Chemosphere 184 (2017) 235e243 Contents lists available at ScienceDirect Chemosphere journal homepage: www.elsevier.com/locate/chemosphere Investigation of heavy metals release from sediment with bioturbation/bioirrigation * ** Yi He, Bin Men , Xiaofang Yang, Yaxuan Li, Hui Xu, Dongsheng Wang State Key Laboratory of Environmental Aquatic Chemistry, Research Centre for Eco-Environmental Science, Chinese Academy of Sciences, Beijing 100085, China highlights graphical abstract DGT-Cu fluxes in pore water Adsorption increased with the presence of Water Complexation Fe/Mn oxidates chironomid larvae. Dissolved Me+ fl Tubificid Heavy metals were highly in uenced Chironomid larvae Particulate Me+ by bioturbation/bioirrigation of Loach O2 loach. Settling fi + Organisms has signi cant impact on Bioavailable Me + Biofilms Me -AVS Adsorption particulate heavy metals release from Me+-Carbonates Sediment particles Me+-OM sediment. Me+ Fe/Mn hydrous oxides may sorb or Sediment Pore water coprecipitate with Cd, Cu, Zn and Pb. article info abstract Article history: Bioturbation/bioirrigation can affect the remobilization of metals from sediments. In this study, exper- Received 19 January 2017 iments were performed to examine the effect of bioturbation/bioirrigation by different organisms on Received in revised form cadmium (Cd), copper (Cu), zinc (Zn) and lead (Pb) releasing from the spiked sediment. The diffusive 16 May 2017 gradient in thin films technique (DGT) revealed that at the end of exposure time, the labile heavy metals Accepted 21 May 2017 concentrations in the pore water for all metal and organisms combinations except Cu and chironomid Available online 2 June 2017 larvae were much lower than that in the control group. However, the concentrations of heavy metals Handling Editor: Martine Leermakers detected by the DGT were virtually indistinguishable among the treatments with tubificid, chironomid larvae and loach. The correlation analysis of heavy metals with iron (Fe) and manganese (Mn) suggested Keywords: that Cd, Zn and Pb were most likely bound as Fe-Mn oxidation form in the pore water, but Cu was in Heavy metals other forms. After 28 d of exposure, bioturbation/bioirrigation produced a significant release of partic- DGT ulate heavy metals into the overlying water, especially in the treatment with loach. The bioturbation/ Bioturbation/bioirrigation bioirrigation impact on the Pb remobilization was less than the other three heavy metals. The effects of Bioaccumulation bioturbaiton/bioirrigation on the heavy metals remobilization in the sediment were complex that with studying the heavy metals remobilization in the sediment and water interface, the biological indicators should be recommended. © 2017 Elsevier Ltd. All rights reserved. 1. Introduction The sediment which buried heavy metals may act as a source of contaminants with certain disturbances such as bioturbation/bio- * Corresponding author. irrigation by benthic organisms (Banta and Andersen, 2003; ** Corresponding author. Thibodeaux and Bierman, 2003; Granberg et al., 2008; Josefsson E-mail addresses: [email protected] (B. Men), [email protected] (D. Wang). http://dx.doi.org/10.1016/j.chemosphere.2017.05.177 0045-6535/© 2017 Elsevier Ltd. All rights reserved. 236 Y. He et al. / Chemosphere 184 (2017) 235e243 et al., 2010). Several studies have demonstrated that bioturbation/ formation of Fe hydroxide precipitates and result of lower Zn fluxes bioirrigation can increase the transfer of heavy metals between in pore water (Simpson and Batley, 2003). So it must pay attention sediment and water. Tubificid renewed the particles and adsorption to the concentrations of heavy metals in the pore water when study sites for Cd at the interface of sediment and water, and also about the bioturbation/bioirrigation effects on the heavy metals increased the Cd contents in the sediment layer (Ciutat et al., 2005). remobilization in the sediment. The diffusive gradient in thin films Hexagenia rigida nymphs lived in the contaminated sediment can (DGT) method can determine the average concentration in the also produce resuspention of large amounts of sediment particles interface of the sediment and solution within the placed time. With rich in Cd and Zn into the water column (Ciutat and Boudou, 2003). laboratory microcosm experiments, DGT may be a good method to There was strong Cd, Cu, and Zn mobilization by bioturbation/ investigate the bioturbation/bioirrigation effects on the changes of bioirrigation of the Chironomus plumosus as their activities of dig- pore water heavy metal concentrations (Roulier et al., 2008; ging into the sediments, and afterwards strong decrease of the Simpson et al., 2012), and also it was a useful tool to assess the three heavy metals concentrations, but to higher levels compared heavy metal bioavailability to benthic organisms in sediment to values of treatments without invertebrate impact (Schaller, (Amato et al., 2016). However, little work has been performed on 2014). The polychaete Marenzelleria spp (Hedman et al., 2008) the bioturbation/bioirrigation effect on the metal remobilization in and carp (Wall et al., 1996) caused the high remobilization of Cd the sediment pore water. from sediment to the overlying water with the bioturbation/bio- Three organisms were chosen for this study, including tubificid irrigation activities. The oligochaete worm Lumbriculus variegates (Limnodrilus hoffmeisteri), chironomid larvae (Chironomus plumosus can enhance Pb transfer across the interface of sediment and water larvae), and loach (Misgurnus bipartitus), hereafter referred to as and also enhance the availability of Pb (Blankson and Klerks, 2016). tubificid, chironomid larvae, and loach, respectively. Consequently, But some researchers found that bioturbation/bioirrigation may the present study aimed at the degree of bioturbation/bioirrigation have little effect on the remobilization of heavy metals in the effect on the heavy metals transfer processes by different types of sediment. The presence of bivalve Tellina deltoidalis had little effect riverine organisms. The heavy metals accumulated in the three on the release of Zn and Pb from the sediment (Atkinson et al., organisms lived in the heavy metals spiked sediment was also 2007). The tubificid also provided little impact for the Pb remobi- investigated. lization from the sediment (Lv, 2009). The Hediste diversicolor did not influence the remobilization of dissolved mercury (Hg) from 2. Materials and methods the sediment to the water since the sediment was rich in organic matter content, Fe/Mn total and hydrous oxides to retain the Hg in 2.1. Sediment and water collection and preparation the sediment (Cardoso et al., 2008). And the bioturbation by Monoporeia affinis was also not sufficient to the release of Cu from The sediment and water were sampled from the Ming Tombs the sediment enriched Cu (Ospina Alvarez et al., 2014). The Reservoir in the northwest of Beijing (China) in May 2013. The different conclusions of the researches suggested that the influence collected water were pre-aerated for 24 h and filtered through of bioturbation/bioirrigation on the heavy metals fluxes in the 0.45 mm cellulose acetate membrane filter. The percentage of the sediment was very complex. particle size below 60 mm of the sediment was 85.7%. The pH value The bioturbation/bioirrigation effects on the heavy metals of the sediment was 7.6. The sediment was rich in organic matter remobilization in the sediment were different with the different that the loss by ignition was 7.9% (He et al., 2015). Wet sediment types of bioturbated organisms. The concentrations of dissolved Cu was added to plastic mixing containers and then spiked with decreased and Mn increased with the presence of amphipod Vic- analytical reagent grade of Cd(NO3)2$4H2O, ZnSO4$7H2O, Pb(NO3)2 toriopisa australiensis compared with the presence only of bivalve and CuSO4$5H2O successively. During the first 2 months, the test Tellina deltoidalis for the different bioturbating intensity (Remaili sediment was stirred twice a week at room temperature in order to et al., 2016). And the high bioturbation by Victoriopisa austral- make it homogenized. The final Cd, Cu, Zn and Pb concentration of iensis also produced significant release of DGT-labile Cd, Ni, Pb and sediment after spiking in each experiment unit was À À À Zn compared with the low bioturbation by Tellina deltoidalis in the 11.3 ± 1.4 mg kg 1, 881.1 ± 68.9 mg kg 1, 1132.8 ± 86.3 mg kg 1, and À pore and overlying water (Amato et al., 2016). The bioturbation 875.8 ± 70.4 mg kg 1 (dry mass, n ¼ 16), respectively. tests with the burrowing Hexagenia sp. had consistently higher overlying water Ni concentrations compared with the amphipod 2.2. Experimental design and setup (Hyalella azteca and Gammarus pseudolimnaeus) tests (Brumbaugh et al., 2013). Comparing the bioturbation by Tubifex tubifex and The experiments of the bioturbation/bioirrigation effects on the Chironomus riparius larvae on the release of uranium (U), the bio- heavy metals releasing from the spiked sediment were conducted tubation by T. tubifex led to a high degree of U release from sedi- the same as previous study (He et al., 2015). The experiments were ment into the overlying water for its effects on sediment reworking conducted for 29 d in glass beakers with diameter of 13 cm and (Lagauzere et al., 2009). Until now, rare research exists evaluating height of 19 cm which were lined with high density polyethylene the effect of the bioturbation/bioirrigation on heavy metals remo- film. 600 mL water and about 2.0 kg contaminated sediment were bilization by different organism types, which can have great in- added into each beaker. Four series of treatments with four repli- fluence on the fate of heavy metals. cates were conducted. The first treatment was a control group In fact, the toxicity and fate of metals in the sediments was without organism adding, the other three series of treatments obviously correlated with the partitioning of metals between the contained 2.0 g of different organism, respectively. The number of À sediment particles and the pore water (Calmano et al., 1993; tubificid, chironomid larvae and loach as 7.5 Â 105 m 2, À À Chapman et al., 1998; Simpson, 2005).