- Email: [email protected]
Restriction of sulfate reduction on the bioavailability and toxicity of trace metals in Antarctic lake sediments
Marine Pollution Bulletin xxx (xxxx) xxxx
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Restriction of sulfate reduction on the bioavailability and toxicity of trace metals in Antarctic lake sediments Yuanqing Chena, Jingwen Gea, Tao Huanga,b, , Lili Shena, Zhuding Chuc, Zhouqing Xiec ⁎
a
School of Resources and Environmental Engineering, Anhui University, Hefei 230601, China Anhui Province Key Laboratory of Wetland Ecosystem Protection and Restoration, Anhui University, Hefei 230601, China c Anhui Key Laboratory of Polar Environment and Global Change, School of Earth and Space Sciences, University of Science and Technology of China, Hefei 230026, Anhui, China b
ARTICLE INFO
ABSTRACT
Keywords: Trace metals Bioavailability Toxicity Ornithogenic sediments Sulfate reduction AVS
In this study, Acid-Volatile Sulfur (AVS), trace metals Cu, Cd and Zn and their chemical speciation based on BCRsequential and simultaneous extraction (SEMs) in Antarctic lake sediments (Y2-1 and YO) were analyzed to investigate the restriction of sulfate reduction on the bioavailability and toxicity of trace metals. Much higher trace metals in Y2-1 indicating a primary source from penguin guano. The main chemical speciation of Cu and Cd in Y2-1 was their oxidizable fraction in contrast to those of weak-acid extraction in YO. Lower ratio of ΣSEM/ AVS in Y2-1 indicating less toxicity of the trace metals. The main chemical speciation of Cd in Y2-1 was their oxidizable fraction in contrast to that exchangeable fraction in penguin guano, indicating that although amounts of Cd was transported from marine to lake by penguins, strong sulfate reduction in ornithogenic sediments restricts the bioavailability and toxicity of Cd through the formation of insoluble sulfide.
1. Introduction Trace metals in water body could be adsorbed physically by minerals in sediments, and be transformed to other chemical speciation induced by variable physicochemical conditions in a sediment-water interface (Sheoran and Sheoran, 2006; Park et al., 2016; Alberti et al., 2018). The Acid-Volatile Sulfur (AVS) in sediments was mainly from the dissimilatory reduction of sulfate, it plays a vital role in the distribution of many bivalent metal ions between sediments and the pore waters and thus restricts the bioavailability, toxicity and mobility of trace metals (Machado et al., 2004; Chai et al., 2017; Shyleshchandran et al., 2018). After the initial report of the strong influence from AVS on the toxicity of Cd in sediments (Di Toro et al., 1990), sulfide in sediments has been taken as one of the key indices for the evaluation of trace metals pollution in the aquatic environment. As an important indices on the evaluation of water pollution, the total quantity of trace metals, however, could not reflect their potential toxicity completely (Tessier et al., 1979; Akcay et al., 2003; Cao et al., 2015), because different chemical speciation of trace metals has different environmental behaviors and ecotoxicology (Brümmer, 1986; Massas et al., 2009; Shikazono et al., 2012). Chemical speciation of trace metals thus was used commonly to evaluate the metals ecotoxicology and their environmental safety (Giller et al., 1998; Nagajyoti et al., 2010). Therefore, it is a great
⁎
importance to study the relationship between sulfide and the various chemical speciation of trace metals to evaluate their bioavailability, toxicity and mobility comprehensively (Yu et al., 2001; Rosado et al., 2016; Shyleshchandran et al., 2018). High levels of organic and inorganic matters, such as trace metals, sulfur, phosphorus and persistent organic pollutants, were transported from the marine to land by seabirds and marine mammals in Polar Regions (Blais et al., 2005, 2007; Michelutti et al., 2008, 2010; Sun et al., 2013; Perfetti-Bolaño et al., 2018). These matters were then washed into lakes or ponds by runoff and formed the ornithogenic or excrement sediments (Sun et al., 2000, 2013; Emslie et al., 2014). Very high levels of trace metals (Brimble et al., 2009; Huang et al., 2011, 2014; Lou et al., 2015), as well as total sulfur and dimethylsulfide, have been measured in these ornithogenic sediments (Sun et al., 2000; Xie et al., 2002; Huang et al., 2009), and thus could have significant impacts on these lacustrine environment. Human activities near scientific stations in the Antarctic Fildes Peninsula and Ardley Island also induced trace metal pollutions in the lake system (Chu et al., 2019). Such of those studies focused mainly on the total quantity of trace metals transported by seabirds from the marine to lakes and ponds, rather than the bioavailability of trace metals and thus their potential biological toxicity. Here, we collected a lake ornithogenic sediment core Y2-1 from Y2 lake at Ardley Island, and a pristine lake sediment
Corresponding author at: School of Resources and Environmental Engineering, Anhui University, Hefei 230601, China. E-mail address: [email protected] (T. Huang).
https://doi.org/10.1016/j.marpolbul.2019.110807 Received 23 October 2019; Received in revised form 3 December 2019; Accepted 6 December 2019 Available online 09 December 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
Please cite this article as: Yuanqing Chen, et al., Marine Pollution Bulletin, https://doi.org/10.1016/j.marpolbul.2019.110807
Marine Pollution Bulletin xxx (xxxx) xxxx
Y. Chen, et al.
core YO from Yanou lake at Fildes Peninsula, Antarctic, to analyze the AVS and chemical speciation of trace metals Cu, Cd and Zn in these sediments, to compare and contrast the bioavailability and toxicity of trace metals in these two different lake systems. We aimed to show that strong sulfate reduction in penguin ornithogenic sediments restricts the bioavailability and toxicity of trace metals effectively through the formation of insoluble sulfides.
with electric heating. The digested subsamples were analyzed for Cu, Zn and Cd by using the inductively coupled plasma mass spectroscopy (ICP-MS). For the chemical speciation of trace metal analyses, a modified method of BCR-sequential extraction (Fathollahzadeh et al., 2014), was used to extract and analyze the speciation of trace metals using ICP-MS. The trace metal speciation from BCR-sequential extractions includes four fractions, weak-acid extraction (F1), the reducible fraction (F2), the oxidizable fraction (F3) and the residual fraction (F4). The AVS, total organic carbon (TOC), total nitrogen (TN) and total phosphorus (TP) in sediments were analyzed in our previous study (Chen et al., 2019). During the AVS analysis, one part of the extracts were analyzed for the content of simultaneously extracted metals (ΣSEM) by ICP-MS. Standard sediment reference materials (GSD-7a and GSD-12) were included with every batch of samples during the analyses of total trace metals. The analytical values for total trace metals are within ± 5% of the certified standards. Duplicate analysis on the extracts in Y2-1 sediments (4 cm, 15 cm, 34 cm and 52 cm) was performed to validate the BCR-sequential and simultaneous extraction procedure and for quality control of the analytical data, and the recovery rate was 80.4%–127.1%.
2. Materials and methods 2.1. Study area Fildes Peninsula (62°08′48″ – 62°14′02″S, 58°53′40″ – 59°01′50″W) locates in the southwest of King George Island, is the largest regional ice-free area with about 30 km2. It is a flat terrain with 10 km long and 2.5–4 km wide, and the highest altitude is about 70 m (Michel et al., 2014). Many scientific stations were established in this peninsula, and lots of scientists worked there every year, especially in the austral summer seasons. Ardley Island is connected to Fildes Peninsula with a sandbar. Although the local climate is cold, 80% of the island is covered with lichen and moss. Ardley Island was once a penguin island, and some lakes there were affected by penguin activities while most lakes in Fildes Peninsula were not.
3. Results 3.1. Total trace metals and the TP, TN and TOC
2.2. Sample collection and pretreatment
Vertical distribution of the TP, TN, TOC, Cu, Zn and Cd in Y2-1 and YO sediments was plotted in Fig. 2. In Y2-1 sediments, the content of TP, TN and TOC was 2.31% ± 1.99%, 0.51% ± 0.66% and 2.52% ± 2.63%, respectively, much higher than those in YO. Similarly, the total concentrations of Cu, Zn and Cd in Y2-1 were much higher than those in YO. TP, TN, TOC, Cu, Zn and Cd in Y2-1 showed a relatively consistent vertical trend, with high values in the depth of 15 cm and below the 45 cm, and lowest values between 40 cm and 45 cm (Fig. 2). While in YO sediments, TP, TN, TOC, Cu, Zn and Cd showed a different vertical trend.
During the 29th Chinese Antarctic Expedition in austral summer 2013, two sediment cores Y2-1 and YO were retrieved from Y2 lake at Ardley Island and Yanou Lake at Fildes Peninsula, respectively (Fig. 1). Y2-1 was an ornithogenic sediment core with a length of 60 cm; it was sectioned into 60 subsamples at a 1 cm interval. YO sediments were not affected by penguin guano, it was 30 cm long and sectioned into 30 subsamples at 1 cm intervals. In this study, 16 subsamples in Y2-1 and 11 in YO were selected for analysis. Before geochemical analyses, one part of subsample was stored in −20 °C, while the other part was freeze-dried and then powdered through a 200-mesh sieve.
3.2. SEMs, AVS and ΣSEM/AVS
2.3. Sample analyses
The simultaneous extraction of Cu, Zn and Cd, AVS and the ratio of ΣSEM/AVS in Y2-1 and YO sediments were plotted in Fig. 3. The concentrations of SEMCu, SEMZn, SEMCd and AVS in Y2-1 sediments
For trace metal analyses, 0.1 g of each powder subsamples were taken, weighed, and digested (HClO4-HNO3-HF) in a Teflon crucible
Fig. 1. Study area and sampling sites on Fildes Peninsula and Ardley Island. 2
Marine Pollution Bulletin xxx (xxxx) xxxx
Y. Chen, et al.
Fig. 2. Vertical distribution of Cu, Zn, Cd, TOC, TN and TP in Y2-1 and YO sediments.
were 3.86 ± 2.53 umol/g, 6.58 ± 2.99 umol/g, 0.024 ± 0.013 umol/g and 10.33 ± 13.09 umol/g, respectively, much higher than those in YO. SEMCu, SEMZn, SEMCd and AVS in Y2-1 sediments showed a consistent trend in vertical distributions; they reached higher values in 15 cm, lowest values in 40 cm–45 cm and the highest in the bottom sections. The concentrations of SEMCu, SEMZn, SEMCd and AVS in YO sediments were 0.44 ± 0.04 umol/g, 0.35 ± 0.04 umol/g, 0.0019 ± 0.0002 umol/g and 0.15 ± 0.16 umol/g, respectively. The AVS in YO sediments increased slightly at 15 cm and reached the highest value in the bottom 30 cm. SEMCu, SEMZn and SEMCd in YO sediments showed a different vertical distribution.
4. Discussion 4.1. Comparison of trace metals in different sediments in Antarctica The Y2-1 sediment was collected from Y2 Lake at Ardley Island, and a ground-breaking study identified the Cu, Zn, Sr, Ba, Ca, P, S, F and Se in this lake sediments as penguin bio-elements which originated mainly from penguin guanos (Sun et al., 2000). The total concentrations of trace metals Cu, Zn and Cd in Y2-1, YO and other Antarctic sediments, as well as fresh penguin guano, were list in Table 1. It showed that the total quantity of trace metals of Cu, Zn and Cd in Y2-1 ornithogenic sediments were similar to those in fresh penguin guano (Chu et al., 2019), and much higher than those in YO and other Antarctic sediments, indicate that all of them were mainly from penguin guano. A number of studies indicated an enrichment of trace metals Cu, Zn, Pb, As, Cd, Hg in Antarctic ornithogenic sediments (Sun and Xie, 2001; Ancora et al., 2002; Xie and Sun, 2008; Huang et al., 2011, 2014; Lou et al., 2015; Perfetti-Bolaño et al., 2018). The vertical distributions of the total Cu, Zn, Cd, TOC, TN and TP in Y2-1 sediments show a consistent trend with more fluctuant (Fig. 2), indicate that all of them were mainly from the penguin guano inputs, and higher levels indicate higher penguin populations in the lake area (Sun et al., 2000). The concentrations of Cu and Zn in YO sediments from a pristine Yanou lake were very low, similar to those of sediments from Ferraz Station and Admiralty Bay (Santos et al., 2005; Ribeiro et al., 2011), indicate that they came mainly from a natural deposition. Consequently, in YO sediments, only Cd and nutrients show a similar vertical trend (Fig. 2),
3.3. Chemical speciation of Cu, Zn and Cd The chemical speciation of Cu, Zn and Cd in Y2-1 and YO sediments were plotted in Fig. 4. The primary chemical speciation of Cu in Y2-1 sediments was the oxidizable fraction (53.43%), in contrast to that of the weak-acid extraction (43.79%) in YO. While the primary chemical speciation of Zn in Y2-1 sediments was the weak-acid extraction (35.70%) and a residual fraction (29.81%), in contrast to that of the oxidizable fraction (37.66%) in YO. The concentration of Cd in Y2-1 sediments was as high as 4.54 ± 2.99 μg/g, with the primary speciation of the oxidizable fraction (41.76%) in contrast to that of the residual fraction (47.54%) as well as the weak-acid extraction (35.91%) in YO.
3
Marine Pollution Bulletin xxx (xxxx) xxxx
Y. Chen, et al.
Fig. 3. Vertical distribution of SEMs, AVS and ratio of ΣSEM/AVS in Y2-1 and YO sediments.
with the lowest and highest values in the depths of 12 cm and 19 cm, respectively. The abnormal distribution of trace metals and nutrients in Yanou Lake may be associated with several influences such as climate change, tephra deposition and transition of sediment environment which have been reported previously (Fretwell et al., 2010; Roberts et al., 2017).
metal ions in pore water of the sediments and form insoluble sulfides (Machado et al., 2004; Chai et al., 2017; Shyleshchandran et al., 2018). The sulfate reduction in sediments was determined by the abundance of Sulfate-Reducing Bacteria (SRB) (Brüchert et al., 2001; Foti et al., 2007; Couture et al., 2016; Li et al., 2018). Some studies showed that the abundance of SRB in sediments reached a peak value at a depth of 10 cm–50 cm in sediments (D'Hondt et al., 2004; Leloup et al., 2009; Zhang et al., 2012), which was consistent with the depth of peak levels of AVS in Y2-1 and YO sediments. The ratio of ΣSEM/AVS in sediments has been used widely to evaluate the biological toxicity of trace metals (Besser et al., 2008; Chai et al., 2015; Shyleshchandran et al., 2018), and the trace metals would present biological toxicity if the ratio > 1.0, and vice versa. Generally, the mean ratio of ΣSEM/AVS in Y2-1 sediments was lower than that in YO (7.01 vs 36.66) (Fig. 2), suggests that the biological toxicity of trace metals in Y2-1 sediments was less than that in YO. The trace metals in Y2-1 sediments present no toxicity in the depths of 8 cm, 12 cm, 48 cm and 56 cm with the ratios between 0.40 and 0.80, and weak toxicity in the depths of 15 cm, 19 cm and 52 cm with the ratios range from 1.08 to 1.48. While the trace metals in YO sediments present high toxicity in the depths of 3 cm, 5 cm, 8 cm and 12 cm with a mean ratio of 91.01, and weak toxicity in the depths of 26 cm, 28 cm and 30 cm with the ratios range from 1.70 to 3.77. The trace metals in Y2-1 sediments were much higher than those in YO, while the biological toxicity of them in Y2-1 sediments was less than that in YO, indicating that although the penguins transported high levels of trace metals and caused pollution to the lake system, the S2− reduced from sulfate that promoted by the
4.2. Restriction of AVS on the bioavailability and toxicity of trace metals The consistent vertical trends of AVS and SEMs in Y2-1 sediments suggest that the S2− from sulfate reduction could combine with ions of Cu2+, Zn2+ and Cd2+ effectively, and thus plays an important role in restricting the bioavailability and toxicity of trace metals. Pearson correlation analysis between AVS and SEMs in YO sediments, however, showed the insignificant relationship (Table 2), indicate that trace metals of Cu, Zn and Cd in Yanou lake were not affected by S2− in contrast to those in Y2-1. The significant positive relationship among SEMZn, SEMCd and ΣSEM in YO sediments (Table 2) suggests that Zn and Cd were the main components of ΣSEM in YO sediments in this study. The ratio of ΣSEM/AVS in sediments was associated closely with the biological toxicity of trace metals, and higher ratios correspond to higher toxicity. It was suggested that there was negligible toxicity when the bivalent metal ions were less than S2− in sediments (Di Toro et al., 1992; Prica et al., 2008; Pignotti et al., 2018). The toxicity of trace metals in sediments was influenced significantly by sulfate reduction, because the S2− from sulfate reduction can combine with the divalent 4
Marine Pollution Bulletin xxx (xxxx) xxxx
Y. Chen, et al.
Fig. 4. Chemical speciation of Cu, Zn and Cd in Y2-1 and YO sediments.
high levels of organic matter (Chen et al., 2019), could restrict the biological toxicity of trace metals.
4.3. Chemical speciation of Cu, Zn and Cd and their mobility The chemical speciation of Cu, Zn and Cd in Y2-1 and YO were plotted in Fig. 4. Trace metals pollution in sediments cannot be
Table 1 Concentrations of Cu, Zn and Cd (ug/g) in the Antarctic sediments and penguin guano. Sampling Site
Materials
Cu
Zn
Cd
Reference
Y2-1 YO Ardley Island Fildes Peninsula Admiralty Bay Ferraz Station Ardley Island
Lake core sediments Lake core sediments Lake surface sediments Lake surface sediments Lake sediments Coastal sediments Penguin guanos
56–779 32–49 166–526 52–144 47–84 44 926
116–881 44–63 121–492 49–68 44–89 52 573
0.65–9.99 0.19–0.27 1.0–4.6 0.5–1.4 0.4–0.9 ND 2.0
This study This study Chu et al., 2019 Chu et al., 2019 Ribeiro et al., 2011 Santos et al., 2005 Chu et al., 2019
ND means not determined. 5
Marine Pollution Bulletin xxx (xxxx) xxxx
Y. Chen, et al.
in Y2-1 sediments (Figs. 3, 4). This consistency, however, was not observed in YO. The oxidizable fraction of trace metals includes two parts, one is the fraction that bound to organic matters, and the other is the form of sulfides (AVS). The Pearson correlation analysis showed a significant positive relationship between AVS and the oxidizable fraction of Cu and Cd in Y2-1 sediments (Table 3), indicating that the sulfide was the primary form of the oxidizable fraction, and S2− from sulfate reduction in Y2-1 could combine ions of Cu and Cd effectively and form AVS. The oxidizable fraction was the main chemical speciation of Cu and Cd in Y2-1 sediments, while that of Zn occupied only a proportion of 19.20% in the total quantity (Fig. 4). This may be due to the different vulcanization of trace metals. For example, trace metals of Ni and Cd could be vulcanized mostly (100% and 81%) by S2−, while the Zn could be vulcanized just by 11%–16% (Huerta-Diaz et al., 1998; Charriau et al., 2011). A previous study on the penguin ornithogenic sediments from the Antarctic Ross sea area showed that the exchangeable fraction was the main chemical speciation of Cd (52.8%) in fresh penguin guano, while that exchangeable fraction of Cd decreased significantly in sediments and it was attributed to the complexation by high levels of organic matter (Lou et al., 2015). In the present study, the weak-acid extraction of Cd (include the fraction of exchangeable and carbonate bounded) occupied only 14.82% of the total Cd in Y2-1 sediments, while the oxidizable fraction occupied 41.76% (Fig. 4). The proportion of weakacid extraction of Cd correlated significantly with AVS in the layer of 8 cm–23 cm in Y2-1 (r = −0.99, p = .001) (Fig. 5), indicating once again that higher S2− reduce the mobility of Cd. In contrast to the sediments collected from ornithogenic soil pit in the McMurdo Dry Valleys in Lou et al. (2015), Y2-1 sediments in the present study were
Table 2 Correlation analysis for the SEMs and AVS in YO sediments.
AVS SEMCu SEMZn SEMCd ΣSEM ⁎⁎
AVS
SEMCu
SEMZn
SEMCd
ΣSEM
1.00
0.22 1.00
−0.15 0.15 1.00
−0.20 0.36 0.93⁎⁎ 1.00
−0.03 0.56 0.91⁎⁎ 0.93⁎⁎ 1.00
Correlation is significant at 0.01 level (2-tailed).
Table 3 Correlation analysis for the AVS and the oxidizable fraction of trace metals (F3) in Y2-1 sediments.
AVS Cu (F3) Zn (F3) Cd (F3) ⁎ ⁎⁎
AVS
Cu (F3)
Zn (F3)
Cd (F3)
1.00
0.78 1.00
0.16 0.09 1.00
0.70⁎⁎ 0.81⁎⁎ 0.60⁎ 1.00
⁎⁎
Correlation is significant at 0.05 level (2-tailed). Correlation is significant at 0.01 level (2-tailed).
reflected completely by its total concentrations (Cuong and Obbard, 2006; Shikazono et al., 2012), because it was associated mainly with the trace metal's mobility and biological toxicity which were determined by their chemical speciation (Fuentes et al., 2004; De la Fuente et al., 2008; Jia et al., 2018). The vertical distribution trend of AVS was consistent with that of the oxidizable fraction of Cu, Zn and Cd
Fig. 5. Correlation between the weak-acid extraction of trace metals and TOC and AVS in Y2-1 sediments (8 cm–23 cm). 6
Marine Pollution Bulletin xxx (xxxx) xxxx
Y. Chen, et al.
collected from Y2 Lake with a stronger anaerobic condition. Our previous study indicated a strong sulfate reduction in the Y2-1 sediments (Chen et al., 2019). Thus, it was indicated that the low weak-acid extraction of Cd in Y2-1 ornithogenic sediments was primarily due to the formation of insoluble sulfides by S2− that reduced from strong sulfate reduction, rather than the complexation by high organic matters. Finally, both of the ratio of ΣSEM/AVS and the chemical speciation of Cd in Y2-1 indicate that though the penguin populations transported high levels of trace metals to the Y2 lake system, the S2− reduced from sulfate reduction that promoted by the high organic matters can restrict the bioavailability, toxicity and mobility of Cd and Cu effectively, through the formation of insoluble sulfides.
Besser, J.M., Brumbaugh, W.G., Ivey, C.D., Ingersoll, C.G., Moran, P.W., 2008. Biological and chemical characterization of metal bioavailability in sediments from Lake Roosevelt, Columbia River, Washington, USA. Arch. Environ. Contam. Toxicol. 54, 557–570. Blais, J.M., Kimpe, L.E., McMahon, D., Keatley, B.E., Mallory, M.L., Douglas, M.S., et al., 2005. Ecology: Arctic seabirds transport marine-derived contaminants. Science 309, 445. Blais, J.M., Macdonald, R.W., Mackay, D., Webster, E., Harvey, C., Smol, J.P., 2007. Biologically mediated transport of contaminants to aquatic systems. Environ. Sci. Technol. 41, 1075–1084. Brimble, S.K., Foster, K.L., Mallory, M.L., Macdonald, R.W., Smol, J.P., Biais, J.M., 2009. High arctic ponds receiving biotransported nutrients from a nearby seabird colony are also subject to potentially toxic loadings of arsenic, cadmium, and zinc. Environ. Toxicol. Chem. 28, 2426–2433. Brüchert, V., Knoblauch, C., Jorgensen, B.B., 2001. Controls on stable sulfur isotope fractionation during bacterial sulfate reduction in arctic sediments. Geochim. Cosmochim. Acta 65, 763–776. Brümmer, G.W., 1986. Heavy Metal Species, Mobility and Availability in Soils. Springer. Cao, L., Tian, H., Yang, J., Shi, P., Lou, Q., Waxi, L., et al., 2015. Multivariate analyses and evaluation of heavy metals by chemometric BCR sequential extraction method in surface sediments from Lingdingyang Bay, South China. Sustainability 7, 4938–4951. Chai, M., Shen, X., Li, R., Qiu, G., 2015. The risk assessment of heavy metals in Futian mangrove forest sediment in Shenzhen Bay (South China) based on SEM-AVS analysis. Mar. Pollut. Bull. 97, 431–439. Chai, M., Li, R., Zan, Q., 2017. Effects of mangrove plants on heavy metal risk in sediment based on SEM-AVS analysis. Reg. Stud. Mar. Sci. 13, 12–18. Charriau, A., Lesven, L., Gao, Y., Leermakers, M., Baeyens, W., Ouddane, B., et al., 2011. Trace metal behaviour in riverine sediments: role of organic matter and sulfides. Appl. Geochem. 26, 80–90. Chen, Y., Shen, L., Huang, T., Chu, Z., Xie, Z., 2019. Transformation of sulfur species in lake sediments at Ardley Island and Fildes Peninsula, King George Island, Antarctic Peninsula. Sci. Total Environ. https://doi.org/10.1016/j.scitotenv.2019.135591. Chu, Z., Yang, Z., Wang, Y., Sun, L., Yang, W., Yang, L., et al., 2019. Assessment of heavy metal contamination from penguins and anthropogenic activities on Fildes Peninsula and Ardley Island, Antarctic. Sci. Total Environ. 646, 951–957. Couture, R.M., Fischer, R., Van Cappellen, P., Gobeil, C., 2016. Non-steady state diagenesis of organic and inorganic sulfur in lake sediments. Geochim. Cosmochim. Acta 194, 15–33. Cuong, D.T., Obbard, J.P., 2006. Metal speciation in coastal marine sediments from Singapore using a modified BCR-sequential extraction procedure. Appl. Geochem. 21, 1335–1346. De la Fuente, C., Clemente, R., Bernal, M.P., 2008. Changes in metal speciation and pH in olive processing waste and sulphur-treated contaminated soil. Ecotoxicol. Environ. Saf. 70, 207–215. D'Hondt, S., Jørgensen, B.B., Miller, D.J., Batzke, A., Blake, R., Cragg, B.A., et al., 2004. Distributions of microbial activities in deep subseafloor sediments. Science 306, 2216–2221. Di Toro, D.M., Mahony, J.D., Hansen, D.J., Scott, K.J., Hicks, M.B., Mayr, S.M., et al., 1990. Toxicity of cadmium in sediments: the role of acid volatile sulfide. Environ. Toxicol. Chem. 9, 1487–1502. Di Toro, D.M., Mahony, J.D., Hansen, D.J., John Scott, K., Carlson, A.R., Ankley, G.T., 1992. Acid volatile sulfide predicts the acute toxicity of cadmium and nickel in sediments. Environ. Sci. Technol. 26, 96–101. Emslie, S.D., Polito, M.J., Brasso, R., Patterson, W.P., Sun, L., 2014. Ornithogenic soils and the paleoecology of pygoscelid penguins in Antarctica. Quatern. Int. 352, 4–15. Fathollahzadeh, H., Kaczala, F., Bhatnagar, A., Hogland, W., 2014. Speciation of metals in contaminated sediments from Oskarshamn Harbor, Oskarshamn, Sweden. Environ. Sci. Pollut. Res. 21, 2455–2464. Foti, M., Sorokin, D.Y., Lomans, B., Mussman, M., Zacharova, E.E., Pimenov, N.V., et al., 2007. Diversity, activity, and abundance of sulfate-reducing bacteria in saline and hypersaline soda lakes. Appl. Environ. Microb. 73, 2093–2100. Fretwell, P.T., Hodgson, D.A., Watcham, E.P., Bentley, M.J., Roberts, S.J., 2010. Holocene isostatic uplift of the South Shetland Islands, Antarctic Peninsula, modelled from raised beaches. Quat. Sci. Rev. 29, 1880–1893. Fuentes, A., Lloréns, M., Sáez, J., Aguilar, M.I., Ortuño, J.F., Meseguer, V.F., 2004. Phytotoxicity and heavy metals speciation of stabilised sewage sludges. J. Hazard. Mater. 108, 161–169. Giller, K.E., Witter, E., Mcgrath, S.P., 1998. Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol. Biochem. 30, 1389–1414. Huang, T., Sun, L., Wang, Y., Liu, X., Zhu, R., 2009. Penguin population dynamics for the past 8500 years at Gardner Island, Vestfold Hills. Antarct. Sci. 21, 571–578. Huang, T., Sun, L., Wang, Y., Kong, D., 2011. Late Holocene Adélie penguin population dynamics at Zolotov Island, Vestfold Hills, Antarctica. J. Paleolimnol. 45, 273–285. Huang, T., Sun, L., Wang, Y., Chu, Z., Qin, X., Yang, L., 2014. Transport of nutrients and contaminants from ocean to island by emperor penguins from Amanda Bay, East Antarctic. Sci. Total Environ. 468, 578–583. Huerta-Diaz, M.A., Tessier, A., Carignan, R., 1998. Geochemistry of trace metals associated with reduced sulfur in freshwater sediments. Appl. Geochem. 13, 213–233. Jia, Y., Chen, W., Zuo, Y., Lin, L., Song, L., 2018. Heavy metal migration and risk transference associated with cyanobacterial blooms in eutrophic freshwater. Sci. Total Environ. 613, 1324–1330. Leloup, J., Fossing, H., Kohls, K., Holmkvist, L., Borowski, C., Jørgensen, B.B., 2009. Sulfate-reducing bacteria in marine sediment (Aarhus Bay, Denmark): abundance and diversity related to geochemical zonation. Environ. Microbiol. 11, 1278–1291. Li, X., Lan, S., Zhu, Z., Zhang, C., Zeng, G., Liu, Y., et al., 2018. The bioenergetics
5. Conclusions We analyzed the AVS, total Cu, Cd and Zn and their chemical speciation in the Antarctic penguin ornithogenic sediments Y2-1 and pristine lake sediments YO to investigate the restriction of sulfate reduction on the bioavailability and toxicity of these trace metals. Much higher levels of Cu, Cd and Zn in Y2-1 sediments were observed in contrast to those in YO. The toxicity of Cu, Cd and Zn in Y2-1 sediments was less than that in YO, indicated by a lower ratio of ΣSEM/AVS in Y21. The main chemical speciation of Cd was its oxidizable fraction in Y21 ornithogenic sediments, in contrast to the exchangeable fraction in the fresh guano. We concluded that although a large of poisonous Cd was transported from the marine to freshwater environment by penguin populations, the S2− reduced from sulfate that promoted by the transported high organic matters, could restrict the bioavailability and toxicity of Cd effectively through the formation of insoluble cadmium sulfide. Since the penguins and thus the ornithogenic sediments and soils distribute widely in the coastal Antarctic, our study would be help on the accurate evaluation of trace metals pollution from the marine to the lacustrine environment by penguin's activity, in the perspective of bioavailability, toxicity and mobility. Author contribution statement Tao Huang: Conceptualization, Methodology, Resources, WritingReviewing and Editing, Funding acquisition, Supervision. Yuanqing Chen: Data curation, Writing- Original draft preparation. Jingwen Ge: Data curation, Investigation. Lili Shen: Data curation, Investigation. Zhuding Chu: Investigation. Zhouqing Xie: Investigation. Declaration of competing interest The authors declare no conflict of interests. Acknowledgements This work was supported by the National Natural Science Foundation of China (No. 41476165) and the Science Research Project of Anhui Department of Education (No. KJ2019A0042). Samples in this study were provided by the BIRDS-Sediment system (Hefei). We thank the Chinese Arctic and Antarctic Administration and Polar Research Institute of China for logistical support in field work. References Akcay, H., Oguz, A., Karapire, C., 2003. Study of heavy metal pollution and speciation in Buyak Menderes and Gediz river sediments. Water Res. 37, 813–822. Alberti, G., Mussi, M., Quattrini, F., Pesavento, M., Biesuz, R., 2018. Metal complexation capacity of Antarctic lacustrine sediments. Chemosphere 196, 402–408. Ancora, S., Volpi, V., Olmastroni, S., Focardi, S., Leonzio, C., 2002. Assumption and elimination of trace elements in Adelie penguins from Antarctica: a preliminary study. Mar. Environ. Res. 54, 341–344.
7
Marine Pollution Bulletin xxx (xxxx) xxxx
Y. Chen, et al. mechanisms and applications of sulfate-reducing bacteria in remediation of pollutants in drainage: a review. Ecotoxicol. Environ. Saf. 158, 162–170. Lou, C., Liu, X., Nie, Y., Emslie, S.D., 2015. Fractionation distribution and preliminary ecological risk assessment of As, Hg and Cd in ornithogenic sediments from the Ross Sea region, East Antarctica. Sci. Total Environ. 538, 644–653. Machado, W., Carvalho, M.F., Santelli, R.E., Maddock, J.E.L., 2004. Reactive sulfides relationship with metals in sediments from an eutrophicated estuary in Southeast Brazil. Mar. Pollut. Bull. 49, 89–92. Massas, I., Ehaliotis, C., Gerontidis, S., Sarris, E., 2009. Elevated heavy metal concentrations in top soils of an Aegean island town (Greece): Total and available forms, origin and distribution. Environ. Monit. Assess. 151, 105–116. Michel, R.F., Schaefer, C.E., López-Martínez, J., Simas, F.N., Haus, N.W., Serrano, E., et al., 2014. Soils and landforms from Fildes Peninsula and Ardley Island, maritime Antarctica. Geomorphology 225, 76–86. Michelutti, N., Keatley, B.E., Brimble, S., Blais, J.M., Liu, H., Douglas, M.S., et al., 2008. Seabird-driven shifts in Arctic pond ecosystems. P. Roy. Soc. B-Biol. Sci. 276, 591–596. Michelutti, N., Blais, J.M., Mallory, M.L., Brash, J., Thienpont, J., Kimpe, L.E., et al., 2010. Trophic position influences the efficacy of seabirds as metal biovectors. P. Natl. Acad. Sci. USA. 107, 10543–10548. Nagajyoti, P.C., Lee, K.D., Sreekanth, T.V., 2010. Heavy metals, occurrence and toxicity for plants: a review. Environ. Chem. Lett. 8, 199–216. Park, J.H., Ok, Y.S., Kim, S.H., Cho, J.S., Heo, J.S., Delaune, R.D., et al., 2016. Competitive adsorption of heavy metals onto sesame straw biochar in aqueous solutions. Chemosphere 142, 77–83. Perfetti-Bolaño, A., Moreno, L., Urrutia, R., Araneda, A., Barra, R., 2018. Influence of Pygoscelis penguin colonies on cu and Pb concentrations in soils on the Ardley peninsula, maritime Antarctica. Water Air Soil Pollut. 229, 390. Pignotti, E., Guerra, R., Covelli, S., Fabbri, E., Dinelli, E., 2018. Sediment quality assessment in a coastal lagoon (Ravenna, NE Italy) based on SEM-AVS and sequential extraction procedure. Sci. Total Environ. 635, 216–227. Prica, M., Dalmacija, B., Rončević, S., Krčmar, D., Bečelić, M., 2008. A comparison of sediment quality results with acid volatile sulfide (AVS) and simultaneously extracted metals (SEM) ratio in Vojvodina (Serbia) sediments. Sci. Total Environ. 389, 235–244. Ribeiro, A.P., Figueira, R.C., Martins, C.C., Silva, C.R., França, E.J., Bícego, M.C., et al., 2011. Arsenic and trace metal contents in sediment profiles from the Admiralty Bay,
King George Island, Antarctica. Mar. Pollut. Bull. 62, 192–196. Roberts, S.J., Monien, P., Foster, L.C., Loftfield, J., Hocking, E.P., Schnetger, B., et al., 2017. Past penguin colony responses to explosive volcanism on the Antarctic Peninsula. Nat. Commun. 8. Rosado, D., Usero, J., Morillo, J., 2016. Ability of 3 extraction methods (BCR, Tessier and protease K) to estimate bioavailable metals in sediments from Huelva estuary (Southwestern Spain). Mar. Pollut. Bull. 102, 65–71. Santos, I.R., Silva-Filho, E.V., Schaefer, C.E., Albuquerque-Filho, M.R., Campos, L.S., 2005. Heavy metal contamination in coastal sediments and soils near the Brazilian Antarctic Station, King George Island. Mar. Pollut. Bull. 50, 185–194. Sheoran, A.S., Sheoran, V., 2006. Heavy metal removal mechanism of acid mine drainage in wetlands: a critical review. Miner. Eng. 19, 105–116. Shikazono, N., Tatewaki, K., Mohiuddin, K.M., Nakano, T., Zakir, H.M., 2012. Sources, spatial variation, and speciation of heavy metals in sediments of the Tamagawa River in Central Japan. Environ. Geochem. Health 34, 13–26. Shyleshchandran, M.N., Mohan, M., Ramasamy, E.V., 2018. Risk assessment of heavy metals in Vembanad Lake sediments (south-west coast of India), based on acid-volatile sulfide (AVS)-simultaneously extracted metal (SEM) approach. Environ. Sci. Pollut. Res. 25, 7333–7345. Sun, L., Xie, Z., 2001. Changes in lead concentration in Antarctic penguin droppings during the past 3,000 years. Environ. Geol. 40, 1205–1208. Sun, L., Xie, Z., Zhao, J., 2000. Palaeoecology: A 3,000-year record of penguin populations. Nature 407, 858. Sun, L., Emslie, S.D., Huang, T., Blais, J.M., Xie, Z., Liu, X., et al., 2013. Vertebrate records in polar sediments: Biological responses to past climate change and human activities. Earth-Science Rev 126, 147–155. Tessier, A., Campbell, P.G., Bisson, M., 1979. Sequential extraction procedure for the speciation of particulate trace metals. Anal. Chem. 51, 844–851. Xie, Z., Sun, L., 2008. A 1,800-year record of arsenic concentration in the penguin dropping sediment, Antarctic. Environ. Geol. 55, 1055–1059. Xie, Z., Sun, L., Wang, J., Liu, B., 2002. A potential source of atmospheric sulfur from penguin colony emissions. J. Geophys. Res.-Atoms. 107 (D22) (ACH 5–1-ACH 5–10). Yu, K., Tsai, L., Chen, S., Ho, S., 2001. Chemical binding of heavy metals in anoxic river sediments. Water Res. 35, 4086–4094. Zhang, W., Wang, Z., Wang, M., 2012. Analyses of the vertical and temporal distributions of sulfate-reducing bacteria in sediments of Lake Erhai, southwest China. Res. J. Chem. Environ. 16, 44–51.
8
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Restriction of sulfate reduction on the bioavailability and toxicity of trace metals in Antarctic lake sediments Yuanqing Chena, Jingwen Gea, Tao Huanga,b, , Lili Shena, Zhuding Chuc, Zhouqing Xiec ⁎
a
School of Resources and Environmental Engineering, Anhui University, Hefei 230601, China Anhui Province Key Laboratory of Wetland Ecosystem Protection and Restoration, Anhui University, Hefei 230601, China c Anhui Key Laboratory of Polar Environment and Global Change, School of Earth and Space Sciences, University of Science and Technology of China, Hefei 230026, Anhui, China b
ARTICLE INFO
ABSTRACT
Keywords: Trace metals Bioavailability Toxicity Ornithogenic sediments Sulfate reduction AVS
In this study, Acid-Volatile Sulfur (AVS), trace metals Cu, Cd and Zn and their chemical speciation based on BCRsequential and simultaneous extraction (SEMs) in Antarctic lake sediments (Y2-1 and YO) were analyzed to investigate the restriction of sulfate reduction on the bioavailability and toxicity of trace metals. Much higher trace metals in Y2-1 indicating a primary source from penguin guano. The main chemical speciation of Cu and Cd in Y2-1 was their oxidizable fraction in contrast to those of weak-acid extraction in YO. Lower ratio of ΣSEM/ AVS in Y2-1 indicating less toxicity of the trace metals. The main chemical speciation of Cd in Y2-1 was their oxidizable fraction in contrast to that exchangeable fraction in penguin guano, indicating that although amounts of Cd was transported from marine to lake by penguins, strong sulfate reduction in ornithogenic sediments restricts the bioavailability and toxicity of Cd through the formation of insoluble sulfide.
1. Introduction Trace metals in water body could be adsorbed physically by minerals in sediments, and be transformed to other chemical speciation induced by variable physicochemical conditions in a sediment-water interface (Sheoran and Sheoran, 2006; Park et al., 2016; Alberti et al., 2018). The Acid-Volatile Sulfur (AVS) in sediments was mainly from the dissimilatory reduction of sulfate, it plays a vital role in the distribution of many bivalent metal ions between sediments and the pore waters and thus restricts the bioavailability, toxicity and mobility of trace metals (Machado et al., 2004; Chai et al., 2017; Shyleshchandran et al., 2018). After the initial report of the strong influence from AVS on the toxicity of Cd in sediments (Di Toro et al., 1990), sulfide in sediments has been taken as one of the key indices for the evaluation of trace metals pollution in the aquatic environment. As an important indices on the evaluation of water pollution, the total quantity of trace metals, however, could not reflect their potential toxicity completely (Tessier et al., 1979; Akcay et al., 2003; Cao et al., 2015), because different chemical speciation of trace metals has different environmental behaviors and ecotoxicology (Brümmer, 1986; Massas et al., 2009; Shikazono et al., 2012). Chemical speciation of trace metals thus was used commonly to evaluate the metals ecotoxicology and their environmental safety (Giller et al., 1998; Nagajyoti et al., 2010). Therefore, it is a great
⁎
importance to study the relationship between sulfide and the various chemical speciation of trace metals to evaluate their bioavailability, toxicity and mobility comprehensively (Yu et al., 2001; Rosado et al., 2016; Shyleshchandran et al., 2018). High levels of organic and inorganic matters, such as trace metals, sulfur, phosphorus and persistent organic pollutants, were transported from the marine to land by seabirds and marine mammals in Polar Regions (Blais et al., 2005, 2007; Michelutti et al., 2008, 2010; Sun et al., 2013; Perfetti-Bolaño et al., 2018). These matters were then washed into lakes or ponds by runoff and formed the ornithogenic or excrement sediments (Sun et al., 2000, 2013; Emslie et al., 2014). Very high levels of trace metals (Brimble et al., 2009; Huang et al., 2011, 2014; Lou et al., 2015), as well as total sulfur and dimethylsulfide, have been measured in these ornithogenic sediments (Sun et al., 2000; Xie et al., 2002; Huang et al., 2009), and thus could have significant impacts on these lacustrine environment. Human activities near scientific stations in the Antarctic Fildes Peninsula and Ardley Island also induced trace metal pollutions in the lake system (Chu et al., 2019). Such of those studies focused mainly on the total quantity of trace metals transported by seabirds from the marine to lakes and ponds, rather than the bioavailability of trace metals and thus their potential biological toxicity. Here, we collected a lake ornithogenic sediment core Y2-1 from Y2 lake at Ardley Island, and a pristine lake sediment
Corresponding author at: School of Resources and Environmental Engineering, Anhui University, Hefei 230601, China. E-mail address: [email protected] (T. Huang).
https://doi.org/10.1016/j.marpolbul.2019.110807 Received 23 October 2019; Received in revised form 3 December 2019; Accepted 6 December 2019 Available online 09 December 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
Please cite this article as: Yuanqing Chen, et al., Marine Pollution Bulletin, https://doi.org/10.1016/j.marpolbul.2019.110807
Marine Pollution Bulletin xxx (xxxx) xxxx
Y. Chen, et al.
core YO from Yanou lake at Fildes Peninsula, Antarctic, to analyze the AVS and chemical speciation of trace metals Cu, Cd and Zn in these sediments, to compare and contrast the bioavailability and toxicity of trace metals in these two different lake systems. We aimed to show that strong sulfate reduction in penguin ornithogenic sediments restricts the bioavailability and toxicity of trace metals effectively through the formation of insoluble sulfides.
with electric heating. The digested subsamples were analyzed for Cu, Zn and Cd by using the inductively coupled plasma mass spectroscopy (ICP-MS). For the chemical speciation of trace metal analyses, a modified method of BCR-sequential extraction (Fathollahzadeh et al., 2014), was used to extract and analyze the speciation of trace metals using ICP-MS. The trace metal speciation from BCR-sequential extractions includes four fractions, weak-acid extraction (F1), the reducible fraction (F2), the oxidizable fraction (F3) and the residual fraction (F4). The AVS, total organic carbon (TOC), total nitrogen (TN) and total phosphorus (TP) in sediments were analyzed in our previous study (Chen et al., 2019). During the AVS analysis, one part of the extracts were analyzed for the content of simultaneously extracted metals (ΣSEM) by ICP-MS. Standard sediment reference materials (GSD-7a and GSD-12) were included with every batch of samples during the analyses of total trace metals. The analytical values for total trace metals are within ± 5% of the certified standards. Duplicate analysis on the extracts in Y2-1 sediments (4 cm, 15 cm, 34 cm and 52 cm) was performed to validate the BCR-sequential and simultaneous extraction procedure and for quality control of the analytical data, and the recovery rate was 80.4%–127.1%.
2. Materials and methods 2.1. Study area Fildes Peninsula (62°08′48″ – 62°14′02″S, 58°53′40″ – 59°01′50″W) locates in the southwest of King George Island, is the largest regional ice-free area with about 30 km2. It is a flat terrain with 10 km long and 2.5–4 km wide, and the highest altitude is about 70 m (Michel et al., 2014). Many scientific stations were established in this peninsula, and lots of scientists worked there every year, especially in the austral summer seasons. Ardley Island is connected to Fildes Peninsula with a sandbar. Although the local climate is cold, 80% of the island is covered with lichen and moss. Ardley Island was once a penguin island, and some lakes there were affected by penguin activities while most lakes in Fildes Peninsula were not.
3. Results 3.1. Total trace metals and the TP, TN and TOC
2.2. Sample collection and pretreatment
Vertical distribution of the TP, TN, TOC, Cu, Zn and Cd in Y2-1 and YO sediments was plotted in Fig. 2. In Y2-1 sediments, the content of TP, TN and TOC was 2.31% ± 1.99%, 0.51% ± 0.66% and 2.52% ± 2.63%, respectively, much higher than those in YO. Similarly, the total concentrations of Cu, Zn and Cd in Y2-1 were much higher than those in YO. TP, TN, TOC, Cu, Zn and Cd in Y2-1 showed a relatively consistent vertical trend, with high values in the depth of 15 cm and below the 45 cm, and lowest values between 40 cm and 45 cm (Fig. 2). While in YO sediments, TP, TN, TOC, Cu, Zn and Cd showed a different vertical trend.
During the 29th Chinese Antarctic Expedition in austral summer 2013, two sediment cores Y2-1 and YO were retrieved from Y2 lake at Ardley Island and Yanou Lake at Fildes Peninsula, respectively (Fig. 1). Y2-1 was an ornithogenic sediment core with a length of 60 cm; it was sectioned into 60 subsamples at a 1 cm interval. YO sediments were not affected by penguin guano, it was 30 cm long and sectioned into 30 subsamples at 1 cm intervals. In this study, 16 subsamples in Y2-1 and 11 in YO were selected for analysis. Before geochemical analyses, one part of subsample was stored in −20 °C, while the other part was freeze-dried and then powdered through a 200-mesh sieve.
3.2. SEMs, AVS and ΣSEM/AVS
2.3. Sample analyses
The simultaneous extraction of Cu, Zn and Cd, AVS and the ratio of ΣSEM/AVS in Y2-1 and YO sediments were plotted in Fig. 3. The concentrations of SEMCu, SEMZn, SEMCd and AVS in Y2-1 sediments
For trace metal analyses, 0.1 g of each powder subsamples were taken, weighed, and digested (HClO4-HNO3-HF) in a Teflon crucible
Fig. 1. Study area and sampling sites on Fildes Peninsula and Ardley Island. 2
Marine Pollution Bulletin xxx (xxxx) xxxx
Y. Chen, et al.
Fig. 2. Vertical distribution of Cu, Zn, Cd, TOC, TN and TP in Y2-1 and YO sediments.
were 3.86 ± 2.53 umol/g, 6.58 ± 2.99 umol/g, 0.024 ± 0.013 umol/g and 10.33 ± 13.09 umol/g, respectively, much higher than those in YO. SEMCu, SEMZn, SEMCd and AVS in Y2-1 sediments showed a consistent trend in vertical distributions; they reached higher values in 15 cm, lowest values in 40 cm–45 cm and the highest in the bottom sections. The concentrations of SEMCu, SEMZn, SEMCd and AVS in YO sediments were 0.44 ± 0.04 umol/g, 0.35 ± 0.04 umol/g, 0.0019 ± 0.0002 umol/g and 0.15 ± 0.16 umol/g, respectively. The AVS in YO sediments increased slightly at 15 cm and reached the highest value in the bottom 30 cm. SEMCu, SEMZn and SEMCd in YO sediments showed a different vertical distribution.
4. Discussion 4.1. Comparison of trace metals in different sediments in Antarctica The Y2-1 sediment was collected from Y2 Lake at Ardley Island, and a ground-breaking study identified the Cu, Zn, Sr, Ba, Ca, P, S, F and Se in this lake sediments as penguin bio-elements which originated mainly from penguin guanos (Sun et al., 2000). The total concentrations of trace metals Cu, Zn and Cd in Y2-1, YO and other Antarctic sediments, as well as fresh penguin guano, were list in Table 1. It showed that the total quantity of trace metals of Cu, Zn and Cd in Y2-1 ornithogenic sediments were similar to those in fresh penguin guano (Chu et al., 2019), and much higher than those in YO and other Antarctic sediments, indicate that all of them were mainly from penguin guano. A number of studies indicated an enrichment of trace metals Cu, Zn, Pb, As, Cd, Hg in Antarctic ornithogenic sediments (Sun and Xie, 2001; Ancora et al., 2002; Xie and Sun, 2008; Huang et al., 2011, 2014; Lou et al., 2015; Perfetti-Bolaño et al., 2018). The vertical distributions of the total Cu, Zn, Cd, TOC, TN and TP in Y2-1 sediments show a consistent trend with more fluctuant (Fig. 2), indicate that all of them were mainly from the penguin guano inputs, and higher levels indicate higher penguin populations in the lake area (Sun et al., 2000). The concentrations of Cu and Zn in YO sediments from a pristine Yanou lake were very low, similar to those of sediments from Ferraz Station and Admiralty Bay (Santos et al., 2005; Ribeiro et al., 2011), indicate that they came mainly from a natural deposition. Consequently, in YO sediments, only Cd and nutrients show a similar vertical trend (Fig. 2),
3.3. Chemical speciation of Cu, Zn and Cd The chemical speciation of Cu, Zn and Cd in Y2-1 and YO sediments were plotted in Fig. 4. The primary chemical speciation of Cu in Y2-1 sediments was the oxidizable fraction (53.43%), in contrast to that of the weak-acid extraction (43.79%) in YO. While the primary chemical speciation of Zn in Y2-1 sediments was the weak-acid extraction (35.70%) and a residual fraction (29.81%), in contrast to that of the oxidizable fraction (37.66%) in YO. The concentration of Cd in Y2-1 sediments was as high as 4.54 ± 2.99 μg/g, with the primary speciation of the oxidizable fraction (41.76%) in contrast to that of the residual fraction (47.54%) as well as the weak-acid extraction (35.91%) in YO.
3
Marine Pollution Bulletin xxx (xxxx) xxxx
Y. Chen, et al.
Fig. 3. Vertical distribution of SEMs, AVS and ratio of ΣSEM/AVS in Y2-1 and YO sediments.
with the lowest and highest values in the depths of 12 cm and 19 cm, respectively. The abnormal distribution of trace metals and nutrients in Yanou Lake may be associated with several influences such as climate change, tephra deposition and transition of sediment environment which have been reported previously (Fretwell et al., 2010; Roberts et al., 2017).
metal ions in pore water of the sediments and form insoluble sulfides (Machado et al., 2004; Chai et al., 2017; Shyleshchandran et al., 2018). The sulfate reduction in sediments was determined by the abundance of Sulfate-Reducing Bacteria (SRB) (Brüchert et al., 2001; Foti et al., 2007; Couture et al., 2016; Li et al., 2018). Some studies showed that the abundance of SRB in sediments reached a peak value at a depth of 10 cm–50 cm in sediments (D'Hondt et al., 2004; Leloup et al., 2009; Zhang et al., 2012), which was consistent with the depth of peak levels of AVS in Y2-1 and YO sediments. The ratio of ΣSEM/AVS in sediments has been used widely to evaluate the biological toxicity of trace metals (Besser et al., 2008; Chai et al., 2015; Shyleshchandran et al., 2018), and the trace metals would present biological toxicity if the ratio > 1.0, and vice versa. Generally, the mean ratio of ΣSEM/AVS in Y2-1 sediments was lower than that in YO (7.01 vs 36.66) (Fig. 2), suggests that the biological toxicity of trace metals in Y2-1 sediments was less than that in YO. The trace metals in Y2-1 sediments present no toxicity in the depths of 8 cm, 12 cm, 48 cm and 56 cm with the ratios between 0.40 and 0.80, and weak toxicity in the depths of 15 cm, 19 cm and 52 cm with the ratios range from 1.08 to 1.48. While the trace metals in YO sediments present high toxicity in the depths of 3 cm, 5 cm, 8 cm and 12 cm with a mean ratio of 91.01, and weak toxicity in the depths of 26 cm, 28 cm and 30 cm with the ratios range from 1.70 to 3.77. The trace metals in Y2-1 sediments were much higher than those in YO, while the biological toxicity of them in Y2-1 sediments was less than that in YO, indicating that although the penguins transported high levels of trace metals and caused pollution to the lake system, the S2− reduced from sulfate that promoted by the
4.2. Restriction of AVS on the bioavailability and toxicity of trace metals The consistent vertical trends of AVS and SEMs in Y2-1 sediments suggest that the S2− from sulfate reduction could combine with ions of Cu2+, Zn2+ and Cd2+ effectively, and thus plays an important role in restricting the bioavailability and toxicity of trace metals. Pearson correlation analysis between AVS and SEMs in YO sediments, however, showed the insignificant relationship (Table 2), indicate that trace metals of Cu, Zn and Cd in Yanou lake were not affected by S2− in contrast to those in Y2-1. The significant positive relationship among SEMZn, SEMCd and ΣSEM in YO sediments (Table 2) suggests that Zn and Cd were the main components of ΣSEM in YO sediments in this study. The ratio of ΣSEM/AVS in sediments was associated closely with the biological toxicity of trace metals, and higher ratios correspond to higher toxicity. It was suggested that there was negligible toxicity when the bivalent metal ions were less than S2− in sediments (Di Toro et al., 1992; Prica et al., 2008; Pignotti et al., 2018). The toxicity of trace metals in sediments was influenced significantly by sulfate reduction, because the S2− from sulfate reduction can combine with the divalent 4
Marine Pollution Bulletin xxx (xxxx) xxxx
Y. Chen, et al.
Fig. 4. Chemical speciation of Cu, Zn and Cd in Y2-1 and YO sediments.
high levels of organic matter (Chen et al., 2019), could restrict the biological toxicity of trace metals.
4.3. Chemical speciation of Cu, Zn and Cd and their mobility The chemical speciation of Cu, Zn and Cd in Y2-1 and YO were plotted in Fig. 4. Trace metals pollution in sediments cannot be
Table 1 Concentrations of Cu, Zn and Cd (ug/g) in the Antarctic sediments and penguin guano. Sampling Site
Materials
Cu
Zn
Cd
Reference
Y2-1 YO Ardley Island Fildes Peninsula Admiralty Bay Ferraz Station Ardley Island
Lake core sediments Lake core sediments Lake surface sediments Lake surface sediments Lake sediments Coastal sediments Penguin guanos
56–779 32–49 166–526 52–144 47–84 44 926
116–881 44–63 121–492 49–68 44–89 52 573
0.65–9.99 0.19–0.27 1.0–4.6 0.5–1.4 0.4–0.9 ND 2.0
This study This study Chu et al., 2019 Chu et al., 2019 Ribeiro et al., 2011 Santos et al., 2005 Chu et al., 2019
ND means not determined. 5
Marine Pollution Bulletin xxx (xxxx) xxxx
Y. Chen, et al.
in Y2-1 sediments (Figs. 3, 4). This consistency, however, was not observed in YO. The oxidizable fraction of trace metals includes two parts, one is the fraction that bound to organic matters, and the other is the form of sulfides (AVS). The Pearson correlation analysis showed a significant positive relationship between AVS and the oxidizable fraction of Cu and Cd in Y2-1 sediments (Table 3), indicating that the sulfide was the primary form of the oxidizable fraction, and S2− from sulfate reduction in Y2-1 could combine ions of Cu and Cd effectively and form AVS. The oxidizable fraction was the main chemical speciation of Cu and Cd in Y2-1 sediments, while that of Zn occupied only a proportion of 19.20% in the total quantity (Fig. 4). This may be due to the different vulcanization of trace metals. For example, trace metals of Ni and Cd could be vulcanized mostly (100% and 81%) by S2−, while the Zn could be vulcanized just by 11%–16% (Huerta-Diaz et al., 1998; Charriau et al., 2011). A previous study on the penguin ornithogenic sediments from the Antarctic Ross sea area showed that the exchangeable fraction was the main chemical speciation of Cd (52.8%) in fresh penguin guano, while that exchangeable fraction of Cd decreased significantly in sediments and it was attributed to the complexation by high levels of organic matter (Lou et al., 2015). In the present study, the weak-acid extraction of Cd (include the fraction of exchangeable and carbonate bounded) occupied only 14.82% of the total Cd in Y2-1 sediments, while the oxidizable fraction occupied 41.76% (Fig. 4). The proportion of weakacid extraction of Cd correlated significantly with AVS in the layer of 8 cm–23 cm in Y2-1 (r = −0.99, p = .001) (Fig. 5), indicating once again that higher S2− reduce the mobility of Cd. In contrast to the sediments collected from ornithogenic soil pit in the McMurdo Dry Valleys in Lou et al. (2015), Y2-1 sediments in the present study were
Table 2 Correlation analysis for the SEMs and AVS in YO sediments.
AVS SEMCu SEMZn SEMCd ΣSEM ⁎⁎
AVS
SEMCu
SEMZn
SEMCd
ΣSEM
1.00
0.22 1.00
−0.15 0.15 1.00
−0.20 0.36 0.93⁎⁎ 1.00
−0.03 0.56 0.91⁎⁎ 0.93⁎⁎ 1.00
Correlation is significant at 0.01 level (2-tailed).
Table 3 Correlation analysis for the AVS and the oxidizable fraction of trace metals (F3) in Y2-1 sediments.
AVS Cu (F3) Zn (F3) Cd (F3) ⁎ ⁎⁎
AVS
Cu (F3)
Zn (F3)
Cd (F3)
1.00
0.78 1.00
0.16 0.09 1.00
0.70⁎⁎ 0.81⁎⁎ 0.60⁎ 1.00
⁎⁎
Correlation is significant at 0.05 level (2-tailed). Correlation is significant at 0.01 level (2-tailed).
reflected completely by its total concentrations (Cuong and Obbard, 2006; Shikazono et al., 2012), because it was associated mainly with the trace metal's mobility and biological toxicity which were determined by their chemical speciation (Fuentes et al., 2004; De la Fuente et al., 2008; Jia et al., 2018). The vertical distribution trend of AVS was consistent with that of the oxidizable fraction of Cu, Zn and Cd
Fig. 5. Correlation between the weak-acid extraction of trace metals and TOC and AVS in Y2-1 sediments (8 cm–23 cm). 6
Marine Pollution Bulletin xxx (xxxx) xxxx
Y. Chen, et al.
collected from Y2 Lake with a stronger anaerobic condition. Our previous study indicated a strong sulfate reduction in the Y2-1 sediments (Chen et al., 2019). Thus, it was indicated that the low weak-acid extraction of Cd in Y2-1 ornithogenic sediments was primarily due to the formation of insoluble sulfides by S2− that reduced from strong sulfate reduction, rather than the complexation by high organic matters. Finally, both of the ratio of ΣSEM/AVS and the chemical speciation of Cd in Y2-1 indicate that though the penguin populations transported high levels of trace metals to the Y2 lake system, the S2− reduced from sulfate reduction that promoted by the high organic matters can restrict the bioavailability, toxicity and mobility of Cd and Cu effectively, through the formation of insoluble sulfides.
Besser, J.M., Brumbaugh, W.G., Ivey, C.D., Ingersoll, C.G., Moran, P.W., 2008. Biological and chemical characterization of metal bioavailability in sediments from Lake Roosevelt, Columbia River, Washington, USA. Arch. Environ. Contam. Toxicol. 54, 557–570. Blais, J.M., Kimpe, L.E., McMahon, D., Keatley, B.E., Mallory, M.L., Douglas, M.S., et al., 2005. Ecology: Arctic seabirds transport marine-derived contaminants. Science 309, 445. Blais, J.M., Macdonald, R.W., Mackay, D., Webster, E., Harvey, C., Smol, J.P., 2007. Biologically mediated transport of contaminants to aquatic systems. Environ. Sci. Technol. 41, 1075–1084. Brimble, S.K., Foster, K.L., Mallory, M.L., Macdonald, R.W., Smol, J.P., Biais, J.M., 2009. High arctic ponds receiving biotransported nutrients from a nearby seabird colony are also subject to potentially toxic loadings of arsenic, cadmium, and zinc. Environ. Toxicol. Chem. 28, 2426–2433. Brüchert, V., Knoblauch, C., Jorgensen, B.B., 2001. Controls on stable sulfur isotope fractionation during bacterial sulfate reduction in arctic sediments. Geochim. Cosmochim. Acta 65, 763–776. Brümmer, G.W., 1986. Heavy Metal Species, Mobility and Availability in Soils. Springer. Cao, L., Tian, H., Yang, J., Shi, P., Lou, Q., Waxi, L., et al., 2015. Multivariate analyses and evaluation of heavy metals by chemometric BCR sequential extraction method in surface sediments from Lingdingyang Bay, South China. Sustainability 7, 4938–4951. Chai, M., Shen, X., Li, R., Qiu, G., 2015. The risk assessment of heavy metals in Futian mangrove forest sediment in Shenzhen Bay (South China) based on SEM-AVS analysis. Mar. Pollut. Bull. 97, 431–439. Chai, M., Li, R., Zan, Q., 2017. Effects of mangrove plants on heavy metal risk in sediment based on SEM-AVS analysis. Reg. Stud. Mar. Sci. 13, 12–18. Charriau, A., Lesven, L., Gao, Y., Leermakers, M., Baeyens, W., Ouddane, B., et al., 2011. Trace metal behaviour in riverine sediments: role of organic matter and sulfides. Appl. Geochem. 26, 80–90. Chen, Y., Shen, L., Huang, T., Chu, Z., Xie, Z., 2019. Transformation of sulfur species in lake sediments at Ardley Island and Fildes Peninsula, King George Island, Antarctic Peninsula. Sci. Total Environ. https://doi.org/10.1016/j.scitotenv.2019.135591. Chu, Z., Yang, Z., Wang, Y., Sun, L., Yang, W., Yang, L., et al., 2019. Assessment of heavy metal contamination from penguins and anthropogenic activities on Fildes Peninsula and Ardley Island, Antarctic. Sci. Total Environ. 646, 951–957. Couture, R.M., Fischer, R., Van Cappellen, P., Gobeil, C., 2016. Non-steady state diagenesis of organic and inorganic sulfur in lake sediments. Geochim. Cosmochim. Acta 194, 15–33. Cuong, D.T., Obbard, J.P., 2006. Metal speciation in coastal marine sediments from Singapore using a modified BCR-sequential extraction procedure. Appl. Geochem. 21, 1335–1346. De la Fuente, C., Clemente, R., Bernal, M.P., 2008. Changes in metal speciation and pH in olive processing waste and sulphur-treated contaminated soil. Ecotoxicol. Environ. Saf. 70, 207–215. D'Hondt, S., Jørgensen, B.B., Miller, D.J., Batzke, A., Blake, R., Cragg, B.A., et al., 2004. Distributions of microbial activities in deep subseafloor sediments. Science 306, 2216–2221. Di Toro, D.M., Mahony, J.D., Hansen, D.J., Scott, K.J., Hicks, M.B., Mayr, S.M., et al., 1990. Toxicity of cadmium in sediments: the role of acid volatile sulfide. Environ. Toxicol. Chem. 9, 1487–1502. Di Toro, D.M., Mahony, J.D., Hansen, D.J., John Scott, K., Carlson, A.R., Ankley, G.T., 1992. Acid volatile sulfide predicts the acute toxicity of cadmium and nickel in sediments. Environ. Sci. Technol. 26, 96–101. Emslie, S.D., Polito, M.J., Brasso, R., Patterson, W.P., Sun, L., 2014. Ornithogenic soils and the paleoecology of pygoscelid penguins in Antarctica. Quatern. Int. 352, 4–15. Fathollahzadeh, H., Kaczala, F., Bhatnagar, A., Hogland, W., 2014. Speciation of metals in contaminated sediments from Oskarshamn Harbor, Oskarshamn, Sweden. Environ. Sci. Pollut. Res. 21, 2455–2464. Foti, M., Sorokin, D.Y., Lomans, B., Mussman, M., Zacharova, E.E., Pimenov, N.V., et al., 2007. Diversity, activity, and abundance of sulfate-reducing bacteria in saline and hypersaline soda lakes. Appl. Environ. Microb. 73, 2093–2100. Fretwell, P.T., Hodgson, D.A., Watcham, E.P., Bentley, M.J., Roberts, S.J., 2010. Holocene isostatic uplift of the South Shetland Islands, Antarctic Peninsula, modelled from raised beaches. Quat. Sci. Rev. 29, 1880–1893. Fuentes, A., Lloréns, M., Sáez, J., Aguilar, M.I., Ortuño, J.F., Meseguer, V.F., 2004. Phytotoxicity and heavy metals speciation of stabilised sewage sludges. J. Hazard. Mater. 108, 161–169. Giller, K.E., Witter, E., Mcgrath, S.P., 1998. Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol. Biochem. 30, 1389–1414. Huang, T., Sun, L., Wang, Y., Liu, X., Zhu, R., 2009. Penguin population dynamics for the past 8500 years at Gardner Island, Vestfold Hills. Antarct. Sci. 21, 571–578. Huang, T., Sun, L., Wang, Y., Kong, D., 2011. Late Holocene Adélie penguin population dynamics at Zolotov Island, Vestfold Hills, Antarctica. J. Paleolimnol. 45, 273–285. Huang, T., Sun, L., Wang, Y., Chu, Z., Qin, X., Yang, L., 2014. Transport of nutrients and contaminants from ocean to island by emperor penguins from Amanda Bay, East Antarctic. Sci. Total Environ. 468, 578–583. Huerta-Diaz, M.A., Tessier, A., Carignan, R., 1998. Geochemistry of trace metals associated with reduced sulfur in freshwater sediments. Appl. Geochem. 13, 213–233. Jia, Y., Chen, W., Zuo, Y., Lin, L., Song, L., 2018. Heavy metal migration and risk transference associated with cyanobacterial blooms in eutrophic freshwater. Sci. Total Environ. 613, 1324–1330. Leloup, J., Fossing, H., Kohls, K., Holmkvist, L., Borowski, C., Jørgensen, B.B., 2009. Sulfate-reducing bacteria in marine sediment (Aarhus Bay, Denmark): abundance and diversity related to geochemical zonation. Environ. Microbiol. 11, 1278–1291. Li, X., Lan, S., Zhu, Z., Zhang, C., Zeng, G., Liu, Y., et al., 2018. The bioenergetics
5. Conclusions We analyzed the AVS, total Cu, Cd and Zn and their chemical speciation in the Antarctic penguin ornithogenic sediments Y2-1 and pristine lake sediments YO to investigate the restriction of sulfate reduction on the bioavailability and toxicity of these trace metals. Much higher levels of Cu, Cd and Zn in Y2-1 sediments were observed in contrast to those in YO. The toxicity of Cu, Cd and Zn in Y2-1 sediments was less than that in YO, indicated by a lower ratio of ΣSEM/AVS in Y21. The main chemical speciation of Cd was its oxidizable fraction in Y21 ornithogenic sediments, in contrast to the exchangeable fraction in the fresh guano. We concluded that although a large of poisonous Cd was transported from the marine to freshwater environment by penguin populations, the S2− reduced from sulfate that promoted by the transported high organic matters, could restrict the bioavailability and toxicity of Cd effectively through the formation of insoluble cadmium sulfide. Since the penguins and thus the ornithogenic sediments and soils distribute widely in the coastal Antarctic, our study would be help on the accurate evaluation of trace metals pollution from the marine to the lacustrine environment by penguin's activity, in the perspective of bioavailability, toxicity and mobility. Author contribution statement Tao Huang: Conceptualization, Methodology, Resources, WritingReviewing and Editing, Funding acquisition, Supervision. Yuanqing Chen: Data curation, Writing- Original draft preparation. Jingwen Ge: Data curation, Investigation. Lili Shen: Data curation, Investigation. Zhuding Chu: Investigation. Zhouqing Xie: Investigation. Declaration of competing interest The authors declare no conflict of interests. Acknowledgements This work was supported by the National Natural Science Foundation of China (No. 41476165) and the Science Research Project of Anhui Department of Education (No. KJ2019A0042). Samples in this study were provided by the BIRDS-Sediment system (Hefei). We thank the Chinese Arctic and Antarctic Administration and Polar Research Institute of China for logistical support in field work. References Akcay, H., Oguz, A., Karapire, C., 2003. Study of heavy metal pollution and speciation in Buyak Menderes and Gediz river sediments. Water Res. 37, 813–822. Alberti, G., Mussi, M., Quattrini, F., Pesavento, M., Biesuz, R., 2018. Metal complexation capacity of Antarctic lacustrine sediments. Chemosphere 196, 402–408. Ancora, S., Volpi, V., Olmastroni, S., Focardi, S., Leonzio, C., 2002. Assumption and elimination of trace elements in Adelie penguins from Antarctica: a preliminary study. Mar. Environ. Res. 54, 341–344.
7
Marine Pollution Bulletin xxx (xxxx) xxxx
Y. Chen, et al. mechanisms and applications of sulfate-reducing bacteria in remediation of pollutants in drainage: a review. Ecotoxicol. Environ. Saf. 158, 162–170. Lou, C., Liu, X., Nie, Y., Emslie, S.D., 2015. Fractionation distribution and preliminary ecological risk assessment of As, Hg and Cd in ornithogenic sediments from the Ross Sea region, East Antarctica. Sci. Total Environ. 538, 644–653. Machado, W., Carvalho, M.F., Santelli, R.E., Maddock, J.E.L., 2004. Reactive sulfides relationship with metals in sediments from an eutrophicated estuary in Southeast Brazil. Mar. Pollut. Bull. 49, 89–92. Massas, I., Ehaliotis, C., Gerontidis, S., Sarris, E., 2009. Elevated heavy metal concentrations in top soils of an Aegean island town (Greece): Total and available forms, origin and distribution. Environ. Monit. Assess. 151, 105–116. Michel, R.F., Schaefer, C.E., López-Martínez, J., Simas, F.N., Haus, N.W., Serrano, E., et al., 2014. Soils and landforms from Fildes Peninsula and Ardley Island, maritime Antarctica. Geomorphology 225, 76–86. Michelutti, N., Keatley, B.E., Brimble, S., Blais, J.M., Liu, H., Douglas, M.S., et al., 2008. Seabird-driven shifts in Arctic pond ecosystems. P. Roy. Soc. B-Biol. Sci. 276, 591–596. Michelutti, N., Blais, J.M., Mallory, M.L., Brash, J., Thienpont, J., Kimpe, L.E., et al., 2010. Trophic position influences the efficacy of seabirds as metal biovectors. P. Natl. Acad. Sci. USA. 107, 10543–10548. Nagajyoti, P.C., Lee, K.D., Sreekanth, T.V., 2010. Heavy metals, occurrence and toxicity for plants: a review. Environ. Chem. Lett. 8, 199–216. Park, J.H., Ok, Y.S., Kim, S.H., Cho, J.S., Heo, J.S., Delaune, R.D., et al., 2016. Competitive adsorption of heavy metals onto sesame straw biochar in aqueous solutions. Chemosphere 142, 77–83. Perfetti-Bolaño, A., Moreno, L., Urrutia, R., Araneda, A., Barra, R., 2018. Influence of Pygoscelis penguin colonies on cu and Pb concentrations in soils on the Ardley peninsula, maritime Antarctica. Water Air Soil Pollut. 229, 390. Pignotti, E., Guerra, R., Covelli, S., Fabbri, E., Dinelli, E., 2018. Sediment quality assessment in a coastal lagoon (Ravenna, NE Italy) based on SEM-AVS and sequential extraction procedure. Sci. Total Environ. 635, 216–227. Prica, M., Dalmacija, B., Rončević, S., Krčmar, D., Bečelić, M., 2008. A comparison of sediment quality results with acid volatile sulfide (AVS) and simultaneously extracted metals (SEM) ratio in Vojvodina (Serbia) sediments. Sci. Total Environ. 389, 235–244. Ribeiro, A.P., Figueira, R.C., Martins, C.C., Silva, C.R., França, E.J., Bícego, M.C., et al., 2011. Arsenic and trace metal contents in sediment profiles from the Admiralty Bay,
King George Island, Antarctica. Mar. Pollut. Bull. 62, 192–196. Roberts, S.J., Monien, P., Foster, L.C., Loftfield, J., Hocking, E.P., Schnetger, B., et al., 2017. Past penguin colony responses to explosive volcanism on the Antarctic Peninsula. Nat. Commun. 8. Rosado, D., Usero, J., Morillo, J., 2016. Ability of 3 extraction methods (BCR, Tessier and protease K) to estimate bioavailable metals in sediments from Huelva estuary (Southwestern Spain). Mar. Pollut. Bull. 102, 65–71. Santos, I.R., Silva-Filho, E.V., Schaefer, C.E., Albuquerque-Filho, M.R., Campos, L.S., 2005. Heavy metal contamination in coastal sediments and soils near the Brazilian Antarctic Station, King George Island. Mar. Pollut. Bull. 50, 185–194. Sheoran, A.S., Sheoran, V., 2006. Heavy metal removal mechanism of acid mine drainage in wetlands: a critical review. Miner. Eng. 19, 105–116. Shikazono, N., Tatewaki, K., Mohiuddin, K.M., Nakano, T., Zakir, H.M., 2012. Sources, spatial variation, and speciation of heavy metals in sediments of the Tamagawa River in Central Japan. Environ. Geochem. Health 34, 13–26. Shyleshchandran, M.N., Mohan, M., Ramasamy, E.V., 2018. Risk assessment of heavy metals in Vembanad Lake sediments (south-west coast of India), based on acid-volatile sulfide (AVS)-simultaneously extracted metal (SEM) approach. Environ. Sci. Pollut. Res. 25, 7333–7345. Sun, L., Xie, Z., 2001. Changes in lead concentration in Antarctic penguin droppings during the past 3,000 years. Environ. Geol. 40, 1205–1208. Sun, L., Xie, Z., Zhao, J., 2000. Palaeoecology: A 3,000-year record of penguin populations. Nature 407, 858. Sun, L., Emslie, S.D., Huang, T., Blais, J.M., Xie, Z., Liu, X., et al., 2013. Vertebrate records in polar sediments: Biological responses to past climate change and human activities. Earth-Science Rev 126, 147–155. Tessier, A., Campbell, P.G., Bisson, M., 1979. Sequential extraction procedure for the speciation of particulate trace metals. Anal. Chem. 51, 844–851. Xie, Z., Sun, L., 2008. A 1,800-year record of arsenic concentration in the penguin dropping sediment, Antarctic. Environ. Geol. 55, 1055–1059. Xie, Z., Sun, L., Wang, J., Liu, B., 2002. A potential source of atmospheric sulfur from penguin colony emissions. J. Geophys. Res.-Atoms. 107 (D22) (ACH 5–1-ACH 5–10). Yu, K., Tsai, L., Chen, S., Ho, S., 2001. Chemical binding of heavy metals in anoxic river sediments. Water Res. 35, 4086–4094. Zhang, W., Wang, Z., Wang, M., 2012. Analyses of the vertical and temporal distributions of sulfate-reducing bacteria in sediments of Lake Erhai, southwest China. Res. J. Chem. Environ. 16, 44–51.
8