Relationship Between Heavy Metals and Dissolved Organic Matter Released from Sediment by Bioturbation/Bioirrigation

JOURNAL OF ENVIRONMENTAL SCIENCES 75 (2019) 216– 223

Available online at www.sciencedirect.com ScienceDirect

www.elsevier.com/locate/jes

Relationship between heavy metals and dissolved organic matter released from sediment by 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

ARTICLE INFO ABSTRACT

Article history: Organic matter (OM) is an important component of sediment. Bioturbation/bioirrigation can Received 4 December 2017 remobilize OM and heavy metals that were previously buried in the sediment. The Revised 22 March 2018 remobilization of buried organic matter, thallium (Tl), cadmium (Cd), copper (Cu) and zinc Accepted 22 March 2018 (Zn) from sediment was studied in a laboratory experiment with three organisms: tubificid, Available online 29 March 2018 chironomid larvae and loach. Results showed that bioturbation/bioirrigation promoted the release of dissolved organic matter (DOM) and dissolved Tl, Cd, Cu and Zn, but only Keywords: dissolved Zn concentrations decreased with exposure time in overlying water. The Bioturbation/bioirrigation presence of organisms altered the compositions of DOM released from sediment, Heavy metal considerably increasing the percentage of fulvic acid-like materials (FA) and humic acid- Sediment like materials (HA). In addition, bioturbation/bioirrigation accelerated the growth and DOM reproduction of bacteria to enhance the proportion of soluble microbial byproduct-like materials (SMP). The DOM was divided into five regions in the three-dimensional excitation emission matrix (3D-EEM), and each part had different correlation with the dissolved heavy metal concentrations. Dissolved Cu had the best correlation with each of the DOM compositions, indicating that Cu in the sediment was in the organic-bound form. Furthermore, the organism type and heavy metal characteristics both played a role in influencing the remobilization of heavy metal. © 2018 The Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences. Published by Elsevier B.V.

Introduction scale of mining and heavy metal smelting, pollution due to heavy metals has become a serious problem in the water environment Sediment is a natural reservoir of nutrients, organic compounds (Singh and Kumar, 2017). In one example, the wastewater and various dissolved substances in aquatic ecosystems (Boehler discharge from a Zn/Pb smelter caused a sudden spike in Tl et al., 2017; Miller et al., 2014; Skierszkan et al., 2013; Watmough, pollution in the nearby waters (0.18–1.03 Tl μg/L) (NCNA, 2010). 2017; Woodruff et al., 1999; Yu et al., 2017; Zhou et al., 2017; Zhu et More than 10 poisoning events involving Tl have occurred in al., 2017). In the aquatic environment, heavy metals from natural China since 1997 (Xiao et al., 2012). In addition, Cd, Cu and Zn are and anthropogenic sources find their way into surface water and commonly occurring heavy metals. Cd and Zn mines are generally accumulate in sediment (Ciutat et al., 2005; Xiong et al., intermixed due to their similar chemical properties (Gu et al., 2017; Zhao et al., 2017). In recent years, with development of the 2013; Moore et al., 2011). Both Cu (Hopkin, 1989)andZn

⁎ Corresponding author. E-mail: [email protected] (Bin Men).

https://doi.org/10.1016/j.jes.2018.03.031 1001-0742/© 2018 The Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences. Published by Elsevier B.V. JOURNAL OF ENVIRONMENTAL SCIENCES 75 (2019) 216– 223 217

(Christensen, 1995) are microelements needed for animal growth, north China. The sediment was sieved with a mesh of 0.5 mm but high accumulation of these metals is harmful to health. aperture to remove gravel, plants, organisms and other Organic matter (OM) and heavy metals coexist in sediment, and impurities. The percentage of sediment particle sizes below OM in sediment has been found to have important implications 60 μm, pH value and loss on ignition of the sediment was for heavy metal speciation, transport, and bioavailability 85.7%, 7.6 and 7.9%, respectively. Then both the sediment and (Bianchi, 2007; Blankson and Klerks, 2017; Dong et al., 2017). OM water were preserved after pretreatment (He et al., 2015). The and heavy metal in sediment were found to combine into simple sediment was spiked with TlNO3, Cd(NO3)2·4H2O, CuSO4·5H2O ormixedligandcomplexesthroughadsorption or complexation, and ZnSO4·7H2O (AR) successively to obtain nominal Tl(I), Cd which affect their environmental behaviors in sediment (II), Cu(II) and Zn(II) concentrations of 11.7 ± 0.3 mg/kg, 11.3 ± (Drouillard et al., 1996; Szkokan-Emilson et al., 2014; 1.4 mg/kg, 587.1 ± 5.2 mg/kg and 715.3 ± 8.8 mg/kg in the Wallschlager et al., 1998). Researchers found that decrease of Ni sediment on a dry weight basis, respectively. Before being and Zn in the overlying water was more likely related to an added to the experimental units, the contaminated sediment association with the organic carbon in the sediment due to was aged in a dark environment for 2 months. Five hundred disturbance (Collins and Kinsela, 2010; Schroeder et al., 2017), grams of the contaminated sediment was placed in plastic while the association of metals with dissolved organic matter aquaria (height 13.8 cm, diameter 10 cm), and 500 mL aerated (DOM) increased significantly due to the loss of reactive Mn-oxide reservoir water was used as the overlying water. The units and Fe-oxyhydroxide sorption phases during reduction (Vink et were left to stand for 24 hr to settle sediment particles that al., 2010). However, research on the relationship between were re-suspended when the overlying water was introduced. remobilization of OM and heavy metals is lacking. The three organisms were cultivated under the experimental Furthermore, the activities of benthic organisms have been conditions for one week. The tubificids were cultivated in found to influence the exchange of dissolved substances in pump tap water, chironomid larvae were in a wet container sediment in different ways (Zhang et al., 2010). This includes with changing water daily and loach were kept in an aerated the mediation of flux, which is due to direct interception by water. benthic organisms, such as the sediment particle re-suspension by the movement of the organisms, ingestion and 1.2. Experimental setup biological sedimentation. Also, indirect effects of change on the physical properties of sediment are caused by building A total of 16 aquaria were randomly assigned to one of four pipelines and depressions with bioturbation/bioirrigation, different treatments: without organisms for control, with which also change the physical and chemical condition of tubificid, with chironomid larvae or with loach. The design water simultaneously (Graf and Rosenberg, 1997; Svensson, included 4 parallel units in each treatment. Five hundred 1998). In addition, bioturbation/bioirrigation causes the trans- individuals of tubificid, 62 individuals of chironomid larvae, or mission of particulate matter in the highest redox reduction 1 individual loach were introduced into each biological unit, zones to enhance the oxidation and reduction for OM respectively. All 16 units were placed in an artificial climate remineralization (Aller, 1994). Bioturbation/bioirrigation also chamber (RXZ intelligent, Ningbo Jiangnan Instrument Fac- could alter the speciation and distribution of heavy metals in tory). The temperature was maintained at 23°C, humidity the sediment to encourage their release. Several studies have remained at 50% and the daily period of light:dark was 16:8 hr demonstrated that bioturbation/bioirrigation has an effect on throughout the entire experiment. the transport of heavy metals across the interface of sediment and water (Blankson and Klerks, 2016, 2017; Brumbaugh et al., 1.3. Sampling and analysis 2013; He et al., 2015, 2017; Men et al., 2016; Schaller, 2014). The aim of this study was to investigate the effect of Twenty milliliters of overlying water was sampled with a bioturbation/bioirrigation by different types of organisms on polypropylene syringe at days 1, 3, 5, and 7 after addition of the transport of DOM and heavy metals from sediment into animals, and filtered through a 0.45 μm mixed cellulose ester the overlying water. We studied the effect of different species, membrane filter (0.45 μm, d = 25 mm, Millipore, USA). Each the molecular weight distribution of the OM and the correla- sample was put into a brown glass bottle and placed in a dark tion between these organic substances and concentrations of environment at 4°C. The DOM concentration was detected by heavy metals in the overlying water respectively. Four a total organic carbon analyzer (TOC-VCPH, Shimadzu, Japan). experimental conditions were set up simultaneously in this The composition of DOM was determined by three-dimen- paper: control (without organisms), with tubificid (Limnodrilus sional excitation emission matrix (3D-EEM) fluorescence hoffmeisteri), with chironomid larvae (Chironomus plumosus spectroscopy (F-4500, Hitachi, Japan). Heavy metal concentra- larvae) and with loach (Misgurnus bipartitus). tions were detected by inductively coupled plasma mass spectrometry (ICP-MS, 7500a, Agilent, USA). The molecular weight distribution of DOM was characterized by the high- performance size exclusion chromatography (HPSEC) method, 1. Materials and methods using a high-performance liquid chromatography system (Waters 1525, Waters, USA) coupled with a size exclusion 1.1. Preparation of contaminated sediments and aquaria chromatography column (Shodex Protein KW-802.5, Shoko, Japan). Samples were filtered through a 0.22 μm mixed Sediment and water were collected from uncontaminated cellulose ester membrane filter (0.22 μm, d =25mm, surface sediment (0–30 cm) in the Ming Tombs Reservoir in Millipore, USA) before analysis by HPSEC. 218 JOURNAL OF ENVIRONMENTAL SCIENCES 75 (2019) 216– 223

1.4. Data analysis (HA), and a small amount of fulvic acid-like materials (FA) in the four treatments. The fluorescence regional integration The data were prepared using Excel 2007. Statistical analyses (FRI) (Table 1)(Chen et al., 2003) showed that, at the end of the were performed using Origin 9.0 and SPSS Base 15.0 software. exposure, the FRI of APN I decreased 7%, while the FRI of APN Pearson correlation coefficients were determined between II, SMP, FA and HA increased 34%, 41%, 71% and 73% in the compositions of DOM and Tl, Cd, Cu and Zn concentrations in control group, respectively. In the tubificid group, the FRI of the overlying water. All samples were measured in triplicate. APN I, APN II, SMP, FA and HA increased 49%, 82%, 49%, 164% The method detection limits for the DOM and heavy metals and 149%, respectively. In the chironomid larvae group, the were μg/L and ng/L. The ICP-MS was based on standard FRI of APN I, APN II, SMP, FA and HA increased 79%, 48%, 38%, quality control procedures using internal standards (yttrium 135% and 117%, respectively. In the loach group, the FRI of and indium). APN I, APN II, SMP, FA and HA increased 30%, 58%, 51%, 91% and 83%, respectively.

2. Results 2.3. The concentrations of dissolved heavy metals

2.1. The concentration and molecular weight distribution of The concentrations of dissolved heavy metals in the overlying DOM water are shown in Fig. 3. At the beginning of exposure, the dissolved Tl concentration was 4.3, 4.5, 4.4 and 6.2 μg/L in the The concentrations of DOM in the overlying water are shown in control, tubificid, chironomid larvae and loach groups, re- Fig. 1a.Duringtheexposuretime,theDOMconcentration spectively. Only the control group showed a decrease in the increased slowly from 9.4 to 10.3 mg/L in the control group and dissolved Tl concentration at the end of exposure. The from 13.5 to 16.2 mg/L in the tubificid group. At the beginning of dissolved Cd concentrations in the overlying water ranged exposure, the DOM concentration was 11.8 mg/L and increased to from 1.3 to 1.9 μg/L, 1.4 to 2.5 μg/L, 1.6 to 2.5 μg/L and 1.8 to 14.4 mg/L on the 3rd day, then the concentration maintained a 2.1 μg/L in the control, tubificid, chironomid larvae and loach steady state in the chironomid larvae group. DOM concentrations groups, respectively. The dissolved Cu concentrations ranged from 16.1 to 18.0 mg/L in the loach group. As shown in Fig. reached a maximum on the 5th day at 41.0, 50.2, 53.0 and 1b, the molecular weight distributions of DOM in the overlying 44.0 μg/L in the control, tubificid, chironomid larvae and loach water were similar among the control, tubificid and chironomid groups, respectively. The dissolved Zn concentrations were larvae groups. In the early exposure, the DOM was mainly highest on the 1st day of the exposure. The values were 3.1, composed of micromolecules, and the molecular weight was 3.6, 4.6 and 3.3 μg/L in the control, tubificid, chironomid larvae 100–1000 Da. After 5 days of exposure, the molecular weight of and loach groups, respectively. These values decreased with DOM was 1000–10,000 Da. In the loach group, the DOM molecular exposure time, reaching 1.4, 1.9, 1.2 and 2.1 μg/L at the end of weight was 1000–10,000 Da on the third day of exposure, and exposure, respectively. later the DOM was dominated by macromolecules.

2.2. The composition of DOM 3. Discussion

EEM results for the DOM in the overlying water are shown in The concentrations of DOM in the overlying water increased Fig. 2. The DOM in the overlying water included abundant during the exposure time. These DOM mainly resulted from the protein-like materials (APN I and APN II), soluble microbial photodegradation of phytoplankton (Vodacek et al., 1995), byproduct-like materials (SMP), humic acid-like materials bacterial degradation (Nelson et al., 2004) and the cell leakage

Fig. 1 – Concentrations (a) (p < 0.05) and molecular weight distribution (b) of dissolved organic matter in the overlying water during the exposure time. Control, without organisms; Tubificid, presence of tubificids; Chironomid larvae, presence of chironomid larvae; Loach, presence of loach. JOURNAL OF ENVIRONMENTAL SCIENCES 75 (2019) 216– 223 219

Control Tubificid Chironimid larvaeLoach

a-1 b-1 c-1 d-1

a-3 b-3 c-3 d-3

a-5 b-5 c-5 d-5

a-7 b-7 c-7 d-7

Fig. 2 – The results of three-dimensional excitation emission matrix in the overlying water at the exposure time of 1 day (a-1, b-1, c-1 and d-1), 3 days (a-3, b-3, c-3 and d-3), 5 days (a-5, b-5, c-5 and d-5), and 7 days (a-7, b-7, c-7 and d-7). Control, without organisms; Tubificid, presence of tubificid; Chironomid larvae, presence of chironomid larvae; Loach, presence of loach.

of plankton and planktonic bacteria (Henderson et al., 2008; oscillation of redox, which was magnified by bioturbation/ Tzortziou et al., 2008). DOM concentrations in the biological bioirrigation in the sediment (Skoog and Arias-Esquivel, 2009; groups were higher than in the control group. This may be Valdes et al., 2009). However, the characteristics of heavy metals because the material exchange may be enhanced significantly also affected their release from sediment. Tl(I) had a strong by bioturbation/bioirrigation compared to molecular diffusion tendency to easily diffuse from the sediment to the overlying (Benoit et al., 2009), the biological waste contained many DOM water (He et al., 2015). Due to the stable forms of Cd in the (Qin et al., 2010; Vanni, 2002), and the bioturbation/bioirrigation sediment, its concentrations were lower than those of Tl in the enhanced the introduction of O2 to strengthen the heterotrophic overlying water. Only the concentrations of dissolved Zn processes that promoted the decomposition of OM in sediment declined with the exposure time. Apart from the Fe/Mn oxides (Gessner et al., 2010). The concentrations of heavy metals at the and metal sulfides adsorbing and coprecipitating with dissolved sediment–water interface were partly linked to the degradation Zn to remove it from the overlying water (Chapman et al., 1998; of OM (Amato et al., 2016; Furrer and Wehrli, 1993), and the Goldberg, 1954; Lewandowski and Hupfer, 2005; Luan and Vadas, increased release of heavy metals by higher bioturbation/ 2015; Tankere-Muller et al., 2007), there was also association bioirrigation (in the loach group) may be attributed to the same with the organic matter (Collins and Kinsela, 2010; Schroeder et reason (Amato et al., 2016). In addition, bioturbation/bioirrigation al., 2017). Organic ions acted as ligands for the metals, which resulted in re-suspension of some sediment particles (Atkinson reduced the concentration of free metal cations (Sanchez-Marin et al., 2007) to release dissolved Tl, Cd, Cu and Zn into overlying et al., 2007),sotheincreaseofDOMintheoverlyingwater water, as well as changes in the particle size of the suspended contributed to part of the decrease in the dissolved Zn sediment, affecting DOM release (Dong et al., 2016). The adsorbed concentration. The result was consistent with a previous study DOM on the sediment particles also released due to the (He et al., 2017). 220 JOURNAL OF ENVIRONMENTAL SCIENCES 75 (2019) 216– 223

Table 1 – EEM FRI of organic matter in the overlying water sediment as a consequence of building channels in the (unit: mg/L). sediment, and promoted the exchange of dissolved materials Exposure time APN APN SMP FA HA between pores and overlying water. These activities in- (day) I II creased the speed and amplitude of the decrease in the redox potential through respiration and aerobic decomposi- Control 1 0.85 0.92 2.18 1.12 5.16 3 0.74 1.15 2.58 1.55 7.00 tion of their metabolites; as a result, the flux of DOM between 5 0.80 1.21 2.78 1.70 7.69 sediment and water increased (Fanjul et al., 2015), and also 7 0.71 1.11 2.75 1.71 8.00 changed the forms of heavy metals in the sediment and Tubificid 1 0.96 1.09 2.22 1.01 4.11 enhanced their migration to the water (Calmano et al., 1993; 3 1.29 1.66 3.06 1.73 7.31 Du Laing et al., 2009; Hare et al., 1994; Huerta-Diaz et al., 1998; 5 1.87 2.04 3.18 2.13 8.13 Peterson et al., 1996; Qiao, 2011; Zoumis et al., 2001). In more 7 1.34 1.84 3.06 2.46 9.44 detail, tubificids could rapidly rework the deposits (Anschutz Chironomid 1 0.87 1.42 2.46 1.17 4.91 larvae 3 1.24 1.71 3.31 2.16 9.38 et al., 2012) and through selective ingestion of the organic 5 0.76 1.21 2.59 1.91 8.64 materials in sediment (Ciutat et al., 2006; Rhoads, 1974; Wu, 7 1.16 1.57 2.53 2.06 7.96 2010) to influence the release of DOM, and they have been Loach 1 1.05 1.25 2.81 1.51 6.83 shown to enhance OM processing (Mermillod-Blondin et al., 3 1.02 1.26 2.72 1.56 6.89 2000). Consistent with a previous study, the bioturbation/ 5 0.89 1.25 2.69 1.71 7.69 bioirrigation by chironomid larvae accelerated the release of 7 1.09 1.58 3.38 2.30 9.97 DOM and heavy metals from sediment to water (Schaller, EEM: excitation emission matrix; FRI: fluorescence regional 2014). The burrowing activities of chironomid larvae tripled integration; APN I: aromatic protein I; APN II: aromatic protein II; the oxygen uptake of sediment, to promote the decomposi- SMP: soluble microbial byproduct-like materials; FA: fulvic acid-like tion and mineralization of OM in surface sediments materials; HA: humic acid-like materials. (Lagauzere et al., 2011). Additionally, the feeding activities of the larvae caused a net downward transport of carbon (Adámek and Maršálek, 2012). In the absence of large Furthermore, bioturbation/bioirrigation by different types organisms, molecular oxygen permeated only a few milli- of organisms also affected the release of DOM and heavy meters into sediment (Revsbech et al., 1980); however, in the metals. Tubificid and chironomid larvae dug into the presence of loach, the material exchange between the

Fig. 3 – The concentrations of dissolved Tl, Cd, Cu and Zn in the overlying water during the exposure time (p < 0.05). Control, without organisms; Tubificid, presence of tubificid; Chironomid larvae, presence of chironomid larvae; Loach, presence of loach. JOURNAL OF ENVIRONMENTAL SCIENCES 75 (2019) 216– 223 221 surface sediments and the overlying water was rapidly balanced with their strong activities, so the concentration 4. Conclusions of DOM was basically in equilibrium in the loach group. This would explain the release of large-molecular-weight OM to Bioturbation/bioirrigation could accelerate the DOM release the overlying water by the bioturbation/bioirrigation of from sediment to overlying water, and the DOM was mainly loach. composed of HA and FA. The composition of DOM changed During the exposure, the five EEM regions of DOM with bioturbation/bioirrigation exposure time, such as the increased, especially those corresponding to the FA and increase of SMP, which was the result of the boom of bacterial HA. The increase of SMP suggested that the presence of growth and propagation by bioturbation/bioirrigation. The organisms also stimulated the growth and reproduction of release of DOM was influenced by the bioturbation/ bacteria. The bioturbation/bioirrigation by tubificid substan- bioirrigation of different organism types. Furthermore, the tially influenced major microbial-driven biogeochemical DOM gradually became dominated by macromolecules, espe- reactions in sediment (Lagauzere et al., 2014), as did the cially in the loach group. The types of organisms affected the chironomid larvae and loach. Although some researchers bioturbation/bioirrigation results regarding the heavy metals. found that Cu and Zn had poor affinity for organic carbon Tubificid increased the dissolved Tl, Cd and Cu release to because of their higher deposition patterns in riverine overlying water, chironomid larvae increased Tl and Cu, and sediment (Rajmohan et al., 2014), up to 99% of Cu ions loach Tl, Cu and Zn. were found to be complexed with organic ligands in an aquatic ecosystem (Croot, 2003). The present study demonstrated that the dissolved Cu was mainly in organic-bound Acknowledgments forms (Du Laing et al., 2009), which was supported by the correlation between the dissolved heavy metal concentra- This study was sponsored by the National Natural Science tions and FRI of DOM in the five regions. In the control Foundation of China (Nos. 21677156, 41201498, 21107125, group, the FRI of APN II, SMP, FA and HA had good 51290282, 51608515), the National Water Pollution Control correlation with the dissolved Cu concentrations, and the and Treatment Science and Technology Major Project (No. FRI of APN II was also correlated well to the dissolved Cd 2015ZX07205-003), and the special fund from the State Key concentrations. In the tubificid group, the FRI of the five Joint Laboratory of Environment Simulation and Pollution regionswasallcorrelatedwelltoTl,CdandCuconcentra- Control (Research Center for Eco-environmental Sciences, tions. In the chironomid larvae group, however, the FRI of Chinese Academy of Sciences) (No. 16Z02ESPCR). SMP, FA and HA had good correlation with dissolved Tl and Cu concentrations, and the dissolved Zn concentrations were significantly negatively correlated to the FRI of FA REFERENCES and HA. In the loach group, the FRI of APN II, SMP, FA and HA was only correlated to dissolved Cu concentrations š (Table 2). Adámek, Z., Mar álek, B., 2012. Bioturbation of sediments by benthic macroinvertebrates and fish and its implication for pond ecosystems: a review. Aquac. Int. 21 (1), 1–17. Aller, R.C., 1994. Bioturbation and remineralization of sedimentary organic matter: effects of redox oscillation. Chem. Geol. Table 2 – The correlation between heavy metals 114 (3–4), 331–345. concentrations and EEM FRI of organic matter in the Amato, E.D., Simpson, S.L., Remaili, T.M., Spadaro, D.A., Jarolimek, overlying water. C.V., Jolley, D.F., 2016. Assessing the effects of bioturbation on APN I APN II SMP FA HA metal bioavailability in contaminated sediments by diffusive gradients in thin films (DGT). Environ. Sci. Technol. 50 (6), Control Tl 0.0636 0.1555 0.0244 −0.0401 0.0677 – ⁎⁎ ⁎ 3055 3064. Cd −0.0254 0.4870 0.7196 0.4968 0.4148 ⁎⁎ ⁎⁎ ⁎⁎ ⁎⁎ Anschutz, P., Ciutat, A., Lecroart, P., Gerino, M., Boudou, A., 2012. Cu 0.0114 0.7348 0.7235 0.8343 0.7424 Effects of tubificid worm bioturbation on freshwater sediment Zn 0.2392 0.0281 −0.082 −0.2939 −0.2120 – ⁎⁎ ⁎⁎ ⁎⁎ ⁎⁎ ⁎⁎ biogeochemistry. Aquat. Geochem. 18 (6), 475 497. Tubificid Tl 0.6940 0.7926 0.8131 0.7887 0.8130 ⁎⁎ ⁎⁎ ⁎⁎ ⁎⁎ ⁎⁎ Atkinson, C.A., Jolley, D.F., Simpson, S.L., 2007. Effect of overlying Cd 0.7347 0.8772 0.9199 0.8856 0.9115 ⁎⁎ ⁎⁎ ⁎⁎ ⁎⁎ ⁎⁎ water pH, dissolved oxygen, salinity and sediment disturbances Cu 0.7185 0.8582 0.7711 0.8771 0.9003 on metal release and sequestration from metal contaminated Zn −0.1005 −0.2353 −0.1555 −0.4710 −0.4727 – ⁎⁎ ⁎⁎ ⁎⁎ marine sediments. Chemosphere 69 (9), 1428 1437. Chironomid Tl 0.2943 0.2859 0.6740 0.8348 0.8772 Benoit, J.M., Shull, D.H., Harvey, R.M., Beal, S.A., 2009. Effect of larvae Cd −0.2001 −0.2525 0.2450 0.1875 0.3036 – ⁎⁎ ⁎⁎ ⁎⁎ bioirrigation on sediment water exchange of methylmercury Cu 0.2460 0.1624 0.6611 0.7690 0.8464 in Boston Harbor, Massachusetts. Environ. Sci. Technol. 43 (10), Zn −0.1753 −0.4330 −0.4705 − − – ⁎⁎ ⁎⁎ 3669 3674. 0.7501 0.7221 Bianchi, T.S., 2007. Biogeochemistry of Estuaries. Oxford Univer- Loach Tl 0.2111 0.1985 0.4183 0.2057 0.3808 sity Press. Cd −0.1535 −0.1559 0.1472 −0.1134 0.1733 ⁎⁎ ⁎⁎ ⁎⁎ ⁎⁎ Blankson, E.R., Klerks, P.L., 2016. The effect of bioturbation by Cu 0.4120 0.7606 0.8923 0.7916 0.8540 Lumbriculus variegatus on transport and distribution of lead in a − − − − Zn 0.2017 0.3980 0.3243 0.4779 0.4011 freshwater microcosm. Environ. Toxicol. Chem. 35 (5), – ⁎ p < 0.05. 1123 1129. ⁎⁎ p < 0.01. Blankson, E.R., Klerks, P.L., 2017. The effect of sediment characteristics on bioturbation-mediated transfer of lead, in 222 JOURNAL OF ENVIRONMENTAL SCIENCES 75 (2019) 216– 223

freshwater laboratory microcosms with Lumbriculus Gu, Z., Wu, M., Li, K., Ning, P., 2013. Variation of heavy metal variegatus. Ecotoxicology 26 (2), 227–237. speciation during the pyrolysis of sediment collected from Boehler, S., Strecker, R., Heinrich, P., Prochazka, E., Northcott, G.L., Dianchi Lake, China. Arab. J. Chem. 10, S2196–S2204. Ataria, J.M., et al., 2017. Assessment of urban stream sediment Hare, L., Carignan, R., Huertadiaz, M.A., 1994. A field study of pollutants entering estuaries using chemical analysis and metal toxicity and accumulation by benthic invertebrates; multiple bioassays to characterise biological activities. Sci. implications for the acid-volatile sulfide (AVS) model. Limnol. Total Environ. 593, 498–507. Oceanogr. 39 (7), 1653–1668. Brumbaugh, W.G., Besser, J.M., Ingersoll, C.G., May, T.W., Ivey, C. He, Y., Men, B., Yang, X., Wang, D., 2015. Bioturbation/bioirrigation D., Schlekat, C.E., et al., 2013. Preparation and characterization effect on thallium released from reservoir sediment by of nickel-spiked freshwater sediments for toxicity tests: different organism types. Sci. Total Environ. 532, 617–624. toward more environmentally realistic nickel partitioning. He, Y., Men, B., Yang, X., Li, Y., Xu, H., Wang, D., 2017. Investigation Environ. Toxicol. Chem. 32 (11), 2482–2494. of heavy metals release from sediment with bioturbation/ Calmano, W., Hong, J., Forstner, U., 1993. Binding and mobilisation bioirrigation. Chemosphere 184, 235–243. of heavy metals in contaminated sediments affected by pH Henderson, R.K., Baker, A., Parsons, S.A., Jefferson, B., 2008. and redox potential. Water Sci. Technol. 28 (8–9), 223–235. Characterisation of algogenic organic matter extracted from Chapman, P.M., Wang, F.Y., Janssen, C., Persoone, G., Allen, H.E., cyanobacteria, green algae and diatoms. Water Res. 42 (13), 1998. Ecotoxicology of metals in aquatic sediments: binding 3435–3445. and release, bioavailability, risk assessment, and remediation. Hopkin, S.P., 1989. Ecophysiology of Metals in Terrestrial Inverte- Can. J. Fish. Aquat. Sci. 55 (10), 2221–2243. brates. Elsevier Applied Science Publishers. Chen, W., Westerhoff, P., Leenheer, J.A., Booksh, K., 2003. Huerta-Diaz, M.A., Tessier, A., Carignan, R., 1998. Geochemistry of Fluorescence excitation–emission matrix regional integration trace metals associated with reduced sulfur in freshwater to quantify spectra for dissolved organic matter. Environ. Sci. sediments. Appl. Geochem. 13 (2), 213–233. Technol. 37 (24), 5701–5710. Lagauzere, S., Moreira, S., Koschorreck, M., 2011. Influence of Christensen, J.M., 1995. Human exposure to toxic metals: factors bioturbation on the biogeochemistry of littoral sediments of an influencing interpretation of biomonitoring results. Sci. Total acidic post-mining pit lake. Biogeosciences 8 (2), 339–352. Environ. 166 (1–3), 89–135. Lagauzere, S., Motelica-Heino, M., Viollier, E., Stora, G., Bonzom, J. Ciutat, A., Anschutz, P., Gerino, M., Boudou, A., 2005. Effects of M., 2014. Remobilisation of uranium from contaminated bioturbation on cadmium transfer and distribution into freshwater sediments by bioturbation. Biogeosciences 11 (12), freshwater sediments. Environ. Toxicol. Chem. 24 (5), 3381–3396. 1048–1058. Lewandowski, J., Hupfer, M., 2005. Effect of macrozoobenthos on Ciutat, A., Weber, O., Gerino, M., Boudou, A., 2006. Stratigraphic two-dimensional small-scale heterogeneity of pore water effects of tubificids in freshwater sediments: a kinetic study phosphorus concentrations in lake sediments: a laboratory based on X-ray images and grain-size analysis. Acta Oecol. 30 study. Limnol. Oceanogr. 50 (4), 1106–1118. (2), 228–237. Luan, H., Vadas, T.M., 2015. Size characterization of dissolved Collins, R.N., Kinsela, A.S., 2010. The aqueous phase speciation metals and organic matter in source waters to streams in and chemistry of cobalt in terrestrial environments. developed landscapes. Environ. Pollut. 197, 76–83. Chemosphere 79 (8), 763–771. Men, B., He, Y., Yang, X., Meng, J., Liu, F., Wang, D., 2016. Croot, P.L., 2003. Seasonal cycle of copper speciation in Gullmar Bioturbation effects on heavy metals fluxes from sediment Fjord, Sweden. Limnol. Oceanogr. 48 (2), 764–776. treated with activated carbon. Environ. Sci. Pollut. Res. 23 (9), Dong, J., Xia, X., Wang, M., Xie, H., Wen, J., Bao, Y., 2016. Effect of 9114–9121. recurrent sediment resuspension–deposition events on bio- Mermillod-Blondin, F., des Chatelliers, M.C., Gerino, M., Gaudet, J. availability of polycyclic aromatic hydrocarbons in aquatic P., 2000. Testing the effect of Limnodrilus sp. (Oligochaeta, environments. J. Hydrol. 540, 934–946. Tubificidae) on organic matter and nutrient processing in the Dong, W., Wan, J., Tokunaga, T.K., Gilbert, B., Williams, K.H., 2017. hyporheic zone: a microcosm method. Arch. Hydrobiol. 149 (3), Transport and humification of dissolved organic matter within 467–487. a semi-arid floodplain. J. Environ. Sci. 57, 24–32. Miller, H., Croudace, I.W., Bull, J.M., Cotterill, C.J., Dix, J.K., Taylor, Drouillard, K.G., Ciborowski, J.J.H., Lazar, R., Haffner, G.D., 1996. R.N., 2014. A 500 year sediment lake record of anthropogenic Estimation of the uptake of organochlorines by the mayfly and natural inputs to Windermere (English Lake District) using Hexagenia limbata (Ephemeroptera: Ephemeridae). J. Great double-spike lead isotopes, radiochronology, and sediment Lakes Res. 22 (1), 26–35. microanalysis. Environ. Sci. Technol. 48 (13), 7254–7263. Du Laing, G., Rinklebe, J., Vandecasteele, B., Meers, E., Tack, F.M.G., Moore, J.W., Stanitski, C.L., Jurs, P.C., 2011. Chemistry: The 2009. Trace metal behaviour in estuarine and riverine flood- Molecular Science. Brooks Cole. plain soils and sediments: a review. Sci. Total Environ. 407 (13), NCNA (New China News Agency), 2010. Production suspended at S 3972–3985. China smeltery as thallium contamination detected. Available: Fanjul, E., Escapa, M., Montemayor, D., Addino, M., Fernanda . http://news.xinhuanet.com/english2010/china/2010-10/22/c_ Alvarez, M., Grela, M.A., et al., 2015. Effect of crab bioturbation 13570289.htm. on organic matter processing in South West Atlantic intertidal Nelson, N.B., Carlson, C.A., Steinberg, D.K., 2004. Production of sediments. J. Sea Res. 95, 206–216. chromophoric dissolved organic matter by Sargasso Sea Furrer, G., Wehrli, B., 1993. Biogeochemical processes at the microbes. Mar. Chem. 89 (1–4), 273–287. sediment water interface — measurements and modeling. 2nd Peterson, G.S., Ankley, G.T., Leonard, E.N., 1996. Effect of International Symp on Environmental Geochemistry. Envi- bioturbation on metal-sulfide oxidation in surficial ronmental Geochemistry 2, pp. 117–119. freshwater sediments. Environ. Toxicol. Chem. 15 (12), Gessner, M.O., Swan, C.M., Dang, C.K., McKie, B.G., Bardgett, R.D., 2147–2155. Wall, D.H., et al., 2010. Diversity meets decomposition. Trends Qiao, Q., 2011. Study on the Influence Factors of the Speciation Ecol. Evol. 25 (6), 372–380. and Release of Heavy Metals in Sediment With Tubificid Goldberg, E.D., 1954. Marine geochemistry. 1. Chemical scavengers Bioturbation. (Master thesis). Jilin University, Changchun, of the sea. J. Geol. 62 (3), 249–265. China. Graf, G., Rosenberg, R., 1997. Bioresuspension and biodeposition: a Qin, X., Sun, H., Wang, C., Yu, Y., Sun, T., 2010. Impacts of crab review. J. Mar. Syst. 11 (3–4), 269–278. bioturbation on the fate of polycyclic aromatic hydrocarbons JOURNAL OF ENVIRONMENTAL SCIENCES 75 (2019) 216– 223 223

in sediment from the Beitang estuary of Tianjin, China. Vink, J.P.M., Harmsen, J., Rijnaarts, H., 2010. Delayed immobiliza- Environ. Toxicol. Chem. 29 (6), 1248–1255. tion of heavy metals in soils and sediments under reducing Rajmohan, N., Prathapar, S.A., Jayaprakash, M., Nagarajan, R., and anaerobic conditions; consequences for flooding and 2014. Vertical distribution of heavy metals in soil profile in a storage. J. Soils Sediments 10 (8), 1633–1645. seasonally waterlogging agriculture field in Eastern Ganges Vodacek, A., Hoge, F.E., Swift, R.N., Yungel, J.K., Peltzer, E.T., Basin. Environ. Monit. Assess. 186 (9), 5411–5427. Blough, N.V., 1995. The in situ and airborne fluorescence Revsbech, N.P., Sorensen, J., Blackburn, T.H., Lomholt, J.P., 1980. measurements to determine UV absorption coefficients and Distribution of oxygen in marine sediments measured with DOC concentrations in surface waters. Limnol. Oceanogr. 40 microelectrodes. Limnol. Oceanogr. 25 (3), 403–411. (2), 411–415. Rhoads, D.C., 1974. Organism–sediment relations on the muddy Wallschlager, D., Desai, M.V.M., Spengler, M., Windmoller, C.C., sea floor. Oceanogr. Mar. Biol. Annu. Rev. 12, 263–300. Wilken, R.D., 1998. How humic substances dominate mercury Sanchez-Marin,P.,Lorenzo,J.I.,Blust,R.,Beiras,R.,2007.Humic geochemistry in contaminated floodplain soils and sediments. acids increase dissolved lead bioavailability for marine J. Environ. Qual. 27 (5), 1044–1054. invertebrates. Environ. Sci. Technol. 41 (16), 5679–5684. Watmough, S.A., 2017. Historical and contemporary metal bud- Schaller, J., 2014. Bioturbation/bioirrigation by Chironomus gets for a boreal shield lake. Sci. Total Environ. 598, 49–57. plumosus as main factor controlling elemental remobilization Woodruff, S.L., House, W.A., Callow, M.E., Leadbeater, B.S.C., 1999. from aquatic sediments? Chemosphere 107, 336–343. The effects of biofilms on chemical processes in surficial Schroeder, H., Fabricius, A.-L., Ecker, D., Ternes, T.A., Duester, L., sediments. Freshw. Biol. 41 (1), 73–89. 2017. Metal(loid) speciation and size fractionation in sediment Wu, S., 2010. Experimental Study on the Influence of Tubificid pore water depth profiles examined with a new meso profiling Worms' Bioturbation on Pollution Releasing From the Sedi- system. Chemosphere 179, 185–193. ments of East Dongting Lake. (Master thesis). Changsha Singh, U.K., Kumar, B., 2017. Pathways of heavy metals contam- University of Science & Technology, Changsha, China. ination and associated human health risk in Ajay River basin, Xiao, T., Yang, F., Li, S., Zheng, B., Ning, Z., 2012. Thallium India. Chemosphere 174, 183–199. pollution in China: a geo-environmental perspective. Sci. Total Skierszkan, E.K., Irvine, G., Doyle, J.R., Kimpe, L.E., Blais, J.M., 2013. Environ. 421, 51–58. Is there widespread metal contamination from in-situ bitu- Xiong, Y., Xiao, T., Liu, Y., Zhu, J., Ning, Z., Xiao, Q., 2017. men extraction at Cold Lake, Alberta heavy oil field? Sci. Total Occurrence and mobility of toxic elements in coals from Environ. 447, 337–344. endemic fluorosis areas in the Three Gorges Region, SW China. Skoog, A.C., Arias-Esquivel, V.A., 2009. The effect of induced Ecotoxicol. Environ. Saf. 144, 1–10. anoxia and reoxygenation on benthic fluxes of organic carbon, Yu, J., Ding, S., Zhong, J., Fan, C., Chen, Q., Yin, H., et al., 2017. phosphate, iron, and manganese. Sci. Total Environ. 407 (23), Evaluation of simulated dredging to control internal phos- 6085–6092. phorus release from sediments: focused on phosphorus – Svensson, J.M., 1998. Emission of N2O, nitrification and denitrifi- transfer and resupply across the sediment water interface. cation in a eutrophic lake sediment bioturbated by Chironomus Sci. Total Environ. 592, 662–673. plumosus. Aquat. Microb. Ecol. 14 (3), 289–299. Zhang, L., Gu, X., Fan, C., Shang, J., Shen, Q., Wang, Z., et al., 2010. Szkokan-Emilson, E.J., Watmough, S.A., Gunn, J.M., 2014. Wet- Impact of different benthic animals on phosphorus dynamics lands as long-term sources of metals to receiving waters in across the sediment–water interface. J. Environ. Sci. 22 (11), mining-impacted landscapes. Environ. Pollut. 192, 91–103. 1674–1682. Tankere-Muller, S., Zhang, H., Davison, W., Finke, N., Larsen, O., Zhao, B., Liu, A., Wu, G., Li, D., Guan, Y., 2017. Characterization of Stahl, H., et al., 2007. Fine scale remobilisation of Fe, Mn, Co, Ni, heavy metal desorption from road-deposited sediment under Cu and Cd in contaminated marine sediment. Mar. Chem. 106 acid rain scenarios. J. Environ. Sci. 51, 284–293. (1–2), 192–207. Zhou, Z., Huang, T., Li, Y., Ma, W., Zhou, S., Long, S., 2017. Tzortziou, M., Neale, P.J., Osburn, C.L., Megonigal, J.P., Maie, N., Sediment pollution characteristics and in situ control in a deep Jaffe, R., 2008. Tidal marshes as a source of optically and drinking water reservoir. J. Environ. Sci. 52, 223–231. chemically distinctive colored dissolved organic matter in the Zhu, L., Liu, J., Xu, S., Xie, Z., 2017. Deposition behavior, risk Chesapeake Bay. Limnol. Oceanogr. 53 (1), 148–159. assessment and source identification of heavy metals in Valdes, J., Sifeddine, A., Ortlieb, L., Pierre, C., 2009. Interplay reservoir sediments of Northeast China. Ecotoxicol. Environ. between sedimentary organic matter and dissolved oxygen Saf. 142, 454–463. availability in a coastal zone of the Humboldt Current System; Zoumis, T., Schmidt, A., Grigorova, L., Calmano, W., 2001. Mejillones Bay, northern Chile. Mar. Geol. 265 (3–4), 157–166. Contaminants in sediments: remobilisation and Vanni, M.J., 2002. Nutrient cycling by animals in freshwater demobilisation. Sci. Total Environ. 266 (1–3), 195–202. ecosystems. Annu. Rev. Ecol. Syst. 33, 341–370.