Anthropogenic pollution and oxygen depletion in the lower Yangtze River as revealed by sedimentary biomarkers

Organic Geochemistry 53 (2012) 95–98

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Anthropogenic pollution and oxygen depletion in the lower Yangtze River as revealed by sedimentary biomarkers Chun Zhu a,⇑, Jian-M. Pan b, Richard D. Pancost a a b

Organic Geochemistry Unit, Bristol Biogeochemistry Research Centre, School of Chemistry, University of Bristol, Bristol BS8 1TS, UK Laboratory of Marine Ecosystem and Biogeochemistry, Second Institute of Oceanography, State Oceanic Administration, Hangzhou 310012, PR China

a r t i c l e

i n f o

Article history: Received 2 October 2011 Received in revised form 14 September 2012 Accepted 14 September 2012 Available online 25 September 2012

a b s t r a c t The Yangtze River receives 37.5% of the municipal sewage of China, whose fate constitutes a major environmental and health concern. This study applied phytosterols, 5b(H)-stanols, tetrahymanol and 17a,21b(H)-C30-hopane to examine sewage and petroleum-derived organic pollutants, and assess their impact on the biogeochemistry of the lower river benthic environment. The results showed that significant contributions from sewage and petroleum pollutants were preserved in the riverbed. These potentially contributed to O2 depletion and apparently an anoxic environment in the riverbed, either directly or via an impact on primary productivity. Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction

2. Material and methodology

The Yangtze River drainage basin is home to 400 million people, with the Yangtze River Delta region being one of the most developed and highly industrialized areas in China. Due to population growth and economic development, the river is subject to extensive anthropogenic pollution, including agricultural runoff, industrial waste, municipal sewage, heavy metals and oil hydrocarbons. In fact, it receives 37.5% of the municipal sewage of China, with an annual sewage discharge of 6.3 billion tons from the 21 big cities along the main stream of the river. Notably, as of the beginning of the 21st Century, 70% of the cities did not comply with the national discharge standard (Report on the Marine Environmental Quality in China, 2001). As a result, the river as a lifeline and ecosystem is deteriorating and it is considered to be one of the most polluted rivers in the world (Wong et al., 2007). Studies have been carried out to examine the cause–effect relationships between, for example: (i) riverine nutrient composition and estuarine eutrophication (Zhou et al., 2008), (ii) reduced sediment load and coastal erosion (Yang et al., 2006) and (iii) organic matter runoff and hypoxia (Zhu et al., 2011d). Few have, however, focussed directly on sewage discharge and shipping pollution and their impact on the river channel environments. Therefore, the goal of this study was to examine sewage and petroleum-derived organic pollutants in the lower Yangtze River and to evaluate their impact on the biogeochemistry of the Yangtze River main stream and its estuary.

The Yangtze River (YR) drains into the East China Sea (ECS) at Shanghai, the largest city in China. The lower YR–ECS shelf system can be defined as five oceanographic regions (Fig. 1): lower river, estuary, coast, open shelf and upwelling area located at the shelf edge (Zhu et al., 2011a). Surface sediments (Fig. 1) were collected from the lower river (0–2 cm), away from the main axis of the dredged shipping channel, by the R/V Jiang Yu in November 2005 using 10 cm diameter multi-corers, and from the estuary-shelf area (0–5 cm) by the R/V Dong Fang Hong 02 in November 2007 using a box corer. Samples were immediately frozen onboard upon collection. Lipids were extracted and analyzed as described by Zhu et al. (2011b). In brief, the total lipid extracts (TLEs) were obtained by ultrasonic extraction of homogenized sediments and split into four fractions over a silica gel column (0.4 g of silica gel 60, 220–400 mesh, 1% deactivated; Fluka). A hydrocarbon fraction (F1) containing ab-C30-hopane was eluted with 4 ml n-hexane and an alcohol fraction (F3) containing sterols and tetrahymanol was eluted with 6 ml NH2-saturated CH2Cl2 [F3; derivatised using bis-(trimethylsilyl)trifluoroacetamide]. Fractions were analyzed using a Thermoquest Finnigan TRACE gas chromatography (GC) instrument, interfaced to a Thermoquest Finnigan TRACE mass spectrometry (MS) instrument (Zhu et al., 2011b). A fused silica column (50 m  0.32 mm) coated with CP Sil-5 (film thickness 0.25 lm) was used with He as carrier gas at constant flow. Electron ionization at 70 eV was used, with scanning from m/z 50 to 650 and a cycle time of 1.7 scan s1. The interface was at 300 °C and the ion source at 240 °C. Compounds of interest were assigned by comparing retention times and mass spectra with those in the literature and quantified using internal standards of 5a-androstane (for the

⇑ Corresponding author. Present address: MARUM, University of Bremen, P.O. Box 330 440, 28334 Bremen, Germany. Tel.: +49 421218 65702; fax: +49 421 218 65715. E-mail address: [email protected] (C. Zhu). 0146-6380/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.orggeochem.2012.09.008

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C. Zhu et al. / Organic Geochemistry 53 (2012) 95–98

Fig. 1. Sampling sites (open diamonds) and oceanographic setting in the lower Yangtze River–ECS shelf system (1, lower river; 2, estuary; 3, coast; 4, offshore upwelling area; 5, the open shelf).

F1 fraction) and 5a-androstan-3b-ol (for the F3 fraction, assuming a relative response factor of 1:1. 3. Results and discussion Eukaryote-derived sterols [phytosterols; including D5-stenols and 5a(H)-stanols], 5b(H)-stanols (including coprostanol, i.e. 5b-cholestan-3b-ol, epicoprostanol, i.e. 5b-cholestan-3a-ol, 5bcampestanol and 5b-stigmastanol), tetrahymanol, and 17a,21b(H)C30-hopane (ab-C30-hopane) were found in the surface sediments of the lower YR–ECS shelf system (Table 1). The concentration of phytosterols increases from the lower river to the open shelf (Fig. 2a). In contrast, the concentration of contamination biomarkers, including total 5b(H)-stanols (Fig. 2b) reflective of sewage input (Bull et al., 2002) and petroleum-derived ab-C30-hopane (Fig. 2b) significantly decreases from the river to the open shelf, with 5b(H)-stanols undetectable (i.e. <1 ng g1 sediment) in offshore sediments. Notably, the river is also characterized by the highest values of the ratios of [5a(H)-stanols]/[D5-stenols] for the entire YR–ECS system examined here. For example, the mean values of cholestan-3b-ol/cholest-5-en-3b-ol (27D/27D5), 24-methylcholestan-3b-ol/24-methylcholes-5-en-3b-ol (28D/28D5), and 24ethylcholestan-3b-ol/24-ethylcholest-5-en-3b-ol (29D/29D5) were 3.1 ± 3.1, 2.3 ± 0.9 and 1.8 ± 1.5, respectively (Fig. 2c), in the river surface sediments. All of these are more than an order of magnitude greater than values typically observed in living organisms (<0.2; Gagosian et al., 1980) and sharply decrease to 0.5 ± 0.6, 0.5 ± 0.4, and 0.9 ± 0.7, respectively, in the coastal region (Fig. 2c).

Fig. 2. Regional mean concentration (mg g1 TOC) of tetrahymanol and phytosterols (a) ab-C30 hopane and total 5b-stanols (b), and regional mean ratio of [tetrahymanol]/[phyto-sterols] and [5a(H)-stanol]/[D5-stenol] (i.e. 27D/27D5, 28D/28D5, 29D/29D5), (c) in surface sediments from the lower YR–ECS shelf system.

Phytosterols are ubiquitous in eukaryotes and anaerobic degradation of D5-stenols produces two groups of stereoisomers, the 5a(H)-stanols and the 5b(H)-stanols. Reduction of D5-sterols to corresponding 5a(H)-stanols, mediated by anaerobic bacteria, commonly occurs at the water–sediment interface and in peat bogs, so the high values of [5a(H)-stanols]/[D5-stenols] have been proposed to indicate reducing conditions (i.e. Nishimura, 1978; Wakeham, 1989). However, preferential preservation of 5a(H)-stanols over D5-stenols during diagenesis (Nishimura, 1978) and direct input of 5a(H)-stanols from freshwater organisms (e.g. dinoflagellates; Robinson et al., 1984) can also result in high values of [5a(H)-stanols]/[D5-stenols]. In the YR–ECS setting, the river is much shallower, with higher sedimentation rate than the open shelf, implying sedimentary organic matter (OM) is subject to more extensive diagenetic alteration in the ECS than in the river. Consequently, elevated values of [5a(H)stanols]/[D5-stenols] would be expected in the ECS open shelf. However, the opposite is observed (Fig. 2c), suggesting that preferential preservation of 5a(H)-stanols over D5-stenols is

Table 1 Regional sampling number (n) and mean biomarker concentration (mg g1 TOC) and biomarker ratios in surface sediments of the lower YR–ECS system.

Lower river Estuary Coast Upwelling Open shelf

n

Phytosterols

Tetrahymanol

R5b-stanols

ab-C30 hopane

27D/27D5

28D/28D5

29D/29D5

½Tetrahymanol ½phytosterols

10 11 17 4 44

0.052 ± 0.030 0.110 ± 0.051 0.201 ± 0.239 0.157 ± 0.040 0.216 ± 0.142

0.019 ± 0.007 0.016 ± 0.008 0.012 ± 0.009 0.008 ± 0.003 0.015 ± 0.013

0.011 ± 0.007 0.008 ± 0.017 0.000 ± 0.001 0.000 ± 0.000 0.000 ± 0.001

0.092 ± 0.045 0.034 ± 0.021 0.016 ± 0.014 0.006 ± 0.003 0.013 ± 0.010

3.1 ± 3.1 3.0 ± 3.0 0.5 ± 0.6 1.0 ± 0.3 1.1 ± 1.7

2.3 ± 0.9 1.8 ± 1.5 0.5 ± 0.4 0.5 ± 0.1 0.4 ± 0.3

1.8 ± 1.5 2.1 ± 1.4 0.9 ± 0.7 1.3 ± 0.3 1.2 ± 0.7

0.4 ± 0.2 0.2 ± 0.1 0.1 ± 0.1 0.1 ± 0.0 0.1 ± 0.1

C. Zhu et al. / Organic Geochemistry 53 (2012) 95–98

Fig. 3. Cross plots of 27D/27D5 vs. 29D/29D5 ratio (R2 0.91, p < 0.001; a), 27D/27D5 vs. 28D/28D5 ratio (R2 0.51, p < 0.001; b), and [5b-stanol]/[phytosterol] vs. [phytostanols]/[phytostenols] ratio (R2 0.40, p < 0.001; c) in surface sediments from the lower Yangtze River and estuary [Note, in panel b, one sample from the estuary (gray dot) is excluded from the correlation as an outlier].

unlikely. Moreover, negative correlation between dinosterol concentration and [5a(H)-stanols]/[D5-stenols] ratios (i.e. 27D/27D5, 28D/28D5, and 29D/29D5; R 0.39 to 0.53, p < 0.001; figures not shown) likely exclude a significant input of 5a(H)-stanols from freshwater dinoflagellates as a cause for the observed spatial trends. Instead, positive correlation among all three molecular pairs of [5a(H)-stanols]/[D5-stenols] in the river-estuary sediments (Fig. 3a and b) suggests that all have experienced systematic conversion of D5-stenols to 5a(H)-stanols under reducing conditions. It is possible that this has not occurred in the river itself and is,

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for example, associated with the sewage discharge, implying that the 5a-stanols are allochthonous. Alternatively, and consistent with other lines of evidence, 5a-stanols are produced in situ and the high values of [5a(H)-stanols]/[D5-stenols] likely reflect reducing, possibly anoxic, conditions in at least parts of the Yangtze riverbed. Indeed, in situ methanogenic activity is suggested for the river sediments by high values of [GDGT-0]/[GDGT-5] (1.96 ± 0.37; Zhu et al., 2011c), with values >2 indicative of significant methanogen input (Blaga et al., 2009), and for the lower YR itself by methane super-saturation of waters (Zhang et al., 2004). Such observations are consistent with at least a partially reducing environment in the lower river. The lower river is also characterized by a significantly lower phytosterol concentration relative to the other four regions (Fig. 2a), likely suggesting lower primary productivity. The seaward increase in phytosterol concentration strongly contrasts with the distribution of tetrahymanol (Fig. 2a), a membrane component of ubiquitous heterotrophic ciliates, whose concentration decreases offshore (except for the sandy/erosional open shelf where extremely low total organic carbon, TOC, results in an apparent elevated concentration). Ciliates modify their lipid composition with their diet: tetrahymanol is biosynthesized if ciliates feed on bacteria rather than sterol-bearing organisms but is not produced when exogenously-supplied sterols are available (Harvey and McManus, 1991; Holler et al., 1993). Both the absolute concentration of tetrahymanol (Fig. 2a) and values of [tetrahymanol]/[phytosterols] decrease (Fig. 2c) remarkedly seaward, suggesting a lack of sterol-bearing prey, and therefore lower primary production in the river than other settings. The relatively low amount of algal biomass in the river, inferred from sedimentary phytosterols and tetrahymanol, is consistent with the much lower Chl a concentration in the lower river–upper estuary zone than in the middle–lower estuary and adjacent shelf (Chai et al., 2006). The 5b(H)-stanols have long been suggested as biomarkers for tracking human and animal waste introduced to natural environments (McCalley et al., 1981; Leeming et al., 1996; Bull et al., 2002). Their occurrence in the river and rapid decrease seaward suggests an input of organic pollution from sewage discharge. Moreover, shipping activities also contribute to organic pollution in the river: the mean concentration of ab-C30-hopane, a petroleum-derived product, is four times higher than the mean concentration of total phytosterols in the river. Beyond the river, ab-C30-hopane concentration decreases sharply. Indeed, Wu et al. (2007) calculated, using a d13C approach, that anthropogenically sourced OM comprised up to 20–50% of the particulate organic carbon (POC) in YR sites close to big cities. Biological degradation of large quantities of anthropogenic pollutants from municipal waste and petroleum hydrocarbons can result in extensive consumption of dissolved O2 in rivers (e.g. Mallin, 2000; Mallin et al., 2002). If sufficiently significant [e.g. they account for up to 50% of the POC, as estimated by Wu et al. (2007)], this added OM input could ultimately lead to O2 depletion or even the inferred anoxic and methanogenic conditions in parts of the YR channel. Indeed, a positive correlation between [5b-stanol]/[phytosterol] and [phytostanols]/[phytostenols] (R2 0.40, p < 0.001; Fig. 3c) ratios argues that a greater proportion of organic pollutants is associated with a high degree of algal biomarker reduction, and could contribute to reducing conditions. Alternatively, the high organic input could lead to eutrophication and algal blooms, which also would consume O2 during their decay (Gooday et al., 2009); however, as noted above, algal productivity in the lower river and upper estuary appears to be low, such that organic pollution-induced O2 depletion seems more likely.

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4. Conclusions Phytosterols, 5b(H)-stanols, tetrahymanol and ab-C30-hopane have been quantified in surface sediments from the lower YR to the ECS shelf edge. Distributions of these biomarkers suggest that: (i) there were significant contributions from sewage and petroleum pollutants to riverbed sedimentary OM, (ii) algal production was likely suppressed in the lower YR and (iii) reducing, probably anoxic, conditions at least partially exist in the riverbed. Based on the relationship between the distribution of pollutants and algal biomarkers, we further suggest that massive organic pollutant input can impact on the riverbed redox environments. Acknowledgements C.Z. recognizes the Higher Education Funding Council for England (HEFCE) and the University of Bristol for a Ph.D. scholarship. J.-M. P. thanks the Public Science and Technology Research Projects of Ocean for support (Grant No. 201005034). We would also like to thank two anonymous reviewers for constructive comments. Guest Associate Editor—T. Eglinton References Blaga, C.I., Reichart, G.J., Heiri, O., Sinninghe Damsté, J.S., 2009. Tetraether membrane lipid distributions in water-column particulate matter and sediments: a study of 47 European lakes along a north–south transect. Journal of Paleolimnology 41, 523–540. Bull, I.D., Lockheart, M.J., Elhmmali, M.M., Roberts, D.J., Evershed, R.P., 2002. The origin of faeces by means of biomarker detection. Environment International 27, 647–654. Chai, C., Yu, Z., Song, X., Cao, X., 2006. The status and characteristics of eutrophication in the Yangtze River (Changjiang) Estuary and the adjacent East China Sea, China. Hydrobiologia 563, 313–328. Gagosian, R.B., Smith, S.O., Lee, C., Farrington, J.W., Frew, N.M., 1980. Steroid transformation in recent marine sediments. In: Douglas, A.G., Maxwell, J.R. (Eds.), Advances in Organic Chemistry 1979. Pergamon Press, Oxford, pp. 407– 419. Gooday, A.J., Jorissen, F., Levin, L.A., Middelburg, J.J., Naqvi, S.W.A., Rabalais, N.N., Scranton, M., Zhang, J., 2009. Historical records of coastal eutrophicationinduced hypoxia. Biogeosciences 6, 1707–1745. Harvey, H.R., Mcmanus, G.B., 1991. Marine cliates as a widespread source of tetrahymanol and hopan-3b-ol in sediments. Geochimica et Cosmochimica Acta 55, 3387–3390.

Holler, S., Pfennig, N., Neunlist, S., Rohmer, M., 1993. Effect of a non-methanogenic symbiont and exogenous stigmasterol on the viability and tetrahymanol content of the anaerobic ciliate Trimyema compressum. European Journal of Protistology 29, 42–48. Leeming, R., Ball, A., Ashbolt, N., Nichols, P., 1996. Using faecal sterols from humans and animals to distinguish faecal pollution in receiving waters. Water Research 30, 2893–2900. Mallin, M.A., 2000. Impacts of industrial-scale swine and poultry production on rivers and estuaries. American Scientist 88, 26–37. Mallin, M.A., Posey, M.H., Mciver, M.R., Parsons, D.C., Ensign, S.H., Alphin, T.D., 2002. Impacts and recovery from multiple hurricanes in a Piedmont-Coastal Plain river system. BioScience 52, 999–1010. McCalley, D.V., Cooke, M., Nickless, G., 1981. Effect of sewage treatment on faecal sterols. Water Research 15, 1019–1025. Nishimura, M., 1978. Geochemical characteristics of high reduction zone of stenols in Suwa sediments and environmental-factors controlling conversion of stenols into stanols. Geochimica et Cosmochimica Acta 42, 349–357. Report on the Marine Environmental Quality in China, 2001. The State Oceanic Administration, China (in Chinese). Robinson, N., Eglinton, G., Brassell, S.C., Cranwell, P.A., 1984. Dinoflagellate origin for sedimentary 4a-methylsteroids and 5a(H)-stanols. Nature 308, 439–442. Wakeham, S.G., 1989. Reduction of stenols to stanols in particulate matter at oxic anoxic boundaries in sea-water. Nature 342, 787–790. Wong, C.M., Williams, C.E., Pittock, J., Collier, U., Schelle, P., 2007. World’s Top 10 Rivers at Risk. WWF International, Gland, Switzerland. . Wu, Y., Zhang, J., Liu, S.M., Zhang, Z.F., Yao, Q.Z., Hong, G.H., Cooper, L., 2007. Sources and distribution of carbon within the Yangtze River system. Estuary Coastal Shelf Science 71, 13–25. Yang, S.L., Li, M., Dai, S.B., Liu, Z., Zhang, J., Ding, P.X., 2006. Drastic decrease in sediment supply from the Yangtze River and its challenge to coastal wetland management. Geophysics Research Letters 33, L06408. Zhang, G.L., Zhang, J., Kang, Y.B., Liu, S.M., 2004. Distributions and fluxes of methane in the East China Sea and the Yellow Sea in spring. Journal of Geophysical Research 109, 1–10. Zhou, M.J., Shen, Z.L., Yu, R.C., 2008. Responses of a coastal phytoplankton community to increased nutrient input from the Changjiang (Yangtze) River. Continental Shelf Research 28, 1483–1489. Zhu, C., Wang, Z.H., Xue, B., Yu, P.S., Pan, J.M., Wagner, T., Pancost, R.D., 2011a. Characterizing the depositional settings for sedimentary organic matter distributions in the Lower Yangtze River–East China Sea Shelf System. Estuary Coastal Shelf Science 93, 182–191. Zhu, C., Wagner, T., PanJ, M., Pancost, R.D., 2011b. Multiple sources and extensive degradation of terrestrial sedimentary organic matter across an energetic, wide continental shelf. Geochemistry Geophysics Geosystem 42, 376–386. Zhu, C., Wiejers, J.W.H., Wagner, T., Pan, J.M., Chen, J.F., Pancost, R.D., 2011c. Sources and distributions of tetraether lipids in surface sediments across a large riverdominated continental margin. Organic Geochemistry 42, 376–386. Zhu, Z.Y., Zhang, J., Wu, Y., Zhang, Y.Y., Lin, J., Liu, S.M., 2011d. Hypoxia off the Changjiang (Yangtze River) Estuary: oxygen depletion and organic matter decomposition. Marine Chemistry 125, 108–116.