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Using Fecal Sterols to Assess Dynamics of Sewage Input in Sediments Along a Human-Impacted River-Estuary System in Eastern China

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Using Fecal Sterols to Assess Dynamics of Sewage Input in Sediments Along a Human-Impacted River-Estuary System in Eastern China Science of the Total Environment 636 (2018) 787–797 Contents lists available at ScienceDirect Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv Using fecal sterols to assess dynamics of sewage input in sediments along a human-impacted river-estuary system in eastern China Ding He a,⁎, Kai Zhang a, Jianhui Tang b, Xingqian Cui c, Yongge Sun a a Institute of Environment & Biogeochemistry (eBig), School of Earth Sciences, Zhejiang University, Hangzhou 310027, China b Yantai Institute of Coastal Zone Research, CAS, Yantai, Shandong 264003, China c Department of Earth, Atmospheric and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA HIGHLIGHTS GRAPHICAL ABSTRACT • Mutiple sedimentary sterols used for The upper left panel showing the formation of 5α-and5β-stanols is mainly modified from Bull et al., 2002. the sewage contamination assessment. • Higher sewage input observed in the Xiaoqing River than the Laizhou Bay. • Significant spatial instead of seasonal variation in fecal sterol concentrations observed. • Seasonal variation of two fecal sterol- based ratios observed. article info abstract Article history: Sedimentary fecal sterols and other sterol biomarkers, combined with bulk total organic carbon (TOC) and its sta- Received 9 February 2018 ble carbon isotope were applied to characterize the sewage contamination across a ca. 280 km transect from the Received in revised form 23 April 2018 Xiaoqing River to the Laizhou Bay, a typical river-estuary system subjected to extensive anthropogenic stress due Accepted 24 April 2018 to rapid regional urbanization and industrialization in eastern China. Two sampling events were performed in Available online 2 May 2018 both spring and summer seasons in the Laizhou Bay adjacent to the Xiaoqing River in order to assess the potential Editor: D. Barcelo seasonal variation. Fecal sterols such as coprostanol and epicoprostanol, which are typical indicators of anthropo- genic sewage input, displayed high concentrations of up to 63.2 μgg−1 dry weight (dw) and 13.1 μgg−1 dw, re- Keywords: spectively. Results suggested that most of the stations along the Xiaoqing River were severely contaminated by Fecal sterols fecal inputs with a decreasing trend from the river to the estuary that was mainly explained by the increasing dis- Sewage contamination tance from the diffuse sewage sources and the gradual dilution by sea water. Although there was no significant Biomarkers difference in fecal sterol concentrations between spring and summer in the Laizhou Bay, suggestive of no signif- Stable carbon isotopes icant difference in sewage abundance, significantly higher average epicoprostanol/coprostanol and lower River-estuary system coprostanol/epicoprostanol ratios were observed in spring than summer, indicative of different sewage sources (e.g., human vs. non-human). Seasonal discharge and land-runoff, air temperature related to microbial activity differences and different extend of animal manure irrigation during agricultural planting could be additional ⁎ Corresponding author. E-mail address: [email protected] (D. He). https://doi.org/10.1016/j.scitotenv.2018.04.314 0048-9697/© 2018 Elsevier B.V. All rights reserved. 788 D. He et al. / Science of the Total Environment 636 (2018) 787–797 reasons and need further investigation. Nevertheless, fecal sterol concentrations, distributions and diagnostic ra- tios should all be taken into consideration to better understand sewage inputs and source dynamics in river- estuary ecosystems. © 2018 Elsevier B.V. All rights reserved. 1. Introduction and receives water discharge from the Xiaoqing River and the Yellow River directly. The Xiaoqing River is the second largest river draining Anthropogenic interference in the form of domestic sewage dis- into the Laizhou Bay, only secondary to the Yellow River. In contrast charge to rivers and coastal areas has caused severe environmental with the Yellow River that is dominated by natural OM (Tao et al., problems such as eutrophication, oxygen depletion and contamination 2015), the Xiaoqing River is severely polluted since the drainage basin (NBSC, 2012; Pan and Wang, 2012). Most of the coastal cities in China of the Xiaoqing River is characterized by high-density population and are characterized by a rapid industrialization and urbanization since extensive agricultural farming (Jiang et al., 2017). Although this system the 1980s. Therefore, the assessment of anthropogenic contamination has been widely studied in terms of water chemistry and sediment in coastal areas is of great interest for both the environment and chemistry (e.g., dissolved organic matter, heavy metals and persistent human health, considering the high population density in these areas organic pollutants) (Ren et al., 2014; Wang et al., 2016; Jiang et al., (e.g., Förstner, 2006; NBSC, 2012; Canuel and Hardison, 2016). 2017; Jiao et al., 2017), our current knowledge on fecal contamination, Sewage input, a major type of anthropogenic contamination that owing to the intensive urbanization in the watershed, is limited. Surface causes declining water quality in aquatic ecosystems, can be assessed sediments in the river-estuary system provide excellent opportunities using molecular markers (e.g., Bull et al., 2002; Carreira et al., 2004; to evaluate levels of anthropogenic contamination and their influence Muniz et al., 2015; Derrien et al., 2017). Sterols, a common type of mo- on coastal ecosystems (e.g., Andrews et al., 1998). With high sedimenta- lecular markers, can be used to determine sources and fate of both an- tion rates of up to 9.4 cm/yr (Li et al., 2012), fast accumulation of pollut- thropogenic (e.g., fecal input; e.g., Bull et al., 2002) and natural organic ants was detected in the Xiaoqing River mouth and Laizhou Bay (Zhang matter (OM; e.g., marine and terrigenous; Volkman, 2005) in environ- et al., 2009). The seasonal variations of the Xiaoqing River, in terms of ments. The phytosterols, including stigmasterol (stigmasta-5,22E- water discharges, rain falls and hydrodynamic processes, could poten- dien-3β-ol) and β-sitosterol (stigamast-5-en-3β-ol), are biomarkers of tially affect the transport and deposition of sewage related OM (Liu terrestrial organic matter (OM; Moreau et al., 2002). Brassicasterol et al., 2009; Gao, 2011; Yu et al., 2016). (ergosta-5,22E-dien-3β-ol) is mainly produced by marine phytoplank- In this study, surface sediments from spring and summer were col- ton (Volkman, 1986); cholesterol (cholest-5-en-3β-ol) is generally at- lected along the Xiaoqing River–Laizhou Bay estuary system to tributed to a wide diversity of phytoplankton and zooplankton (i) determine concentrations and sources of sedimentary sterols, (ii) as- (e.g., Volkman, 2005). These two sterols (brassicasterol and cholesterol) sess sewage contamination levels in surface sediments, and (iii) exam- are widely used as biomarkers of aquatic OM. In contrast, the fecal ste- ine spatial and seasonal influences on sedimentary fecal sterol rols such as coprostanol (5β-cholestan-3β-ol) and epicoprostanol (5β- distributions and possible controlling factors. Results from this study cholestan-3α-ol) are usually considered to be derived from fecal pollu- could potentially be relevant to sewage regulation and treatment in tion and urban wastewater inputs (Grimaltetal.,1990; González-Oreja the future. and Saiz-Salinas, 1998; Bull et al., 2002; Carreira et al., 2004; Vane et al., 2010; Adnan et al., 2012; Abreu-Mota et al., 2014; Muniz et al., 2015; Rada et al., 2016). Coprostanol, a fecal sterol (5β-stanol) detected pre- 2. Materials and methods dominantly in human feces, is preferentially produced in human guts by enzymatic reduction of cholesterol through anaerobic bacteria 2.1. Description of study sites (Macdonald et al., 1983). Coprostanol comprises up to 60% of total ste- rols in human feces (Leeming et al., 1996). Similar to other sterols that The Xiaoqing River is ca. 240 km and covers a drainage basin of ca. are commonly hydrophobic, coprostanol is generally associated with 2800 km2.Itflows through numerous large cities, such as Jinan, Zibo, particulate matter in sewage and is finally incorporated and preserved Binzhou, Dongying and Weifang, and is comprehensively utilized for in the bottom sediments (Bartlett, 1987). Previous studies proposed controlling flood, irrigation, and shipping, etc. The Xiaoqing River coprostanol concentrations above a certain level to be indicative of sew- empties into the Laizhou Bay in the Bohai Sea. The population sizes of age contamination in aquatic sediments, although various thresholds Jinan, Zibo, Binzhou, Dongying and Weifang cities are approximately were applied, such as 0.1, 0.5 or 0.7 μgg−1 dry weight (Grimalt et al., 7.23 million, 4.71 million, 3.8 million, 2.13 million, and 9.28 million, re- 1990; González-Oreja and Saiz-Salinas, 1998; Rada et al., 2016). How- spectively. The average annual rainfall rate in the Xiaoqing River basin is ever, Tse et al. (2014) suggested that coprostanol alone may not be sew- ca. 620 mm/yr with strong heterogeneity monthly. For example, July age specific, since in situ anaerobic hydrogenation or microbial and August account for N50% of the annual total rainfall (Gao, 2011). reduction processes can also produce coprostanol in sediments using The average air temperature in spring and summer are 5 °C and 27 °C, cholesterol as the precursor (Fattore et al., 1996). Instead, a more robust respectively, based on data from a weather monitoring station in Jinan assessment of sewage contamination can be conducted by investigating City (Gao, 2011). In recent years, the Xiaoqing River has undergone se- sterol-based ratios (e.g., Grimalt et al., 1990; Writer et al., 1995). For ex- rious pollution due to rapid urbanization and industrialization. Accord- ample, sterol-based diagnostic ratios have been applied to evaluate ing to a survey in 2014 (Jinan Environmental Quality Report), 68.8% of (i) whether the sewage was treated or not before being discharged Jinan's industrial emission was discharged into the Xiaoqing River. (Mudge and Seguel, 1999), and (ii) the origins of the feces (human vs.
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