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Assessing the effects of bioturbation on metal bioavailability in contaminated sediments by diffusive gradients in thin films (DGT) Elvio Diego Amato, Stuart L Simpson, Timothy Michael Remaili, David Spadaro, Chad V. Jarolimek, and Dianne F Jolley Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.5b04995 • Publication Date (Web): 05 Feb 2016 Downloaded from http://pubs.acs.org on February 13, 2016
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Environmental Science & Technology
Article Type: Research article
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Assessing the effects of bioturbation on metal bioavailability in contaminated sediments by diffusive gradients in thin films (DGT)
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Elvio D. Amato†‡, Stuart L. Simpson†*, Timothy M. Remaili †‡, David A. Spadaro†, Chad V. Jarolimek†, and
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Dianne F. Jolley ‡*
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† Centre for Environmental Contaminants Research, CSIRO Land and Water, Locked Bag 2007, Kirrawee, NSW 2232, Australia
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‡ School of Chemistry, University of Wollongong, NSW 2522, Australia
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* To whom correspondence may be addressed (
[email protected];
[email protected])
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Phone: +61 2 442213516; +61 2 97106807
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ABSTRACT.
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an organisms’ exposure to metals. Recently, the performance of the in situ technique of diffusive gradients
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in thin films (DGT) for predicting metal bioavailability has been investigated in response to the increasing
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demand of considering contaminant bioavailability in sediment quality assessments. In this study, we test
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the ability of the DGT technique for predicting the metal bioavailability in clean and contaminated
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sediments that are being subjected to varying degrees of sediments disturbance: low bioturbation (bivalve
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Tellina deltoidalis alone) and high bioturbation (bivalve and actively burrowing amphipod, Victoriopisa
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australiensis). Significant release of DGT-labile Cd, Ni, Pb and Zn, but lower Cu and Fe, occurred in the
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pore and overlying waters of sediments exposed to high bioturbation conditions, resulting in higher
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bioaccumulation of zinc in bivalves. Strong relationships were found between bioaccumulation of Pb and Zn
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and time-integrated DGT-metal fluxes, whereas poor relationships were obtained using total or dilute-acid
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extractable metal concentrations. This results demonstrate that DGT is a useful tool for assessing metal
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bioavailability in sediments, and can provide useful predictions of metal bioavailable to benthic organisms
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in dynamic sediment environments.
The burrowing and feeding activities of benthic organisms can alter metal speciation in sediments and affect
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Keywords: Passive sampling; In situ, metal fluxes; bioturbation; sub-lethal toxicity; amphipod; sediment quality assessment
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INTRODUCTION
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Metal bioavailability is strongly linked to metal speciation, which in sediments is regulated by
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biogeochemical processes. Burrowing and feeding activities of benthic organisms may alter the speciation of
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metals in sediments by mixing and transporting fluids and sediment particles1-3. The introduction of
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oxygenated water into sub-oxic and anoxic regions of the sediment may cause oxidation of dissolved Fe(II)
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and Mn(II) to iron and manganese oxyhydroxide solid phases, and also oxidation of labile sulfide phases
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such as acid-volatile sulfide (AVS).4-6 As these processes modify the partitioning of metals between
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dissolved and particulate phases and the fluxes of metals to the pore waters, they also modify the exposure
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and bioavailability of metals to the organisms in the sediments and overlying waters.7-9
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Diffusive gradients in thin films (DGT) is an in situ technique that measures fluxes of metals present
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in the sediment pore water as well as weakly-bound metals that dissociate from solid phases.10 In previous
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studies, we demonstrated that DGT metal fluxes can be used for predicting toxicity to the amphipod Melita
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plumulosa11 and the bivalve Tellina deltoidalis12 exposed to metal-contaminated marine sediments under
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laboratory conditions. For nickel-spiked freshwater sediments, Costello et al.13 found that DGT-nickel
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concentrations in surface sediments were less useful for predicting effects to macroinvertebrate abundance
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or diversity than the potentially simpler measurements, for example, dilute-acid extractable nickel (SEM-Ni)
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or (SEM-AVS)/foc (where SEM is simultaneously extracted metal released by the dilute-acid extraction,
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and foc is the fraction of organic carbon in the sediment).
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Many studies have observed useful relationships between DGT-labile metal concentrations and
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bioaccumulation, for example Roulier et al.14 for copper and lead in the freshwater chironomid
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Chironomus riparius; van der Geest and León Paumen15 for copper in the freshwater worm Tubifex; Dabrin
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et al.16 cadmium accumulation in the freshwater mud snail Potamopyrgus antipodarum; and, Amato et al.17
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for Cu, Pb and Zn and T. deltoidalis exposed to contaminated marine sediments under laboratory and field
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conditions.
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The majority of sediment toxicity and bioaccumulation studies are undertaken by exposing single
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species of organisms to contaminants in sediments. However, in most sediment environments a range of
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organisms coexist with differing behaviours and sensitivities to contaminants. The exposure and the risk
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posed by the contaminants to the organisms in natural environments may therefore be significantly
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influenced by the interactions between species and the behaviours that modify the bioavailability of
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contaminants in sediments.8,18 For sediment quality assessments that rely heavily on laboratory-based
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bioassays to assess potential impacts of contaminants to ecosystem health, neglecting to consider inter-
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organism interactions may result in inaccurate assessment outcomes.
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DGT sediment probes that are deployed through the sediment-water interface (SWI) can provide
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information on metal speciation in different compartments of the sediment (oxic, sub-oxic, anoxic), and
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potentially provide useful information on changes in metal bioavailability due to biological disturbance. In
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this study, the use of DGT-metal fluxes were investigated for assessing the exposure and predicting the
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bioaccumulation of metals in contaminated sediments as they are bioturbated by different organisms. Three ACS Paragon Plus Environment
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sediments with different levels of contamination and physical properties were exposed to bioturbation by
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either the bivalves T. deltoidalis alone (low bioturbation) or combined with the amphipod Victoriopisa
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australiensis (high bioturbation). The DGT-metal fluxes (Cd, Cu, Fe, Mn, Ni, Pb, Zn) and major
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bioaccumulated metals (Cu, Pb and Zn) were used to assess the degree to which the high bioturbation by the
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amphipod influenced the metal bioaccumulation by the bivalve, and the benefits gained from using DGT-
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metal flux measurements as an assessment tool, compared to other more traditional approaches such as total
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and dilute-acid extractable metal concentrations, and the excess of AVS over SEM (AVS-SEM).19,20
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MATERIALS AND METHODS
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General Methods. All plasticware used for analyses was new and cleaned by soaking in 10% (v/v) HNO3
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(BDH, AnalR) for ≥24 h then rinsed in deionised water (>18 MΩ·cm, Milli-Q, Millipore). Glass beakers
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used for bioassays were washed in a dishwasher (Gallay Scientific) with detergent followed by acid washing
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(1% HNO3) and rinsing with deionised water. All chemicals were analytical reagent grade or equivalent
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analytical purity.
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Filtered aliquots (0.45 µm, Sartorius) sampled from overlying waters were combined from replicates
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and used for dissolved metal analysis. Sediment subsamples were collected before transfer into test vessels
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and used to determine sediment chemical properties shown in Table 1. At the end of the experiment,
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additional sediment mini-cores (thickness = 1 cm, 4 cm deep) were extracted from each test vessel and
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immediately stored at -20 °C until analysis. These samples were used for investigating relationships between
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AEM concentrations and metal bioaccumulation in organisms exposed to sediments, as AEM concentrations
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were expected to change during the exposure period. The extrusion of sediment mini-cores (top and bottom
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1.3±0.2 cm) and preparation of sediment for acid-volatile sulfide (AVS) and AEM analyses were undertaken
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in a nitrogen gas-filled glove box. The fraction of fine particles of the sediment (
