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Temperature sensitivity of biodegradable dissolved organic carbon increases with elevating humification degree in subtropical rivers
Science of the Total Environment 635 (2018) 1367–1371
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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Short Communication
Temperature sensitivity of biodegradable dissolved organic carbon increases with elevating humification degree in subtropical rivers Rong Mao, Si-Yue Li ⁎ The Three Gorges Institute of Ecological Environment, Chongqing Institute of Green and Intelligent Technology, Chinese Academy of Sciences, Chongqing 400714, China
H I G H L I G H T S • The Q10 values of BDOC were determined in the Three Gorges Reservoir river networks. • Approximately two-fold variations in Q10 value of BDOC were observed. • Q10 elevated with increasing humification degree, but decreased with increasing pH. • DOC quality and pH are powerful predictors of Q10 of BDOC in subtropical rivers. • C quality-temperature hypothesis can be applied to BDOC in subtropical rivers.
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Article history: Received 10 February 2018 Received in revised form 19 April 2018 Accepted 19 April 2018 Available online xxxx Editor: José Virgílio Cruz Keywords: Carbon cycle Carbon quality-temperature hypothesis Climate warming Inland waters Q10 value
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a b s t r a c t Biodegradable dissolved organic carbon (BDOC) plays a key role in C cycle in inland waters. However, the magnitude of temperature sensitivity (Q10 value) of BDOC is still unclear, and the effect of DOC quality on Q10 value of BDOC is not well verified in these aquatic systems. Here, we used a laboratory incubation experiment to determine the Q10 value of BDOC in 57 rivers in the Three Gorges Reservoir area, China, and then tested whether C quality-temperature hypothesis could be applied to BDOC in inland waters. We observed approximately twofold variations in Q10 values of BDOC (1.42–2.67) in these rivers. Moreover, the tight positive relationship between the Q10 values of BDOC and DOC humification index indicated the applicability of C quality-temperature hypothesis in subtropical rivers. In addition, the Q10 values of BDOC exhibited a negative relationship with pH. These findings suggest that DOC quality and pH are powerful predictors of temperature sensitivity of BDOC in subtropical rivers. In conclusion, our results would help to improve the C models and predict the feedback between climate warming and C dynamics in inland waters. © 2018 Elsevier B.V. All rights reserved.
1. Introduction Inland waters are an indispensable component of global carbon (C) cycle because of their critical roles in transporting C from land to ⁎ 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.-Y. Li).
https://doi.org/10.1016/j.scitotenv.2018.04.256 0048-9697/© 2018 Elsevier B.V. All rights reserved.
ocean and regulating atmospheric greenhouse gas concentrations (Cole et al., 2007; Raymond et al., 2013). In these aquatic systems, dissolved organic C (DOC) is the dominant form of organic C in the water column and plays an essential part in modulating C dynamics from local to global scales (Kellerman et al., 2015; Schiller et al., 2017). Generally, the quantity and quality of DOC are largely controlled by the processes of biodegradation and photodegradation in the aquatic environments (Moran and Zepp, 1997; Catalán et al., 2016). Both of these processes can convert DOC to inorganic compounds or result in a shift
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in DOC chemical composition (Moran et al., 2000; Hansen et al., 2016), probably exerting a remarkable impact on the biological utilization and fate of DOC in inland waters. In inland waters, DOC acts as the main source of substrates for aquatic heterotrophic microorganisms (Schiller et al., 2017). Thus, biodegradable DOC (BDOC) is of great importance to the production of carbon dioxide and methane and the amount and composition of DOC in these aquatic systems (Moran et al., 2000; Catalán et al., 2016; Hansen et al., 2016). In general, BDOC is profoundly influenced by a great variety of factors, such as initial chemical composition (Kalbitz et al., 2003; Kellerman et al., 2015), nutrient availability (Wickland et al., 2012; Mao et al., 2017), water retention time (Catalán et al., 2016), and climate conditions (Wickland et al., 2012). Any changes in these factors would result in the substantial variation of BDOC, which may produce a marked influence on organic C transportation and transformation in inland waters. In the recent decades, the Earth's climate has dramatically warmed, and this trend will be continuing as a consequence of rising concentrations of greenhouse gases in the atmosphere (IPCC, 2015). Consequently, climate warming inevitably leads to a notable increase in mean water temperature in inland aquatic ecosystems (van Vliet et al., 2011). Considering that most inland waters are net heterotrophic (Shah et al., 2017), elevated temperature is predicted to enhance BDOC through stimulated aquatic microbial growth and metabolic activity (Brown et al., 2004). Generally, temperature sensitivity (commonly expressed as Q10, indicating the organic C mineralization rate changes with a 10 °C rise in temperature) of BDOC is assumed to be 2.0 (Catalán et al., 2016). However, previous studies have shown that Q10 values are not constant across different terrestrial ecosystems (Davidson and Janssens, 2006; Lützow and Kögel-Knabner, 2009). Unfortunately, the magnitudes of Q10 values of BDOC remain uncertain in inland waters due to the lack of empirical studies. In general, Q10 values of organic C decomposition vary with the intrinsic organic C quality (Hartley and Ineson, 2008; Li et al., 2017), microbial community composition (Davidson and Janssens, 2006), pH (Li et al., 2017), and nutrient availability (Davidson and Janssens, 2006; Sihi et al., 2016) in terrestrial ecosystems. Among them, the intrinsic organic C quality is regarded as one of the most important factors controlling Q10 values, because organic C often consists of different C component with various activation energy (Hartley and Ineson, 2008; Davidson and Janssens, 2006). Recalcitrant organic C fraction containing more biochemically complex compounds has greater activation energy than labile organic C fraction, and thus decomposes slower (Davidson and Janssens, 2006; Lützow and Kögel-Knabner, 2009). According to the Arrhenius equation, organic C decomposition reaction with lower activation energy should have lower Q10 values (Davidson and Janssens, 2006; Conant et al., 2011). Accordingly, temperature sensitivity of organic C decomposition should increase with the substrate recalcitrance (i.e., C quality-temperature hypothesis) (Bosatta and Ågren, 1999). Indeed, previous studies have documented that recalcitrant soil organic C fraction has a higher temperature sensitivity than labile soil organic C fraction in most terrestrial ecosystems (e.g. Fierer et al., 2005; Hartley and Ineson, 2008; Sihi et al., 2016). Moreover, Shah et al. (2017), synthesizing 1025 records of litter decomposition in streams and rivers, have observed that temperature sensitivity of litter decomposition increased with decreasing substrate quality. However, whether this hypothesis can be applied to BDOC is still unclear in inland waters. Therefore, knowledge about the relationship between DOC quality and Q10 values of BDOC will help to accurately develop C models and understand C dynamics in inland waters in the context of global warming. In this study, we obtained water samples from 57 rivers from late June to early July in the Three Gorges Reservoir area, China, and then measure the concentrations of DOC, dissolved bound nitrogen (DNb), − NH+ 4 -N, NO3 -N, dissolved inorganic N (DIN), dissolved organic N (DON), and dissolved total phosphorus (DTP), pH, DOC humification
index, and BDOC at both 20 °C and 30 °C in these waters. In the previous studies, DOC humification index related positively to the abundances of humic-like component (Williams et al., 2010) and polyphenol-like components with H/C ratios b 1 and O/C ratios N 0.6 (Dadi et al., 2017), and the aromatic character of the moleculars (Fuentes et al., 2006), and was found to be negatively correlated with BDOC (Kalbitz et al., 2003). Therefore, we used humification index to indicate DOC quality; DOC with a greater value of humification index represents a lower DOC quality, and thus is more resistance to biodegradation. The specific objectives of this study were to: (1) clarify the Q10 values of BDOC in these subtropical rivers, and (2) test the applicability of C quality-temperature hypothesis to BDOC in inland waters. 2. Materials and methods 2.1. Site description This study was performed in the Three Gorges Reservoir area (28°44′–31°40′N, 106°10′–111°10′E), China. The Three Gorges Reservoir lies in the upper reach of Yangtze River, and the water level periodically fluctuates from 145 m in summer to 175 m in winter. The study site belongs to humid subtropical monsoon climate. Mean annual temperature is 16.5–19.0 °C and monthly mean temperature ranges from 3.4–7.2 °C in January to 28.0–30.0 °C in July. Mean annual precipitation is 1250 mm, 70% of which falls between May and September (Li et al., 2018). 2.2. Sample collection and measurement From late June to early July 2016, we collected water samples from 57 rivers, which represented the majority of rivers in the Three Gorges Reservoir area (Fig. 1 and Supplementary material). In each river, running surface water (10 cm depth) was sampled in the center of the river channel using acid-washed plastic containers, filtered with Whatman GF/F glass fiber filters (0.7 μm pore size) within 12 h, and then stored in the dark (4 °C) until analysis (b120 h). For all water samples, DOC concentration was analyzed by the high temperature combustion method on a total organic carbon analyzer (TOC-5000, Shimadzu, Japan), DNb and DTP concentrations were determined by the hydrazine sulphate spectrophometric method and ammonium molybdate spectrophometric method on a continuous-flow autoanalyzer (AA3, Seal Analytical, Germany) after alkaline peroxodisulfate digestion − (Ebina et al., 1983), respectively, NH+ 4 -N and NO3 -N concentrations were measured using the sodium salicylate sodium hypochlorite method and the hydrazine sulphate spectrophometric method on a continuous-flow autoanalyzer, respectively, and pH was assessed by a HACH portable pH meter. DIN concentration was the sum of NH+ 4 -N and NO− 3 -N concentrations, and DON concentration was calculated by subtraction of DIN from DNb. The stoichiometric ratios among DOC, DNb, DIN, DON, and DTP are expressed on the mass basis. Threedimensional fluorescence excitation-emission spectra of DOC across a range of excitation (220 to 400 nm) and emission (250–500 nm) wavelengths were obtained using a Hitachi F-7000 fluorescence spectrometer (Hitachi High Technologies, Tokyo, Japan) (Fellman et al., 2010). Humification index was calculated as the ratio of the area under the emission spectra 435–480 nm divided by 300–445 nm at excitation wavelength 254 nm, and was widely used to indicate the DOC humification degree in aquatic systems (Zsolnay et al., 1999; Fellman et al., 2010). To determine temperature sensitivity of BDOC, water samples were aerobically incubated in the dark at both 20 °C and 30 °C for 42 days (Wickland et al., 2012). Sets of 250-mL glass bottles were filled with 50 mL filtrates per bottle, and covered with Teflon-lined stoppers and crimp seals. We prepared eight bottles for each water sample: three bottles were incubated at 20 °C and 30 °C, respectively, and another two bottles were used to determine the initial concentration of dissolved
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Fig. 1. Spatial distribution of sampling sites in the Three Gorges Reservoir area, China.
inorganic C (DIC). In addition, three bottles with 50 mL Milli-Q deionized water were used as blanks. On days 2, 6, 12, 18, 30, and 42, 10mL headspace gas was collected, and CO2 concentration was measured using a gas chromatograph (Agilent 7890A, Agilent Technologies, USA). The bottles were purged with CO2-free air for 10 min after gas sampling and then sealed. Final DIC concentration in the water samples was determined by the end of incubation. DIC concentration was measured on a total organic carbon analyzer. For all water samples, CO2 production in the headspace and DIC concentration in the water were calculated by the differences between water samples and the blanks over the 42-day incubation period. BDOC was obtained by the differences in the initial and final DIC contents in the water and the cumulative headspace CO2 production, and was described as the percent of the initial DOC concentration (Wickland et al., 2012). Q10 value of BDOC was calculated according to the following formula: Q10 = BDOC30/BDOC20, where BDOC20 and BDOC30 are BDOC at two incubation temperatures 20 °C and 30 °C, respectively (Sihi et al., 2016).
8.87 with an average value of 8.22, and humification index varied from 2.01 to 8.80 with a mean value of 3.96 (Table 1). For all water samples, BDOC increased with elevating incubation temperature, and Q10 values shifted from 1.42 to 2.67 with a mean value of 2.03 (Table 1). BDOC ranged from 13.1% to 37.0% with an average value of 24.6% at 20 °C, and varied between 25.9% and 66.7% with a mean value of 48.7% at 30 °C (Table 1). In addition, Q10 values of BDOC was negatively correlated with pH (R2 = 0.317, p b 0.001), but was positively correlated with humification index (R2 = 0.530, p b 0.001) (Fig. 2). However, the Q10 values of BDOC exhibited no significant relationships with DOC:DNb, DOC:DIN, DOC:DON, and DOC:DTP ratios (all p N 0.05) (Fig. 2). 4. Discussion The mean Q10 value of BDOC was 2.03 ± 0.32 in these subtropical rivers, which was similar to the values reported in the northern high-
2.3. Statistical analyses Shapiro-Wilk's test was used to test the normality of data, and only pH and Q10 values followed a normal distribution. Thus, all the data were natural log transformed before statistical analyses. Relationships between BDOC and the initial DOC:DNb ratio, DOC:DTP ratio, DOC:DIN ratio, DOC:DON ratio, pH, and humification index were tested using the linear regression analyses. These analyses were performed with the SPSS statistical package (v. 13.0) for Windows. 3. Results − The average DOC, DNb, NH+ 4 -N, NO3 -N, DIN, DON, and DTP concentrations for these 57 water samples were 12.5 mg L−1, 4.2 mg L−1, 16.8 μg L−1, 1.2 mg L−1, 1.2 mg L−1, 3.0 mg L−1, and 0.10 mg L−1, respectively (Table 1). Across the water samples collected, DOC:DNb ratio exhibited a tenfold variation with values ranging from 1.15 to 11.96 (mean value of 3.93), and DOC:DTP ratio varied between 34.0 and 499.8 (mean value of 157.3) (Table 1). Meanwhile, DOC:DIN ratio ranged from 3.1 to 58.4 (mean value of 14.4), and DOC:DON ratio varied from 1.39 to 20.23 (mean value of 7.84) (Table 1). In addition, pH ranged between 7.47 and
Table 1 Initial surface water properties and biodegradable dissolved organic carbon (BDOC) in the subtropical rivers in the Three Gorge Reservoir area, China. Water properties
Mean ± SD
Maximum
Minimum
DOC (mg L−1) DBN (mg L−1) DTP (mg L−1) −1 NH+ ) 4 -N (μg L −1 NO− ) 3 -N (mg L DIN (mg L−1) DON (mg L−1) Humification index pH DOC:DBN ratio DOC:DIN ratio DOC:DON ratio DOC:DTP ratio BDOC20 (% of initial DOC) BDOC30 (% of initial DOC) Q10 values
12.5 ± 6.6 4.2 ± 2.3 0.10 ± 0.06 16.8 ± 10.7 1.2 ± 0.6 1.2 ± 0.6 3.0 ± 2.2 3.96 ± 1.55 8.22 ± 0.29 3.93 ± 2.64 14.4 ± 13.9 7.84 ± 9.09 157.3 ± 95.9 24.6 ± 6.5 48.7 ± 10.6 2.03 ± 0.32
37.5 10.5 0.30 63.2 2.8 2.8 10.0 8.80 8.87 11.96 58.4 20.23 499.8 37.0 66.7 2.67
7.1 0.7 0.02 5.3 0.4 0.4 0.2 2.01 7.47 1.15 3.1 1.39 34.0 13.1 25.9 1.42
DBN, dissolved bound nitrogen; DIN, dissolved inorganic N; DON, dissolved organic N; DTP, dissolved total phosphorus; BDOC20, BDOC at 20 °C; BDOC30, BDOC at 30 °C.
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Fig. 2. Relationships between Q10 values and the initial water properties. DOC, dissolved organic carbon; DNb, dissolved bound nitrogen; DIN, dissolved inorganic N; DON, dissolved organic N; DTP, dissolved total phosphorus.
latitude rivers (2.0 ± 0.6; Wickland et al., 2012) and the assumed values (2.0) for organic C decomposition in inland waters (Catalán et al., 2016) and terrestrial ecosystems (Davidson and Janssens, 2006). However, there was an about twofold variability in the Q10 values of BDOC (1.42 to 2.67) across these rivers, which was comparable to the results of Wickland et al. (2012) who observed that Q10 values of BDOC ranged from 1.1 to 3.2 in the Yukon River and its tributaries in Alaska, USA. In addition, the Q10 values for soil organic C decomposition were not constant, and generally varied over wide ranges (0.9–6.9) in terrestrial ecosystems (Lützow and Kögel-Knabner, 2009). In general, Q10 values of soil organic C decomposition are controlled by the initial organic C quality (Hartley and Ineson, 2008; Li et al., 2017), C:N:P stoichiometry (He and Yu, 2016), and microbial community structure (Bárcenas-Moreno et al., 2009). In this study, we observed highly spatial variations of C: N:P stoichiometric ratios, humification index, and pH among the subtropical rivers. For example, DOC humification index varied from 2.01 to 8.80 in these rivers. Moreover, microbial community composition and structure varied with these water parameters in aquatic systems (Beier et al., 2008). Therefore, the spatial changes in Q10 values were probably caused by the substantial differences in DOC quality, nutrient availability, and aquatic microorganisms among the rivers (Beier et al., 2008; He and Yu, 2016; Shah et al., 2017). These findings address that the generally used Q10 value for DOC biodegradation can not be simply applied to the inland waters, and also imply that the spatial heterogeneity of Q10 values of BDOC should be considered to accurately assess and predict C dynamics in subtropical rivers in the context of climate warming.
Notably, Q10 values of BDOC showed a tight negative relationship with the humification index of DOC in these subtropical rivers. In northern high-latitude rivers, Wickland et al. (2012) also observed that Q10 values of BDOC were positively correlated with the hydrophobic organic acid fraction that is resistant to microbial degradation. These findings supported the C quality-temperature hypothesis which suggests that temperature sensitivity of soil organic C decomposition should increase with substrate recalcitrance (Bosatta and Ågren, 1999; Fierer et al., 2005). In general, DOC with greater humification index decomposed more slowly than that with lower humification index (Kalbitz et al., 2003). Accordingly, the higher activation energy associated with the microbial degradation of recalcitrant DOC resulted in the greater temperature sensitivity of BDOC (Bosatta and Ågren, 1999; Hartley and Ineson, 2008). Our result clearly demonstrates that the C quality-temperature hypothesis can be applied to BDOC in the subtropical rivers, and implies that humification index should be a good indicator of temperature sensitivity of BDOC in inland waters. However, humic-like substances such as aromatic C compounds can be easily photochemically oxidized by the solar radiation in the freshwater systems (Osburn et al., 2001; Hansen et al., 2016). Given that biodegradation and photodegradation occur simultaneously in inland waters, the dual roles of humification degree in regulating DOC degradation should be taken into account. In this study, we observed a negative relationship between pH and Q10 values of BDOC in the selected rivers. In contrast, soil pH is found to be positively correlated with Q10 values of soil organic C decomposition in various terrestrial ecosystems (Craine et al., 2010; GutiérrezGirón et al., 2015; Li et al., 2017). In addition, Li et al. (2017) pointed
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out that such positive relationship may only exist in nearly neutral soils. In this study, pH ranged from 7.47 to 8.87 in these subtropical rivers. Thus, these inconsistent patterns between terrestrial and aquatic ecosystems may be caused by the substantial difference in pH. Generally, aquatic microbial community structure is tightly related to pH in inland waters (Beier et al., 2008). The differences in aquatic microbial composition along the pH gradient probably accounted for this negative relationship because of the idiosyncratic responses to elevating temperature among microorganisms in these rivers (Bárcenas-Moreno et al., 2009). In order to uncover the mechanisms underlying the negative relationship between pH and Q10 values, further studies are urgently needed to clarify the effect of pH on aquatic microbial community composition and structure along the pH gradient in inland waters. Interestingly, Q10 values of BDOC did not correlate well with the initial DOC:DNb, DOC:DIN, DOC:DON and DOC:DTP ratios. In the previous studies, nutrient availability was found to be a primary factor affecting the temperature sensitivity of soil organic C decomposition in grassland, wetland, and forest ecosystems (He and Yu, 2016; Sihi et al., 2016). In inland waters, nutritional requirements of aquatic microorganisms can be satisfied at the relatively low levels of inorganic nutrients (Fernandes et al., 2014). Therefore, N and P might not constrain the responses of microbial degradation of DOC to elevated incubation temperature in these subtropical rivers (He and Yu, 2016). In summary, temperature sensitivity of BDOC exhibited remarkably spatial heterogeneity (from 1.42 to 2.67) across the subtropical rivers. Moreover, DOC humification degree and pH co-regulated the spatial change in temperature sensitivity of BDOC. Our results clearly confirm the applicability of the C quality-temperature hypothesis in subtropical rivers, and also provide insights into accurately developing C models and predicting C cycles in inland waters in the context of climate warming. Acknowledgments This study was funded by the “Hundred Talent Program” of the Chinese Academy of Sciences (granted to Dr. Siyue Li), the CAS “Light of West China” Program, and the National Natural Science Foundation of China (Grant No. 31670473). We thank Dr. Mao-Fei Ni and Jia-Cheng Luo for the field work, and editor José Virgílio Cruz and the anonymous reviewers for their constructive comments on the earlier draft of this manuscript. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi. org/10.1016/j.scitotenv.2018.04.256. References Bárcenas-Moreno, G., Gómez-Brandón, M., Rousk, J., Bååth, E., 2009. Adaptation of soil microbial communities to temperature: comparison of fungi and bacteria in a laboratory experiment. Glob. Chang. Biol. 15, 2950–2957. Beier, S., Witzel, K.P., Marxsen, J., 2008. Bacterial community composition in Central European running waters examined by temperature gradient gel electrophoresis and sequence analysis of 16S rRNA genes. Appl. Environ. Microbiol. 74, 188–199. Bosatta, E., Ågren, G.I., 1999. Soil organic matter quality interpreted thermodynamically. Soil Biol. Biochem. 31, 1889–1891. Brown, J.H., Gillooly, J.F., Allen, A.P., Savage, V.M., West, G.B., 2004. Toward a metabolic theory of ecology. Ecology 85, 1771–1789. Catalán, N., Marcé, R., Kothawala, D.N., Tranvik, L.J., 2016. Organic carbon decomposition rates controlled by water retention time across inland waters. Nat. Geosci. 9, 501–504. 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. Conant, R.T., Ryan, M.G., Ågren, G.I., Birge, H.E., Davidson, E.A., Eliasson, P.E., Evans, S.E., Frey, S.D., Giardina, C.P., Hopkins, F.M., Hyvönen, R., Kirschbaum, M.U.F., Lavallee, J.M., Leifeld, J., Parton, W.J., Steinweg, J.M., Wallenstein, M.D., Wetterstedt, J.A.M., Bradford, M.A., 2011. Temperature and soil organic matter decomposition ratessynthesis of current knowledge and a way forward. Glob. Chang. Biol. 17, 3392–3404.
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Short Communication
Temperature sensitivity of biodegradable dissolved organic carbon increases with elevating humification degree in subtropical rivers Rong Mao, Si-Yue Li ⁎ The Three Gorges Institute of Ecological Environment, Chongqing Institute of Green and Intelligent Technology, Chinese Academy of Sciences, Chongqing 400714, China
H I G H L I G H T S • The Q10 values of BDOC were determined in the Three Gorges Reservoir river networks. • Approximately two-fold variations in Q10 value of BDOC were observed. • Q10 elevated with increasing humification degree, but decreased with increasing pH. • DOC quality and pH are powerful predictors of Q10 of BDOC in subtropical rivers. • C quality-temperature hypothesis can be applied to BDOC in subtropical rivers.
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Article history: Received 10 February 2018 Received in revised form 19 April 2018 Accepted 19 April 2018 Available online xxxx Editor: José Virgílio Cruz Keywords: Carbon cycle Carbon quality-temperature hypothesis Climate warming Inland waters Q10 value
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a b s t r a c t Biodegradable dissolved organic carbon (BDOC) plays a key role in C cycle in inland waters. However, the magnitude of temperature sensitivity (Q10 value) of BDOC is still unclear, and the effect of DOC quality on Q10 value of BDOC is not well verified in these aquatic systems. Here, we used a laboratory incubation experiment to determine the Q10 value of BDOC in 57 rivers in the Three Gorges Reservoir area, China, and then tested whether C quality-temperature hypothesis could be applied to BDOC in inland waters. We observed approximately twofold variations in Q10 values of BDOC (1.42–2.67) in these rivers. Moreover, the tight positive relationship between the Q10 values of BDOC and DOC humification index indicated the applicability of C quality-temperature hypothesis in subtropical rivers. In addition, the Q10 values of BDOC exhibited a negative relationship with pH. These findings suggest that DOC quality and pH are powerful predictors of temperature sensitivity of BDOC in subtropical rivers. In conclusion, our results would help to improve the C models and predict the feedback between climate warming and C dynamics in inland waters. © 2018 Elsevier B.V. All rights reserved.
1. Introduction Inland waters are an indispensable component of global carbon (C) cycle because of their critical roles in transporting C from land to ⁎ 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.-Y. Li).
https://doi.org/10.1016/j.scitotenv.2018.04.256 0048-9697/© 2018 Elsevier B.V. All rights reserved.
ocean and regulating atmospheric greenhouse gas concentrations (Cole et al., 2007; Raymond et al., 2013). In these aquatic systems, dissolved organic C (DOC) is the dominant form of organic C in the water column and plays an essential part in modulating C dynamics from local to global scales (Kellerman et al., 2015; Schiller et al., 2017). Generally, the quantity and quality of DOC are largely controlled by the processes of biodegradation and photodegradation in the aquatic environments (Moran and Zepp, 1997; Catalán et al., 2016). Both of these processes can convert DOC to inorganic compounds or result in a shift
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in DOC chemical composition (Moran et al., 2000; Hansen et al., 2016), probably exerting a remarkable impact on the biological utilization and fate of DOC in inland waters. In inland waters, DOC acts as the main source of substrates for aquatic heterotrophic microorganisms (Schiller et al., 2017). Thus, biodegradable DOC (BDOC) is of great importance to the production of carbon dioxide and methane and the amount and composition of DOC in these aquatic systems (Moran et al., 2000; Catalán et al., 2016; Hansen et al., 2016). In general, BDOC is profoundly influenced by a great variety of factors, such as initial chemical composition (Kalbitz et al., 2003; Kellerman et al., 2015), nutrient availability (Wickland et al., 2012; Mao et al., 2017), water retention time (Catalán et al., 2016), and climate conditions (Wickland et al., 2012). Any changes in these factors would result in the substantial variation of BDOC, which may produce a marked influence on organic C transportation and transformation in inland waters. In the recent decades, the Earth's climate has dramatically warmed, and this trend will be continuing as a consequence of rising concentrations of greenhouse gases in the atmosphere (IPCC, 2015). Consequently, climate warming inevitably leads to a notable increase in mean water temperature in inland aquatic ecosystems (van Vliet et al., 2011). Considering that most inland waters are net heterotrophic (Shah et al., 2017), elevated temperature is predicted to enhance BDOC through stimulated aquatic microbial growth and metabolic activity (Brown et al., 2004). Generally, temperature sensitivity (commonly expressed as Q10, indicating the organic C mineralization rate changes with a 10 °C rise in temperature) of BDOC is assumed to be 2.0 (Catalán et al., 2016). However, previous studies have shown that Q10 values are not constant across different terrestrial ecosystems (Davidson and Janssens, 2006; Lützow and Kögel-Knabner, 2009). Unfortunately, the magnitudes of Q10 values of BDOC remain uncertain in inland waters due to the lack of empirical studies. In general, Q10 values of organic C decomposition vary with the intrinsic organic C quality (Hartley and Ineson, 2008; Li et al., 2017), microbial community composition (Davidson and Janssens, 2006), pH (Li et al., 2017), and nutrient availability (Davidson and Janssens, 2006; Sihi et al., 2016) in terrestrial ecosystems. Among them, the intrinsic organic C quality is regarded as one of the most important factors controlling Q10 values, because organic C often consists of different C component with various activation energy (Hartley and Ineson, 2008; Davidson and Janssens, 2006). Recalcitrant organic C fraction containing more biochemically complex compounds has greater activation energy than labile organic C fraction, and thus decomposes slower (Davidson and Janssens, 2006; Lützow and Kögel-Knabner, 2009). According to the Arrhenius equation, organic C decomposition reaction with lower activation energy should have lower Q10 values (Davidson and Janssens, 2006; Conant et al., 2011). Accordingly, temperature sensitivity of organic C decomposition should increase with the substrate recalcitrance (i.e., C quality-temperature hypothesis) (Bosatta and Ågren, 1999). Indeed, previous studies have documented that recalcitrant soil organic C fraction has a higher temperature sensitivity than labile soil organic C fraction in most terrestrial ecosystems (e.g. Fierer et al., 2005; Hartley and Ineson, 2008; Sihi et al., 2016). Moreover, Shah et al. (2017), synthesizing 1025 records of litter decomposition in streams and rivers, have observed that temperature sensitivity of litter decomposition increased with decreasing substrate quality. However, whether this hypothesis can be applied to BDOC is still unclear in inland waters. Therefore, knowledge about the relationship between DOC quality and Q10 values of BDOC will help to accurately develop C models and understand C dynamics in inland waters in the context of global warming. In this study, we obtained water samples from 57 rivers from late June to early July in the Three Gorges Reservoir area, China, and then measure the concentrations of DOC, dissolved bound nitrogen (DNb), − NH+ 4 -N, NO3 -N, dissolved inorganic N (DIN), dissolved organic N (DON), and dissolved total phosphorus (DTP), pH, DOC humification
index, and BDOC at both 20 °C and 30 °C in these waters. In the previous studies, DOC humification index related positively to the abundances of humic-like component (Williams et al., 2010) and polyphenol-like components with H/C ratios b 1 and O/C ratios N 0.6 (Dadi et al., 2017), and the aromatic character of the moleculars (Fuentes et al., 2006), and was found to be negatively correlated with BDOC (Kalbitz et al., 2003). Therefore, we used humification index to indicate DOC quality; DOC with a greater value of humification index represents a lower DOC quality, and thus is more resistance to biodegradation. The specific objectives of this study were to: (1) clarify the Q10 values of BDOC in these subtropical rivers, and (2) test the applicability of C quality-temperature hypothesis to BDOC in inland waters. 2. Materials and methods 2.1. Site description This study was performed in the Three Gorges Reservoir area (28°44′–31°40′N, 106°10′–111°10′E), China. The Three Gorges Reservoir lies in the upper reach of Yangtze River, and the water level periodically fluctuates from 145 m in summer to 175 m in winter. The study site belongs to humid subtropical monsoon climate. Mean annual temperature is 16.5–19.0 °C and monthly mean temperature ranges from 3.4–7.2 °C in January to 28.0–30.0 °C in July. Mean annual precipitation is 1250 mm, 70% of which falls between May and September (Li et al., 2018). 2.2. Sample collection and measurement From late June to early July 2016, we collected water samples from 57 rivers, which represented the majority of rivers in the Three Gorges Reservoir area (Fig. 1 and Supplementary material). In each river, running surface water (10 cm depth) was sampled in the center of the river channel using acid-washed plastic containers, filtered with Whatman GF/F glass fiber filters (0.7 μm pore size) within 12 h, and then stored in the dark (4 °C) until analysis (b120 h). For all water samples, DOC concentration was analyzed by the high temperature combustion method on a total organic carbon analyzer (TOC-5000, Shimadzu, Japan), DNb and DTP concentrations were determined by the hydrazine sulphate spectrophometric method and ammonium molybdate spectrophometric method on a continuous-flow autoanalyzer (AA3, Seal Analytical, Germany) after alkaline peroxodisulfate digestion − (Ebina et al., 1983), respectively, NH+ 4 -N and NO3 -N concentrations were measured using the sodium salicylate sodium hypochlorite method and the hydrazine sulphate spectrophometric method on a continuous-flow autoanalyzer, respectively, and pH was assessed by a HACH portable pH meter. DIN concentration was the sum of NH+ 4 -N and NO− 3 -N concentrations, and DON concentration was calculated by subtraction of DIN from DNb. The stoichiometric ratios among DOC, DNb, DIN, DON, and DTP are expressed on the mass basis. Threedimensional fluorescence excitation-emission spectra of DOC across a range of excitation (220 to 400 nm) and emission (250–500 nm) wavelengths were obtained using a Hitachi F-7000 fluorescence spectrometer (Hitachi High Technologies, Tokyo, Japan) (Fellman et al., 2010). Humification index was calculated as the ratio of the area under the emission spectra 435–480 nm divided by 300–445 nm at excitation wavelength 254 nm, and was widely used to indicate the DOC humification degree in aquatic systems (Zsolnay et al., 1999; Fellman et al., 2010). To determine temperature sensitivity of BDOC, water samples were aerobically incubated in the dark at both 20 °C and 30 °C for 42 days (Wickland et al., 2012). Sets of 250-mL glass bottles were filled with 50 mL filtrates per bottle, and covered with Teflon-lined stoppers and crimp seals. We prepared eight bottles for each water sample: three bottles were incubated at 20 °C and 30 °C, respectively, and another two bottles were used to determine the initial concentration of dissolved
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Fig. 1. Spatial distribution of sampling sites in the Three Gorges Reservoir area, China.
inorganic C (DIC). In addition, three bottles with 50 mL Milli-Q deionized water were used as blanks. On days 2, 6, 12, 18, 30, and 42, 10mL headspace gas was collected, and CO2 concentration was measured using a gas chromatograph (Agilent 7890A, Agilent Technologies, USA). The bottles were purged with CO2-free air for 10 min after gas sampling and then sealed. Final DIC concentration in the water samples was determined by the end of incubation. DIC concentration was measured on a total organic carbon analyzer. For all water samples, CO2 production in the headspace and DIC concentration in the water were calculated by the differences between water samples and the blanks over the 42-day incubation period. BDOC was obtained by the differences in the initial and final DIC contents in the water and the cumulative headspace CO2 production, and was described as the percent of the initial DOC concentration (Wickland et al., 2012). Q10 value of BDOC was calculated according to the following formula: Q10 = BDOC30/BDOC20, where BDOC20 and BDOC30 are BDOC at two incubation temperatures 20 °C and 30 °C, respectively (Sihi et al., 2016).
8.87 with an average value of 8.22, and humification index varied from 2.01 to 8.80 with a mean value of 3.96 (Table 1). For all water samples, BDOC increased with elevating incubation temperature, and Q10 values shifted from 1.42 to 2.67 with a mean value of 2.03 (Table 1). BDOC ranged from 13.1% to 37.0% with an average value of 24.6% at 20 °C, and varied between 25.9% and 66.7% with a mean value of 48.7% at 30 °C (Table 1). In addition, Q10 values of BDOC was negatively correlated with pH (R2 = 0.317, p b 0.001), but was positively correlated with humification index (R2 = 0.530, p b 0.001) (Fig. 2). However, the Q10 values of BDOC exhibited no significant relationships with DOC:DNb, DOC:DIN, DOC:DON, and DOC:DTP ratios (all p N 0.05) (Fig. 2). 4. Discussion The mean Q10 value of BDOC was 2.03 ± 0.32 in these subtropical rivers, which was similar to the values reported in the northern high-
2.3. Statistical analyses Shapiro-Wilk's test was used to test the normality of data, and only pH and Q10 values followed a normal distribution. Thus, all the data were natural log transformed before statistical analyses. Relationships between BDOC and the initial DOC:DNb ratio, DOC:DTP ratio, DOC:DIN ratio, DOC:DON ratio, pH, and humification index were tested using the linear regression analyses. These analyses were performed with the SPSS statistical package (v. 13.0) for Windows. 3. Results − The average DOC, DNb, NH+ 4 -N, NO3 -N, DIN, DON, and DTP concentrations for these 57 water samples were 12.5 mg L−1, 4.2 mg L−1, 16.8 μg L−1, 1.2 mg L−1, 1.2 mg L−1, 3.0 mg L−1, and 0.10 mg L−1, respectively (Table 1). Across the water samples collected, DOC:DNb ratio exhibited a tenfold variation with values ranging from 1.15 to 11.96 (mean value of 3.93), and DOC:DTP ratio varied between 34.0 and 499.8 (mean value of 157.3) (Table 1). Meanwhile, DOC:DIN ratio ranged from 3.1 to 58.4 (mean value of 14.4), and DOC:DON ratio varied from 1.39 to 20.23 (mean value of 7.84) (Table 1). In addition, pH ranged between 7.47 and
Table 1 Initial surface water properties and biodegradable dissolved organic carbon (BDOC) in the subtropical rivers in the Three Gorge Reservoir area, China. Water properties
Mean ± SD
Maximum
Minimum
DOC (mg L−1) DBN (mg L−1) DTP (mg L−1) −1 NH+ ) 4 -N (μg L −1 NO− ) 3 -N (mg L DIN (mg L−1) DON (mg L−1) Humification index pH DOC:DBN ratio DOC:DIN ratio DOC:DON ratio DOC:DTP ratio BDOC20 (% of initial DOC) BDOC30 (% of initial DOC) Q10 values
12.5 ± 6.6 4.2 ± 2.3 0.10 ± 0.06 16.8 ± 10.7 1.2 ± 0.6 1.2 ± 0.6 3.0 ± 2.2 3.96 ± 1.55 8.22 ± 0.29 3.93 ± 2.64 14.4 ± 13.9 7.84 ± 9.09 157.3 ± 95.9 24.6 ± 6.5 48.7 ± 10.6 2.03 ± 0.32
37.5 10.5 0.30 63.2 2.8 2.8 10.0 8.80 8.87 11.96 58.4 20.23 499.8 37.0 66.7 2.67
7.1 0.7 0.02 5.3 0.4 0.4 0.2 2.01 7.47 1.15 3.1 1.39 34.0 13.1 25.9 1.42
DBN, dissolved bound nitrogen; DIN, dissolved inorganic N; DON, dissolved organic N; DTP, dissolved total phosphorus; BDOC20, BDOC at 20 °C; BDOC30, BDOC at 30 °C.
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Fig. 2. Relationships between Q10 values and the initial water properties. DOC, dissolved organic carbon; DNb, dissolved bound nitrogen; DIN, dissolved inorganic N; DON, dissolved organic N; DTP, dissolved total phosphorus.
latitude rivers (2.0 ± 0.6; Wickland et al., 2012) and the assumed values (2.0) for organic C decomposition in inland waters (Catalán et al., 2016) and terrestrial ecosystems (Davidson and Janssens, 2006). However, there was an about twofold variability in the Q10 values of BDOC (1.42 to 2.67) across these rivers, which was comparable to the results of Wickland et al. (2012) who observed that Q10 values of BDOC ranged from 1.1 to 3.2 in the Yukon River and its tributaries in Alaska, USA. In addition, the Q10 values for soil organic C decomposition were not constant, and generally varied over wide ranges (0.9–6.9) in terrestrial ecosystems (Lützow and Kögel-Knabner, 2009). In general, Q10 values of soil organic C decomposition are controlled by the initial organic C quality (Hartley and Ineson, 2008; Li et al., 2017), C:N:P stoichiometry (He and Yu, 2016), and microbial community structure (Bárcenas-Moreno et al., 2009). In this study, we observed highly spatial variations of C: N:P stoichiometric ratios, humification index, and pH among the subtropical rivers. For example, DOC humification index varied from 2.01 to 8.80 in these rivers. Moreover, microbial community composition and structure varied with these water parameters in aquatic systems (Beier et al., 2008). Therefore, the spatial changes in Q10 values were probably caused by the substantial differences in DOC quality, nutrient availability, and aquatic microorganisms among the rivers (Beier et al., 2008; He and Yu, 2016; Shah et al., 2017). These findings address that the generally used Q10 value for DOC biodegradation can not be simply applied to the inland waters, and also imply that the spatial heterogeneity of Q10 values of BDOC should be considered to accurately assess and predict C dynamics in subtropical rivers in the context of climate warming.
Notably, Q10 values of BDOC showed a tight negative relationship with the humification index of DOC in these subtropical rivers. In northern high-latitude rivers, Wickland et al. (2012) also observed that Q10 values of BDOC were positively correlated with the hydrophobic organic acid fraction that is resistant to microbial degradation. These findings supported the C quality-temperature hypothesis which suggests that temperature sensitivity of soil organic C decomposition should increase with substrate recalcitrance (Bosatta and Ågren, 1999; Fierer et al., 2005). In general, DOC with greater humification index decomposed more slowly than that with lower humification index (Kalbitz et al., 2003). Accordingly, the higher activation energy associated with the microbial degradation of recalcitrant DOC resulted in the greater temperature sensitivity of BDOC (Bosatta and Ågren, 1999; Hartley and Ineson, 2008). Our result clearly demonstrates that the C quality-temperature hypothesis can be applied to BDOC in the subtropical rivers, and implies that humification index should be a good indicator of temperature sensitivity of BDOC in inland waters. However, humic-like substances such as aromatic C compounds can be easily photochemically oxidized by the solar radiation in the freshwater systems (Osburn et al., 2001; Hansen et al., 2016). Given that biodegradation and photodegradation occur simultaneously in inland waters, the dual roles of humification degree in regulating DOC degradation should be taken into account. In this study, we observed a negative relationship between pH and Q10 values of BDOC in the selected rivers. In contrast, soil pH is found to be positively correlated with Q10 values of soil organic C decomposition in various terrestrial ecosystems (Craine et al., 2010; GutiérrezGirón et al., 2015; Li et al., 2017). In addition, Li et al. (2017) pointed
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out that such positive relationship may only exist in nearly neutral soils. In this study, pH ranged from 7.47 to 8.87 in these subtropical rivers. Thus, these inconsistent patterns between terrestrial and aquatic ecosystems may be caused by the substantial difference in pH. Generally, aquatic microbial community structure is tightly related to pH in inland waters (Beier et al., 2008). The differences in aquatic microbial composition along the pH gradient probably accounted for this negative relationship because of the idiosyncratic responses to elevating temperature among microorganisms in these rivers (Bárcenas-Moreno et al., 2009). In order to uncover the mechanisms underlying the negative relationship between pH and Q10 values, further studies are urgently needed to clarify the effect of pH on aquatic microbial community composition and structure along the pH gradient in inland waters. Interestingly, Q10 values of BDOC did not correlate well with the initial DOC:DNb, DOC:DIN, DOC:DON and DOC:DTP ratios. In the previous studies, nutrient availability was found to be a primary factor affecting the temperature sensitivity of soil organic C decomposition in grassland, wetland, and forest ecosystems (He and Yu, 2016; Sihi et al., 2016). In inland waters, nutritional requirements of aquatic microorganisms can be satisfied at the relatively low levels of inorganic nutrients (Fernandes et al., 2014). Therefore, N and P might not constrain the responses of microbial degradation of DOC to elevated incubation temperature in these subtropical rivers (He and Yu, 2016). In summary, temperature sensitivity of BDOC exhibited remarkably spatial heterogeneity (from 1.42 to 2.67) across the subtropical rivers. Moreover, DOC humification degree and pH co-regulated the spatial change in temperature sensitivity of BDOC. Our results clearly confirm the applicability of the C quality-temperature hypothesis in subtropical rivers, and also provide insights into accurately developing C models and predicting C cycles in inland waters in the context of climate warming. Acknowledgments This study was funded by the “Hundred Talent Program” of the Chinese Academy of Sciences (granted to Dr. Siyue Li), the CAS “Light of West China” Program, and the National Natural Science Foundation of China (Grant No. 31670473). We thank Dr. Mao-Fei Ni and Jia-Cheng Luo for the field work, and editor José Virgílio Cruz and the anonymous reviewers for their constructive comments on the earlier draft of this manuscript. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi. org/10.1016/j.scitotenv.2018.04.256. References Bárcenas-Moreno, G., Gómez-Brandón, M., Rousk, J., Bååth, E., 2009. Adaptation of soil microbial communities to temperature: comparison of fungi and bacteria in a laboratory experiment. Glob. Chang. Biol. 15, 2950–2957. Beier, S., Witzel, K.P., Marxsen, J., 2008. Bacterial community composition in Central European running waters examined by temperature gradient gel electrophoresis and sequence analysis of 16S rRNA genes. Appl. Environ. Microbiol. 74, 188–199. Bosatta, E., Ågren, G.I., 1999. Soil organic matter quality interpreted thermodynamically. Soil Biol. Biochem. 31, 1889–1891. Brown, J.H., Gillooly, J.F., Allen, A.P., Savage, V.M., West, G.B., 2004. Toward a metabolic theory of ecology. Ecology 85, 1771–1789. Catalán, N., Marcé, R., Kothawala, D.N., Tranvik, L.J., 2016. Organic carbon decomposition rates controlled by water retention time across inland waters. Nat. Geosci. 9, 501–504. 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. Conant, R.T., Ryan, M.G., Ågren, G.I., Birge, H.E., Davidson, E.A., Eliasson, P.E., Evans, S.E., Frey, S.D., Giardina, C.P., Hopkins, F.M., Hyvönen, R., Kirschbaum, M.U.F., Lavallee, J.M., Leifeld, J., Parton, W.J., Steinweg, J.M., Wallenstein, M.D., Wetterstedt, J.A.M., Bradford, M.A., 2011. Temperature and soil organic matter decomposition ratessynthesis of current knowledge and a way forward. Glob. Chang. Biol. 17, 3392–3404.
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