Abstract
Exposure to trace metals is a leading factor associated with the development of non-communicable diseases. Aquatic ecosystems are not only effective agents of trace metal dispersion but are also at risk of contaminant enrichment. The use of sentinel organism as indicators of water quality is one method to evaluate potential human and ecological risk. An alternative or companion approach is to employ chemical techniques that mimic biotic accumulation/responses by aquatic fauna. The Diffusive Gradients-in-Thin-Films (DGT) technique has been widely used in bioavailability studies in water, soil and sediment. Many efforts have been made trying to understand the relationships between DGT labile determinations of trace elements and its biouptake by different organisms. However, the relationship between DGT labile determinations and the biological accumulation/response in aquatic animals is still not clear. The present work aims to improve the understanding of this relationship by summarizing the works using DGT devices and accumulation/response by animals in aquatic media. Several papers studying nineteen different elements in aquatic media are revised and discussed. The papers were separated and discussed in four categories: DGT and Biotic response, DGT and Bioaccumulation, DGT and Biomonitoring, and DGT and Bioturbation. DGT is expected to correlate well with the biological accumulation/responses in kinetically controlled situations. In biomonitoring studies, the use of chemical (DGT) and biological approaches gives complementary and high valuable information. The use of DGT and biological approaches should be considered in future studies about bioavailability and might improve the comprehension about uptake of trace metals by the aquatic fauna.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abel PD (2002) Water pollution biology. Taylor and Francis, London
Amato E, Simpson SL, Belzunce-Segarra MJ, Jarolimek CVE, Jolley DF (2015) Metal fluxes from porewaters and bioaccumulation in benthic invertebrates. Environ Sci Technol 49:14204–14212. https://doi.org/10.1021/acs.est.5b03655
Amato E, Simpson SL, Remaily TM, Spadaro DA, Jarolimek CVE, Jolley DF (2016) Assessing the effects of bioturbation on metal bioavailability in contaminated sediments by diffusive gradients in thin films (DGT). Environ Sci Technol 50:3055–3064. https://doi.org/10.1021/acs.est.5b04995
Andral B, Stanisiere JY, Sauzade D, Damier E, Thebault H, Galgani FE, Boissery P (2004) Monitoring chemical contamination levels in the Mediterranean based on the use of mussel caging. Mar Pollut Bull 49:704–712. https://doi.org/10.1016/j.marpolbul.2004.05.008
Batley GE, Apte SC, Stauber JL (2004) Speciation and bioavailability of trace metals in water: progress since 1982. Aust J Chem 57:903–919. https://doi.org/10.1071/CH04095
Bourgeault A, Gourlai-Francé C, Vincent-Hubert F, Palais F, Geffard A, Biagianti-Risgourg S, Pain-Devin S, Tusseau-Vuillemin MH (2010) Lessons from a transplantation of zebra mussels into a small urban river: an integrated ecotoxicological assessment. Environ Toxicol 25:468–487. https://doi.org/10.1002/tox.20591
Bourgeault A, Ciffroy P, Garnier C, Cossu-Leguille C, Masfaraud JF, Charlatchka R, Garnier JM (2013) Speciation and bioavailability of dissolved copper in different fresh waters: comparison of modelling, biological and chemical responses in aquatic mosses and gammarids. Sci Total Environ 452–453:68–77. https://doi.org/10.1016/j.scitotenv.2013.01.097
Bradac P, Behra R, Sigg L (2009) Accumulation of cadmium in periphyton under various freshwater speciation conditions. Environ Sci Technol 43:7291–7296. https://doi.org/10.1021/es9013536
Bradac P, Wagner B, Kistler D, Traber J, Behra R, Sigg L (2010) Cadmium speciation and accumulation in periphyton in a small stream with dynamic concentration variations. Environ Pollut 158:641–648. https://doi.org/10.1016/j.envpol.2009.10.031
Buzier R, Tusseau-Vuillemin MH, Mouchel JM (2006) Evaluation of DGT as a metal speciation tool in wastewater. Sci Total Environ 358:277–285. https://doi.org/10.1016/j.scitotenv.2005.09.051
Caro A, Chereau G, Briant N, Roques C, Freydier R, Delpoux S, Ecalas A, Elbaz-Poulichet F (2015) Contrasted responses of Ruditapes decussatus (filter and deposit feeding) and Loripes lacteus (symbiotic) exposed to polymetallic contamination (Port-Camargue, France). Sci Total Environ 505:526–534. https://doi.org/10.1016/j.scitotenv.2014.10.001
Casiot C, Egal M, Elbaz-Poulichet F, Bruneel O, Bancon-Monrigny C, Cordier MA, Gomez E, Aliaume C (2009) Hydrological and geochemical control of metals and arsenic in a Mediterranean river contaminated by acid mine drainage (the Amous River, France); preliminary assessment of impacts on fish (Leuciscus cephalus). Appl Geochem 24:787–799. https://doi.org/10.1016/j.apgeochem.2009.01.006
Chen M, Ding S, Liu L, Xu D, Han C, Zhang C (2015) Iron-coupled inactivation of phosphorus in sediments by macrozoobenthos (chironomid larvae) bioturbation: evidences from high-resolution dynamic measurements. Environ Pollut 204:241–247. https://doi.org/10.1016/j.envpol.2015.04.031
Chen M, Ding S, Liu L, Xu D, Gong M, Tang H, Zhang C (2016) Kinectics of phosphorus release from sediments and its relationship with iron speciation influenced by the mussel (Corbicula fluminea) bioturbation. Sci Total Environ 542:833–840. https://doi.org/10.1016/j.scitotenv.2015.10.155
Chen M, Ding S, Liu L, Wang Y, Xing X, Wang D, Gong M, Zhang C (2017) Fine-scale bioturbation effects of tubificid worm (Limnodrilus hoffmeisteri) on the lability of phosphorus sediments. Environ Pollut 219:604–611. https://doi.org/10.1016/j.envpol.2016.06.023
Clarisse O, Lotufo GR, Hintelmann H, Best EPH (2012) Biomonitorng and assessment of monomethylmercury exposure in aquatic systems using DGT technique. Sci Total Environ 416:449–454. https://doi.org/10.1016/j.scitotenv.2011.11.077
Costello DM, Burton GA, Hammerschmidt CRE, Taulbee WK (2012) Evaluating the performance of diffusive gradients in thin films for predicting Ni sediment toxicity. Environ Sci Technol 46:10239–10246. https://doi.org/10.1021/es302390m
Dabrin A, Durand CL, Garric J, Geffard J, Geffard O, Ferrari BJD, Coquery M (2012) Coupling geochemical and biological approaches to assess the availability of cadmium in fresh water sediment. Sci Total Environ 42:308–315. https://doi.org/10.1016/j.scitotenv.2012.02.069
Degryse F, Smolders R, Zhang H, Davison W (2009) Predicting availability of mineral elements to plants with the DGT technique: a review of experimental data and interpretation by modelling. Environ Chem 6:198–218. https://doi.org/10.1071/EN09010
Ding S, Jia F, Xu D, Sun Q, Zhang L, Fan C, Zhang C (2011) High-resolution, two-dimensional measurement of dissolved reactive phosphorus in sediments using diffusive gradients in thin films technique in combination with routine procedure. Environ Sci Technol 45:9680–9686. https://doi.org/10.1021/es202785p
Divis P, Docekalova H, Brulik L, Pavli M, Hekera P (2007) Use of the diffusive gradients in thin films technique to evaluate (bio)available trace metal concentrations in river water. Anal Bioanal Chem 387:2239–2244. https://doi.org/10.1007/s00216-006-0996-y
Divis P, Machát J, Szkandera R, Docekalova H (2012) In situ measurement of bioavailable concentrations at the downstream on the Morava River using transplanted aquatic mosses and DGT technique. Int J Environ Res 6(1):87–94. https://doi.org/10.22059/ijer.2011.475
Estrada ES, Juhel G, Han P, Kelly BC, Lee WK, Bayen S (2017) Multi-tool assessment of trace metals in mangroves combining sediment and clam sampling, DGT passive samplers and caged mussels. Sci Total Environ 574:847–857. https://doi.org/10.1016/j.scitotenv.2016.09.055
Ferreira D, Tousset N, Ridame C, Tusseau-Vuillemin MH (2008) More than inorganic copper is bioavailable to aquatic mosses at environmentally relevant concentrations. Environ Toxicol Chem 27(10):2108. https://doi.org/10.1897/07-249.1
Ferreira D, Ciffroy P, Tusseau-Vuillemin MH, Bourgeault A, Garnier JM (2013) DGT as surrogate of biomonitors for predicting the bioavailability of copper in freshwaters: an ex situ validation study. Chemosphere 91:241–247. https://doi.org/10.1016/j.chemosphere.2012.10.016
Forstner U (1983) Metal transfer between solid and aqueous phases. Springer, Berlin
He Y, Yang X, Li Y, Xu H, Wang D (2017) Investigation of heavy metals release from sediment with bioturbation/bioirrigation. Chemosphere 184:235–243. https://doi.org/10.1016/j.chemosphere.2017.05.177
Johnston E, Webb JA, Keough M (2003) Pulse disturbances and the colonization of hard-substrates and in situ determination of copper using diffusive gradients in thin films (DGT): quantifying dose and responses in the field. Biofouling 19(5):335–345. https://doi.org/10.1080/08927010310001612036
Jordan AM, Teasdale PR, Dunn RJK, Lee SY (2008) Modelling copper uptake by Saccostrea glomerata with diffusive gradient in thin films measurements. Environ Chem 5:274–280. https://doi.org/10.1071/EN07092
Lebrun JD, Dufour M, Uher E, Faburé J, Mons R, Charlatchka R, Gourlay-Francé C, Fechner LC, Ferrari BJD (2017) To what extend the dam dredging can influence the background level of metals in the Rhine River: using chemical and biological long-term monitoring to answer. Knowl Manag Aquat Ecosyst 418:54–65. https://doi.org/10.1051/kmae/2017049
Lin S, Taylor AA, Ji Z, Chang CH, Kinsinger NM, Ueng W, Walker SL, Nel AB (2015) Understanding the transformation, speciation, and hazard potential of copper particles in a model septic tank system using zebrafish to monitor effluent. ACS Nano 9(2):2038–2048. https://doi.org/10.1021/nn507216f
Luider CD, Crusius J, Playle RC, Curtis PJ (2004) Influence of natural organic matter source on copper speciation as demonstrated by Cu binding to fish gills, ion selective electrode, and by DGT gel sampler. Environ Sci Technol 38:2865–2872. https://doi.org/10.1021/es030566y
Mangal V, Zhu Y, Shi YX, Guéguen C (2016) Assessing cadmium and vanadium accumulation using diffusive gradient in thin-films (DGT) and phytoplankton in the Churchill River estuary, Manitoba. Chemopshere 163:90–98. https://doi.org/10.1016/j.chemosphere.2016.08.008
Martin AJ, Goldblatt R (2007) Speciation, behavior, and bioavailability of copper downstream of a mine-impacted lake. Environ Toxicol Chem 26(12):2594–2603. https://doi.org/10.1897/07-038.1
Menegario AA, Yabuki LMN, Luko KS, Williams PN, Blackburn DM (2017) Use of diffusive gradient in thin films for in situ measurements: a review on the progress in chemical fractionation, speciation and bioavailability of metals in waters. Anal Chim Acta 983:54–66. https://doi.org/10.1016/j.aca.2017.06.041
Montero N, Belzunce-Segarra MJ, Del Campo A, Garmendia JM, Ferrer L, Larreta J, González M, Maidana MA, Espino M (2013) Integrative environmental assessment of the impact of the Pasaia harbour activities on Oiartzun estuary (southeastern Bay of Bisay). J Mar Syst 109–110:S252–S260. https://doi.org/10.1016/j.jmarsys.2011.06.002
Nedrich SM, Burton GA Jr (2017) Sediment Zn-release during post-drought re-flooding: assessing environmental risk to Hyalella azteca and Daphnia magna. Environ Pollut 230:1116–1124. https://doi.org/10.1016/j.envpol.2017.07.073
Niyogi S, Wood CM (2004) Biotic Ligand Model, a flexible tool for developing sit-specific water quality guidelines for metals. Environ Sci Technol 38(23):6177–6192. https://doi.org/10.1021/es0496524
Parthasarathi C, Zhao J, Chakrabarti CL (2009) Copper and nickel speciation in mine effluents by combination of two independent techniques. Anal Chim Acta 636:70–76. https://doi.org/10.1016/j.aca.2009.01.030
Pelcová P, Vicarová P, Ridosková A, Docekalová H, Kopp R, Mares J, Postulková E (2017) Prediction of mercury bioavailability to common carp (Cyprinus carpio L) using the diffusive gradient in thin films technique. Chemosphere 187:181–187. https://doi.org/10.1016/j.chemosphere.2017.08.097
Pellet B, Geffard O, Lacour C, Kermoal T, Gourlay-Francé CA (2009) A model predicting waterborne cadmium bioaccumulation in Gammarus pulex: the effects of dissolved organic ligands, calcium and temperature. Environ Toxicol Chem 28(11):2434–2442. https://doi.org/10.1897/09-042.1
Pisanello F, Marziali L, Rosignolli F, Poma G, Roscioli C, Pozzoni F, Guzzela L (2016) In situ bioavailability of DDT and Hg in sediments of the Toce River (Lake Maggiore basin, Northern Italy): accumulation in benthic invertebrates and passive samplers. Environ Sci Pollut Res 23:10542–10555. https://doi.org/10.1007/s11356-015-5900-x
Rainbow PS (2002) Trace metal concentrations in aquatic invertebrates: why and so what? Environ Pollut 120:497–507. https://doi.org/10.1016/S0269-7491(02)00238-5
Ren J, Luo J, Ma H, Wang X, Ma LQ (2013) Bioavailability and oxidative stress of cadmium to Corbicula fluminea. Environ Sci Process Impacts 15:860–869. https://doi.org/10.1016/j.chemosphere.2007.06.061
Roulier JL, Tusseau-Vuillemin MH, Coquery M, Garric J (2008) Measurements of dynamic mobilization of trace metals in sediments using DGT and comparison with bioaccumulation in Chironomus riparius: first results of an experimental study. Chemosphere 70:925–932. https://doi.org/10.1016/j.chemosphere.2007.06.061
Royset O, Rosseland BO, Kristensen T, Kroglund F, Garmo OA, Steiness E (2005) Diffusive gradients in thin films sampler predicts stress in brown trout (Salmo trutta L.) exposed to aluminum in acid fresh waters. Environ Sci Technol 39:1167–1174. https://doi.org/10.1021/es049538l
Sakellari A, Karavoltsos S, Theodorou D, Dassenakis M, Scoullos M (2013) Bioaccumulation of metals (Cd, Cu, Zn) by the marine bivalves M. galloprovincialis, P. radiate, V. verrucosa and C. chine in Mediterranean coastal microenvironments: association with metal bioavailability. Environ Monit Assess 185:3383–3395. https://doi.org/10.1007/s10661-012-2799-2
Schintu M, Durante L, Maccioni A, Meloni P, Degetto S, Contu A (2008) Measurements of environmental trace-metal levels in Mediterranean coastal areas with transplanted mussels and DGT techniques. Mar Pollut Bull 57:832–837. https://doi.org/10.1016/j.marpolbul.2008.02.038
Schoyen M, Allan IJ, Ruus A, Havardstun J, Hjermann DO, Beyer J (2017) Comparison of caged and native blue mussels (Mytilus edulis spp.) for environmental monitoring of PAH, PCB and trace metals. Mar Environ Res 130(221):232. https://doi.org/10.1016/j.marenvres.2017.07.025
Simpson SL, Yverneau H, Cremazy A, Jarolimek CV, Price HL, Jolley DF (2012) DGT- induced cupper flux predicts bioaccumulation and toxicity to bivalves in sediments with varying properties. Environ Sci Technol 46:9038–9046. https://doi.org/10.1021/es301225d
Slaveykova VI, Wilkinson KJ (2005) Predicting the bioavailability of metals and metal complexes: critical review of the biotic ligand model. Environ Chem 2:9–24. https://doi.org/10.1021/es301225d
Sondergaard J, Bach LE, Gustavson K (2014) Measuring bioavailable metals using diffusive gradients in thin films (DGT) and transplanted seaweed (Fucus vesiculosus), blue mussels (Mytilus edulis) and sea snails (Littorina sextalis) suspended from monitoring buoy near a former lead-zinc mine in West Greenland. Mar Pollut Bull 78:102–109. https://doi.org/10.1016/j.marpolbul.2013.10.054
Stark JS, Johnstone GJ, Palmer AS, Snape I, Larner BL, Riddle MJ (2006) Monitoring the remediation of a near shore waste disposal site in Antartica using the amphipod Paramoera walkeri and diffusive gradients in thin films (DGTs). Mar Pollut Bull 52:1595–1610. https://doi.org/10.1016/j.marpolbul.2006.05.020
Tusseau-Vuillemin MH, Gilbin R, Bakkaus E, Garric J (2004) Performance of diffusive gradient in thin films to evaluate the toxic fraction of copper to Daphnia magna. Environ Toxicol Chem 23(9):2154–2161. https://doi.org/10.1897/03-202a
Van der Geest HG, Paumen ML (2008) Dynamics of metal availability and toxicity in historically polluted floodplain sediments. Sci Total Environ 406:419–425. https://doi.org/10.1016/j.scitotenv.2008.05.052
Van Leeuwen HP, Town RM, Buffle J, Cleven RF, Davison W, Puy J, Van Riemsdijk WH, Sigg L (2005) Dynamic speciation analysis and bioavailability of metals in aquatic systems. Environ Sci Technol 9(22):8545–8556. https://doi.org/10.1021/es050404x
Vannuci-Silva M, Souza JM, Oliveira FF, Araujo MAG Jr, Francionni E, Eismann CE, Kiang CH, Govone JS, Belzunce-Segarra MJ, Menegario AA (2017) Bioavailability of metals at a southern Brazilian coastal area of high environmental concern under antropic influence: evaluation using transplanted bivalves (Nodipencten nodosus) and the DGT technique. Water Air Soil Pollut 228:222. https://doi.org/10.1007/s11270-017-3387-4
Waltham NJ, Teasdale PR, Connoly RM (2011) Contaminants in water, sediment and fish biomonitor species from natural and artificial estuarine habitats along the urbanized Gold Coast, Queensland. J Environ Monit 13:3409–3419. https://doi.org/10.1039/c1em10664c
Wang Z, Zhao P, Yan C, Chris VD, Yan Y, Chi Q (2014) Combined use of DGT and transplanted shrimp (Litopenaeus vannamei) to assess the bioavailable metal of complex contamination: implication for implementing bioavailability-based water quality criteria. Environ Sci Pollut Res 21:4502–4515. https://doi.org/10.1007/s11356-013-2415-1
Wang P, Yao Y, Wang C, Hou J, Qian J, Miao L (2017) Impact of macrozoobenthic bioturbation and wind fluctuation interactions on net methylmercury in freshwater lakes. Water Res 123:320–330. https://doi.org/10.1016/j.watres.2017.07.072
Webb JA, Keough MJ (2002) Measurement of environmental trace-metal levels with transplanted mussels and diffusive gradients in thin films (DGT): a comparison of techniques. Mar Pollut Bull 44:222–229. https://doi.org/10.1016/S0025-326X(01)00244-2
Yao Y, Wang C, Wang P, Hou J, Wang T, Liu C, Yuan E (2016) In situ, high-resolution ZrO-Chelex DGT for the investigation of iron-coupled inactivation of arsenic in sediments by macrozoobenthos bioturbation and hydrodynamic interactions. Sci Total Environ 562:451–462. https://doi.org/10.1016/j.scitotenv.2016.03.172
Yin H, Cai Y, Duan H, Gao J, Fan C (2014) Use of DGT and conventional methods to predict sediment metal bioavailability to a field inhabitant freshwater snail (Bellamya aeruginosa) from Chinese eutrophic lakes. J Hazard Mater 264:184–194. https://doi.org/10.1016/j.jhazmat.2013.11.030
Zhang H, Davison W (1995) Performance characteristics of diffusion gradients in thin films for the in situ measurement of trace metal in aqueous solution. Anal Chem 67:3391–3400. https://doi.org/10.1021/ac00115a005
Zhang H, Davison W (1999) Diffusional characteristics of hydrogels used in DGT and DET techniques. Anal Chim Acta 398(2–3):329–340. https://doi.org/10.1016/s0003-2670(99)00458-4
Zhang H, Davison W (2000) Direct in situ measurements of labile inorganic and organically bound metal species in synthetic solutions and natural waters using diffusive gradients in thin films. Anal Chem 72:4447–4457. https://doi.org/10.1021/ac0004097
Zhang H, Davison W (2015) Use of diffusive gradients in thin-films for studies of chemical speciation and bioavailability. Environ Chem 12:85–101. https://doi.org/10.1071/EN14105
Zhao CM, Campbell PGC, Wilkinson KJ (2016) When are metal complexes bioavailable. Environ Chem 13:423–425. https://doi.org/10.1071/EN15205
Zhou Q, Zhang J, Fu J, Shi J, Jiang G (2008) Biomonitoring: an appealing tool for assessment of metal pollution in the aquatic system. Anal Chim Acta 606:135–150. https://doi.org/10.1016/j.aca.2007.11.01
Acknowledgements
The authors thank the foundations of Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP: 2015/03397-4 and 2015/50306-4), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq: 304849/2016-2 and 403666/2016-3) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes) for their financial support.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Eismann, C.E., Menegário, A.A., Gemeiner, H. et al. Predicting Trace Metal Exposure in Aquatic Ecosystems: Evaluating DGT as a Biomonitoring Tool. Expo Health 12, 19–31 (2020). https://doi.org/10.1007/s12403-018-0280-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12403-018-0280-3