dry season. • DOM had greater HIX, and lower FI values in wet season than in dry season. • DOM biodegradation remained unchanged across seasons. • DOM biodegradation negatively related to DOC:DTP and DTN:DTP ratios in dry season. • DOM biodegradation negatively correlated with HIX in wet season.
a r t i c l e
i n f o
Article history: Received 19 July 2018 Received in revised form 12 October 2018 Accepted 15 October 2018 Available online 16 October 2018 Editor: Kevin V. Thomas Keywords: Biodegradability Carbon dioxide production Nutrient availability Riverine C cycle The Three Gorges Reservoir area
a b s t r a c t Dissolved organic carbon (DOC) plays an indispensable role in biogeochemical cycles and ecosystem services in rivers. However, little is known about the seasonal variations of DOC biodegradation in subtropical rivers. Here, we investigated the concentrations of DOC, dissolved total nitrogen (DTN), and dissolved total phosphorus (DTP), humification index (HIX), fluorescence index (FI), and DOC biodegradation in 57 rivers in the dry and wet seasons in the Three Gorges Reservoir area, China, and the aims were to clarify the temporal changes in DOC biodegradation and its driving factors in these subtropical rivers. Compared with dry season, DTN and DTP concentrations, and HIX value were greater, and FI value was lower in the wet season. However, DOC biodegradation remained unchanged across the two sampling seasons. Further, DOC biodegradation negatively correlated with DOC:DTP ratio, DTN:DTP ratio, and FI in the dry season, but only with HIX in the wet season. These findings emphasis that, despite unchanged DOC biodegradation, the key factors driving DOC biodegradation shift from C: N:P stoichiometry in the dry season to initial chemical composition in the wet season in subtropical rivers. Our results regarding the temporal patterns of DOC biodegradation and the underlying mechanisms bear important implications for a better understanding of C dynamics in subtropical river ecosystems. © 2018 Elsevier B.V. All rights reserved.
1. Introduction
⁎ Corresponding author at: Chongqing Institute of Green and Intelligent Technology (CIGIT), Chinese Academy of Sciences (CAS), 266, Fangzheng Avenue, Shuitu High-tech Park, Beibei, Chongqing 400714, China. E-mail address: [email protected] (S. Li).
https://doi.org/10.1016/j.scitotenv.2018.10.220 0048-9697/© 2018 Elsevier B.V. All rights reserved.
Riverine ecosystems are a fundamental component of global carbon (C) cycle, because they are important agents in modulating the transfer of organic matter from the lands to the oceans, and act as a substantial source of greenhouse gases to the atmosphere at local to global scales (Cole et al., 2007; Aufdenkampe et al., 2011; Raymond et al., 2013). In
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these ecosystems, dissolved organic carbon (DOC) is the largest pools of transported organic C, and provides the main substrates for aquatic microorganisms, especially heterotrophic bacteria (Volk et al., 1997; Balcarczyk et al., 2009; Schiller et al., 2017). Accordingly, microbial process of DOC, i.e., DOC biodegradation, accounts for a large proportion of aquatic metabolism, and is key to C cycling and greenhouse gas fluxes in riverine ecosystems (Judd et al., 2006; Cole et al., 2007; Lambert et al., 2015). In rivers, DOC is primarily derived from autochthonous and terrigenous organic matter, and is a highly heterogeneous pool of a vast diversity of soluble organic compounds with varying lability (Hosen et al., 2014). Thus, the biodegradability of DOC is largely influenced by the intrinsic properties, such as the initial chemical composition (Balcarczyk et al., 2009; Mann et al., 2012) and C:nutrient stoichiometry (Wickland et al., 2012; Mao et al., 2017). In general, DOC biodegradation differs across seasons because of the marked differences in DOC sources and associated C quality and nutrient availability in temperate and arctic rivers (Holmes et al., 2008; Wickland et al., 2012; Abbott et al., 2014; Shin et al., 2016). For example, Wickland et al. (2012) have pointed that DOC biodegradation was greatest during winter (35–53%), and decreased into spring (17–38%) and summer (3–36%) in the Yukong River and its tributaries in Alaska, USA. Moreover, the mechanisms underlying the seasonal patterns of DOC biodegradation are still inconclusive in these rivers, and may vary with DOC sources, chemical composition and background nutrient concentrations (Holmes et al., 2008; Wickland et al., 2012; Abbott et al., 2014; Hosen et al., 2014). Unfortunately, the temporal variations of DOC biodegradation in tropical and subtropical rivers have not been well studied. Considering the critical roles of riverine ecosystems in regulating C and nutrient cycles from regional to global scales, it is urgent to clarify the shifts in DOC biodegradation and its driving factors across seasons in the tropical and subtropical rivers. The Three Gorges Reservoir is built on the upper reach of the Yangzte River of China, and is regarded as one of the largest hydropower dams in the world. The Three Gorge Reservoir catchment is located in the subtropical East Asia summer monsoon region that is characterized by the distinctive dry season (from October to April) and wet season (from May to September) (Zhao et al., 2010). In our preliminary study, DOC biodegradation is believed to be limited by P availability in the river networks in the Three Gorges Reservoir region (Mao et al., 2017). However, the temporal variations of DOC biodegradation and its influencing factors are still unclear due to the lack of empirical studies, which could limit our full understanding of C budget in this catchment and even the Yangtze River. Here, we investigated DOC biodegradation, DOC, dissolved total nitrogen (DTN), and dissolved total phosphorus (DTP) concentrations, humification index (HIX), and fluorescence index (FI) in the dry and wet seasons in 57 rivers in the Three Gorges Reservoir catchment, China. The specific objectives were to (1) assess the temporal variations of DOC biodegradation using a laboratory incubation experiments, and (2) identify the possible mechanisms controlling DOC biodegradation across the two sampling seasons.
2. Materials and methods 2.1. Study sites This study was conducted in the Three Gorges Reservoir catchment (28°44′–31°40′N, 106°10′–111°10′E) located in south-central China. The Three Gorges Reservoir is a typical valley-type reservoir, and the total catchment area is approximately 56,000 km2 (Zhao et al., 2010). The water level (above sea level) fluctuates between 145 m and 175 m following the normal operation of the Three Gorges Dam in 2010. When the water level reaches 175 m, the surface area of the Three Gorges Reservoir is approximately 1084 km2 with 660 km in length. Mean annual temperature of the study sites is 15–19 °C, and
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mean annual precipitation is 1250 mm (70% falling in May– September) (Wu et al., 2004). 2.2. Sample collection and measurements In this study, water samples were collected from 57 tributaries of the Yangtze rivers in the dry season (from late October to early November 2015) and wet season (from late June to early July 2016) in the Three Gorges Reservoir catchment. During each sampling season, we collected one water sample per river, resulting in a total of 114 water samples. The selected rivers cover the majority of the tributaries of the Yangtze River in this region. The detailed descriptions of the sampling sites are shown in Fig. 1 and Supplementary material. In each river, three water samples were collected 10 cm below the water surface in the center of the river channel and then mixed to form a homogenized sample. In total, 2-L running water was sampled per river and stored in acid-washed plastic containers. Water samples were filtered with pre-combusted glass fiber filters (GF/F 47 mm, 0.7μm, Whatman) on the sampling day, stored in the dark at 4 °C in the refrigerator, and then transported on ice to the laboratory within five days of water collection (Vonk et al., 2015). DOC biodegradation experiment was started immediately when the water samples were transported to the laboratory, and the measurements of DOC, DTN, and DTP concentrations, and DOC fluorescence properties were completed within seven days of water collection. DOC concentration was measured by the high-temperature catalytic oxidation method on a total organic carbon analyzer (TOC-5000, Shimadzu, Japan), and DTN and DTP concentrations were measured by the hydrazine reduction method and the molybdenum blue method on a continuous-flow autoanalyzer (AA3, Seal Analytical, Germany) following peroxodisulfate oxidation, respectively (Ebina et al., 1983). The detection limits for DOC, DTN, and DTP concentrations were 4 μg L−1, 6 μg L−1, and 3 μg L−1, respectively. In this study, the stoichiometric ratios among DOC, DTN, and DTP are mass ratios. Fluorescence excitation-emission matrices (EEMs) were measured on the filtered river samples at room temperature using a Hitachi F7000 fluorescence spectrometer (Hitachi High Technologies, Japan). Meanwhile, a sample of Milli-Q deionized water was used as a blank. The fluorescence intensity was measured at excitation wavelengths ranging from 220 to 400 nm at 2-nm increments and at emission wavelengths ranging from 250 to 500 nm at 2-nm increments. When necessary, water samples were diluted to avoid inner filter effects. EEMs were corrected for instrument optics, inner filter corrected, Raman area normalized at excitation 350 nm, Raman normalized blank subtracted, and multiplied by the dilution factor, and were reported in Raman Units (O'Donnell et al., 2016). In this study, FI and HIX were used to describe DOC sources and chemical characteristics, respectively. FI is the ratio of the emission fluorescence intensities at 450 nm and 500 nm at the excitation wavelength 370 nm, and is used to identify the sources of DOC in aquatic ecosystems (McKnight et al., 2001). HIX is calculated as the ratio of the area under the emission spectra 435–480 nm divided by 300–445 nm at excitation wavelength 254 nm, which can assess the humification degree of DOC (Zsolnay et al., 1999; Fellman et al., 2010); humification is related to the increase in the aromatic character of the molecules and the possible increments in the conjunction degree in unsaturated aliphatic chains (Fuentes et al., 2006). DOC biodegradation was measured using a laboratory incubation method described by Wickland et al. (2012) and Vonk et al. (2015). Specifically, 50 mL of water was added to 250-mL glass bottles, and then the bottles were sealed and capped with Teflon-lined stoppers and crimp seals. We established five bottles for each water sample; three bottles were incubated at 20 °C in the dark to measure the biodegradability of DOC, and another two bottles were used to determine the initial dissolved inorganic C (DIC) concentration (Wickland et al., 2012). In addition, three bottles with 50 mL Milli-Q deionized water were included as references. Because 0.7-μm filter could permit sufficient microbes to
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Fig. 1. Location of the sampling site in the Three Gorges Reservoir Region, China.
pass through it (Vonk et al., 2015), we did not add inoculum to the water samples in this study. On days 2, 6, 12, 18, 30, and 42, approximately 10-mL headspace gas was sampled, and then CO2 concentration in the headspace gas was assessed on a gas chromatograph (Agilent 7890A, Agilent Technologies, USA). Following gas sampling, the bottles were refreshed with CO2-free air for 10 min and then sealed. During the incubation, we shook the water samples every two days to ensure aerobic conditions. On day 42, the final DIC concentration in the water samples was measured following CO2 analyses. DOC biodegradation was calculated based on the initial and final DIC contents in the water and the cumulative headspace CO2 production, and was expressed as the percent of the initial DOC concentration. 2.3. Statistical analyses For the selected 57 rivers, paired-t-test was used to examine the differences in water parameters between dry and wet seasons. Relationships between DOC biodegradation and the stoichiometric ratios of DOC, DTN, and DTP, or DOC fluorescence properties were tested with the nonlinear regression analyses. The statistical analyses were conducted using the SPSS statistical software (v. 13.0), and a statistical significant level of 0.05 was accepted. 3. Results DOC concentration did not differ between dry and wet seasons (p = 0.681; 12.1 and 12.4 mg L−1, respectively), whereas DTN (p = 0.026) and DTP (p b 0.001) concentrations were significantly higher in the wet season (4.16 mg L−1 and 99.9 μg L−1, respectively) than in the dry season (3.48 mg L−1 and 67.8 μg L−1, respectively) (Fig. 2). As a consequence, C:P (p b 0.001) and N:P (p b 0.001) ratios were significantly lower in the wet season (157 and 49.3, respectively) than in the dry season (293 and 91.8, respectively) (Fig. 2). However, there was no significant difference in C:N ratio between dry and wet seasons (p = 0.730).
DOC fluorescence properties varied significantly with sampling seasons (Table 1). Specifically, FI was significantly greater in the dry season than in the wet season (p b 0.001), while HIX exhibited a reverse seasonal change trend (p b 0.001, Table 1). DOC biodegradation showed no significant difference between dry and wet seasons (p = 0.951; 24.5% and 24.6%, respectively) (Table 1). However, the dynamics of cumulative CO2 production during 42-day incubation period differed across the two sampling seasons (Fig. 3). Cumulative CO2 production in the dry season (16.9%) was greater than that in the wet season (13.4%) in the first 18 days (all p b 0.001), whereas there was no significant difference in cumulative CO2 production between dry and wet seasons by the end of incubation (Fig. 3). When all data were pooled together, DOC biodegradation did not correlate significantly with C:N ratio, C:P ratio, N:P ratio, FI, and HIX (Figs. 4 and 5). However, DOC biodegradation negatively correlated with the initial C:P ratio (R2 = 0.749, p b 0.001), N:P ratio (R2 = 0.469, p b 0.001) and FI (R2 = 0.307, p b 0.001) in the dry season, but showed a negative relationship with HIX (R2 = 0.477, p b 0.001) in the wet season (Figs. 4 and 5). 4. Discussion In contrast to temperate and arctic rivers (Holmes et al., 2008; Wickland et al., 2012; Hosen et al., 2014), DOC biodegradation remained constant across the two sampling seasons in these subtropical rivers, although DTN and DTP concentrations and HIX in the wet season were greater than that in the dry season (Table 1 and Fig. 2). These inconsistences among the rivers might be caused by the spatial differences in seasonality of nutrient availability and initial chemical composition (Balcarczyk et al., 2009; Hosen et al., 2014). For example, DOC biodegradation was observed to be greater in the winter and early spring than the other seasons in arctic rivers as a result of high N availability and labile DOC chemical composition (Holmes et al., 2008; Mann et al., 2012; Wickland et al., 2012). In this study, DTN and DTP concentrations
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Fig. 2. Temporal variations of dissolved organic carbon (DOC), dissolved total nitrogen (DTN), and dissolved total phosphorus (DTP) concentrations and their ratios in subtropical rivers.
increased from dry season to wet season, but HIX exhibited an opposite seasonal change trend in these subtropical rivers. Abbott et al. (2014) observed that increased nutrient availability only enhanced labile DOC biodegradation, and did not affect recalcitrant DOC biodegradation in arctic rivers. Accordingly, one possible mechanism responsible for unchanged DOC biodegradation across the two sampling seasons was the counteractive effect between nutrient availability and DOC quality. Nevertheless, our finding clearly indicates that the seasonal patterns of DOC biodegradation in subtropical rivers differ with that in temperate and arctic rivers. Considering that DOC biodegradation is primarily driven by the aquatic heterotrophic microorganisms (Cole et al., 2007; Vonk et al., 2015), further studies regarding the temporal variations of microbial community structure and metabolic efficiency are needed to fully understanding of the unchanged DOC biodegradation across seasons in subtropical rivers. In subtropical rivers, the biodegradability of DOC is generally believed to be limited by P availability (Mao et al., 2017). However, we only observed the negative relationship between DOC biodegradation and DOC:DTP ratio or DTN:DTP ratio in the dry season (Fig. 2). Moreover, DOC biodegradation declined with elevating HIX in the wet season in these rivers (Fig. 3). In temperate rivers, Hosen et al. (2014) also found that DOC biodegradation negatively correlated with HIX only in spring and summer. These results confirmed that, despite unchanged DOC biodegradation, the key factors influencing DOC biodegradation might differ across seasons in riverine ecosystems. In the present study, such temporal shift in controls of DOC biodegradation might be caused by substantial differences in P availability and associated C:N:P stoichiometric ratios across the two sampling seasons (Abbott et al., 2014). In the wet season, P availability probably did not become a growth-limiting mineral nutrient for heterotrophic microorganisms due to the greater DTP concentration and associated lower DOC:DTP
ratio in subtropical rivers (Fig. 2). These indicated that, with increasing DTP concentration, the initial chemical composition would be an overriding driver of DOC biodegradation in subtropical rivers. In these subtropical rivers, FI declined from dry season to wet season, whereas HIX exhibited a reverse seasonal pattern (Table 1). In general, FI is used to distinguish DOC which is derived from terrestrial (low FI ~ 1.2) or microbial (high FI ~ 1.8) sources (McKnight et al., 2001; Huguet et al., 2009), and HIX is used as an indicator of the extent of humification of DOC, with higher values indicating an increasing degree of humification (Zsolnay et al., 1999; Fellman et al., 2010). These changes in fluorescence properties all point to seasonal shift in DOC sources and associated chemical composition in the subtropical rivers. Compared with wet season, the greater FI value (1.89) in the dry season indicated that DOC was primarily derived from extracellular release and leachate from aquatic bacteria and algae other than from terrestrial plant and soil organic matter (Fellman et al., 2010), and thus had a lower degree of humification or aromaticity (Balcarczyk et al., 2009). Indeed, the relative abundance of aromatic compounds or humic-like components in DOC was observed to be the highest during the wet
Table 1 Temporal variations of humification index (HIX), fluorescence index (FI), and dissolved organic carbon (DOC) biodegradation in subtropical rivers. Parameters
Dry season
Wet season
p value
FI HIX DOC biodegradation
1.89 (0.05) 1.68 (0.15) 24.5 (0.6)
1.63 (0.02) 3.96 (0.20) 24.6 (0.9)
b0.001 b0.001 0.951
Values are means and data in the brackets are standard error (n = 57).
Fig. 3. Cumulative CO2 production during 42-day incubations. The data represent the mean value, the error bars are the standard error (n = 57), and ns and *** indicate p N 0.05 and p b 0.001 between dry and wet seasons, respectively.
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Fig. 4. Relationships between dissolved organic matter (DOC) biodegradation and the initial stoichiometric ratios among dissolved organic carbon (DOC), dissolved total nitrogen (DTN), and dissolved total phosphorus (DTP).
season in tropical rivers (Seidel et al., 2016) and temperate rivers (Fellman et al., 2009). Both DTN and DTP concentrations were observed to be greater in the wet season than in the dry season, despite an unchanged DOC concentration across the two sampling seasons (Fig. 2). Previous studies also found elevated DTN, and DTP concentrations in the rivers during high rainfall in the subtropical East Asian monsoon region (Hao et al., 2017; Ran et al., 2017) and other regions (Cauwet and Sidorov, 1996; Parr et al., 2015). In this hilly region, high precipitation in the wet season probably increased N and P exports to rivers by enhanced surface runoff and leaching (Li et al., 2009; Li and Bush, 2015). Consequently, DTN and DTP concentrations were higher in the wet season than in the dry season in these rivers. In the riverine ecosystems, the amounts of DTN and DTP are the key nutrient elements influencing water chemistry and eutrophication (Hao et al., 2017; Ran et al., 2017). Therefore, these results would help to uncover the temporal variations of water quality in the subtropical rivers in the Three Gorges Reservoir area. In the Three Gorges Reservoir area, increased P loading to the rivers will be continued because of the extensive fertilizer use for maintaining crop yields (Ran et al., 2017). In this study, DOC biodegradation remained constant, although DTP increased by 50% from dry season to wet season (Table 1 and Fig. 2). This implies that, in the context of P eutrophication, microbial decomposition of DOC is constrained by the initial chemical composition, and DOC biodegradation may not be accelerated as previously predicted in subtropical rivers (Mao et al., 2017). The fate of DOC in river ecosystems is either transported downstream or emitted to the atmosphere as greenhouse gases through
microbial decomposition (Cole et al., 2007). Our results suggest that increased P loading would not cause substantial influences on DOC dynamics and alter regional C budget in the aquatic networks in the Three Gorges Reservoir area. Generally, labile DOC compounds are believed to have short turnover times ranging from hours to a few days, and thus DOC biodegradation is strongly recommended to be measured immediately following water sampling (Vonk et al., 2015; Kamjunke et al., 2017). In this study, we initiated the laboratory incubation experiment to assess DOC biodegradation after the filtered water samples were kept in darkness at a low temperature (4 °C) for approximately five days, because rapid incubation setup was not feasible at these remote field sites. Because of the lack of empirical studies, the effect of cold storage on aquatic microbial composition was still unknown. However, Lee et al. (2007) observed that soil microbial biomass and structure were unaffected by 28-day cold storage at 4 °C in forests and agricultural lands. Moreover, previous studies have reported that short-term cold storage at 4 °C had minor effects on DOC quantity and absorbance properties for freshwater samples (Peacock et al., 2015; Marlen and Dominik, 2018). Accordingly, we assumed that cold storage for about five days would produce negligible influences on DOC biodegradation, although this pretreatment method could underestimate DOC biodegradation. Nonetheless, the results of this study could be helpful for the assessment of temporal pattern of DOC biodegradation in the subtropical rivers of the Three Gorges Reservoir area. Meanwhile, we propose that additional studies are urgently needed to clarify the effects of water sample storage on DOC biodegradation in aquatic ecosystems.
Fig. 5. Relationships between dissolved organic matter (DOC) biodegradation and DOC fluorescence properties.
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5. Conclusions In summary, DOC biodegradation remained unchanged across two sampling seasons, although DOC chemical composition and P availability exhibited substantial temporal variations in the fluvial networks of the Three Gorges Reservoir area, China. However, the key factors driving DOC biodegradation differed between dry and wet seasons in these subtropical rivers. Remarkably, DOC biodegradation was primarily controlled by the C:N:P stoichiometry in the dry season, and by the humification degree in the wet season. Therefore, our results could have important implications for the better understanding and prediction of C dynamics in subtropical river networks in the Three Gorges Reservoir area. Supplementary data to this article can be found online at https://doi. org/10.1016/j.scitotenv.2018.10.220. Acknowledgements This study was funded by the “Hundred Talent Program” of the Chinese Academy of Sciences (R53A362Z10, granted to Dr. Siyue Li) and the National Natural Science Foundation of China (NSFC Grant No. 31670473). We thank the editor Kevin Thomas and two anonymous reviewers for their helpful suggestions in improving the earlier draft of the manuscript. References Abbott, B.W., Larouche, J.R., Jones Jr., J.B., Bowden, W.B., Balser, A.W., 2014. Elevated dissolved organic carbon biodegradability from thawing and collapsing permafrost. J. Geophys. Res. 119, 2049–2063. Aufdenkampe, A.K., Mayorga, E., Raymond, P.A., Melack, J.M., Doney, S.C., Alin, S.R., Aalto, R.E., Yoo, K., 2011. Riverine coupling of biogeochemical cycles between land, oceans, and atmosphere. Front. Ecol. Environ. 9, 53–60. Balcarczyk, K.L., Jones Jr., J.B., Jaffe, R., Maie, N., 2009. Stream dissolved organic matter bioavailability and composition in watersheds underlain with discontinuous permafrost. Biogeochemistry 94, 255–270. Cauwet, G., Sidorov, I., 1996. The biogeochemistry of Lena river: organic carbon and nutrients distribution. Mar. Chem. 53, 211–227. Cole, J.J., Prairie, Y.T., Caraco, N.F., McDowell, W.H., Tranvik, L.J., Striegl, R.G., Duarte, C.M., Kortelainen, P., Downing, J.A., Middelburg, J.J., Melack, J., 2007. Plumbing the global carbon cycle: integrating inland waters into terrestrial carbon budget. Ecosystems 10, 171–184. Ebina, J., Tsutsui, T., Shirai, T., 1983. Simultaneous determination of total nitrogen and total phosphorus in water using peroxodisulfate oxidation. Water Res. 17, 1721–1726. Fellman, J.B., Hood, E., Edwards, R.T., D'Amore, D.V., 2009. Changes in the concentration, biodegradability, and fluorescent properties of dissolved organic matter during stormflows in coastal temperate watersheds. J. Geophys. Res. 114, G01021. Fellman, J.B., Hood, E., Spencer, R.G.M., 2010. Fluorescence spectroscopy opens new windows into dissolved organic matter dynamics in freshwater ecosystems: a review. Limnol. Oceanogr. 55, 2452–2462. Fuentes, M., González-Gaitano, G., García-Mina, J.M., 2006. The usefulness of UV-visible and fluorescence spectroscopies to study the chemical nature of humic substances from soils and composts. Org. Geochem. 37, 1949–1959. Hao, Z., Gao, Y., Yang, T., 2017. Seasonal variation of DOC and associated stoichiometry for the freshwater ecosystem in the subtropical watershed: indicating the optimal C:N:P ratio. J. Hydrol. 78, 37–47. Holmes, R.M., McClelland, J.W., Raymond, P.A., Frazer, B.B., Peterson, B.J., Stieglitz, M., 2008. Lability of DOC transported by Alaskan rivers to the Arctic Ocean. Geophys. Res. Lett. 35, L03402. Hosen, J.D., McDonough, O.T., Febria, C.M., Palmer, M.A., 2014. Dissolved organic matter quality and bioavailability changes across an urbanization gradient in headwater streams. Environ. Sci. Technol. 48, 7817–7824. Huguet, A., Vacher, L., Relexans, S., Saubusse, S., Froidefond, J.M., Parlanti, E., 2009. Properties of fluorescent dissolved organic matter in the Gironde Estuary. Org. Geochem. 40, 706–719.
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