Environmental Science and Pollution Research

, Volume 26, Issue 19, pp 19549–19559 | Cite as

Predicting mercury bioavailability in soil for earthworm Eisenia fetida using the diffusive gradients in thin films technique

  • Viet Huu Nguyen
  • Seah Kah Yee
  • Yongseok Hong
  • Deok Hyun Moon
  • Seunghee HanEmail author
Research Article


In general, the diffusive gradients in thin films (DGT) technique is an effective tool for evaluating metal bioavailability; however, its applicability is subject to the type of metal and organism involved. In this study, the accumulated masses of Hg in DGT probes and in the earthworm species Eisenia fetida were monitored for 10 days, to test if the DGT technique can be used as a predicting method for the bioavailability of soil Hg to earthworms. In the Hg exposure tests using soils prepared with different peat moss concentrations of 5, 10, 15, and 20% and varying pH values of 4.6, 5.6, and 6.2, the experimentally determined DGT-soil accumulation factor (DSAF) and biota-soil accumulation factor (BSAF) both increased as the peat moss content decreased and the pH increased. According to a one compartment model, this was a result of the increased Hg uptake rate constant (k1) and the relatively stable Hg elimination constant (k2) under lower peat moss and higher pH conditions. It is interesting to note that the Hg uptake rates by DGT and earthworms were considerably higher for fresh soils than for aged soils, while porewater (and acid-extractable) Hg concentrations were rather similar between the two types of soils. Across diverse soil properties, steady-state Hg in earthworm tissue showed a strong positive correlation with DGT-measured Hg flux ([earthworm Hg] = 354(DGT−Hg flux)−34, r2 = 0.88), while meager correlations were found between Hg concentration in earthworms and that in porewater (and acid-extractable). The overall results indicate that DGT-measured Hg flux is a better tool than conventional methods for predicting Hg bioavailability for earthworms inhabiting diverse types of soil.


Diffusive gradients in thin films Bioavailability Mercury Earthworms pH Peat moss 



This study was supported by the GIST Research Institute (GRI) grant funded by the GIST in 2019, and the Polar Academic Program (PE18900).

Supplementary material

11356_2019_5180_MOESM1_ESM.docx (90 kb)
ESM 1 (DOCX 90 kb)


  1. Amato ED, Simpson SL, Jarolimek CV, Jolley DF (2014) Diffusive gradients in thin films technique provide robust prediction of metal bioavailability and toxicity in estuarine sediments. Environ Sci Technol 48:4485–4494CrossRefGoogle Scholar
  2. Amato ED, Simpson SL, Belzunce-Segarra MJ, Jarolimek CV, Jolley DF (2015) Metal fluxes from porewaters and labile sediment phases for predicting metal exposure and bioaccumulation in benthic invertebrates. Environ Sci Technol 49:14204–14212CrossRefGoogle Scholar
  3. Amato ED, Simpson SL, Remaili TM, Spadaro DA, Jarolimek CV, Jolley DF (2016) Assessing the effects of bioturbation on metal bioavailability in contaminated sediments by diffusive gradients in thin films (DGT). Environ Sci Technol 50:3055–3064CrossRefGoogle Scholar
  4. Amato ED, Marasinghe Wadige CPM, Taylor AM, Maher WA, Simpson SL, Jolley DF (2018) Field and laboratory evaluation of DGT for predicting metal bioaccumulation and toxicity in the freshwater bivalve Hyridella australis exposed to contaminated sediments. Environ Pollut 243:862–871CrossRefGoogle Scholar
  5. Amirbahman A, Massey DI, Lotufo G, Steenhaut N, Brown LE, Biedenbach JM, Magar VS (2013) Assessment of mercury bioavailability to benthic macroinvertebrates using diffusive gradients in thin films (DGT). Environ Sci: Processes Impacts 15:2104–2114Google Scholar
  6. Bade R, Oh S, Shin WS (2012) Diffusive gradients in thin films (DGT) for the prediction of bioavailability of heavy metals in contaminated soils to earthworm (Eisenia foetida) and oral bioavailable concentrations. Sci Total Environ 416:127–136CrossRefGoogle Scholar
  7. Caillat A, Ciffroy P, Grote M, Rigaud S, Garnier J-M (2014) Bioavailability of copper in contaminated sediments assessed by a DGT approach and the uptake of copper by the aquatic plant Myriophyllum aquaticum. Environ Toxicol Chem 33:278–285CrossRefGoogle Scholar
  8. Chen J, Shiyab S, Han FX, Monts DL, Waggoner CA, Yang Z, Su Y (2009) Bioaccumulation and physiological effects of mercury in Pteris vittata and Nephrolepis exaltata. Ecotoxicology 18:110–121CrossRefGoogle Scholar
  9. Clarisse O, Foucher D, Hintelmann H (2009) Methylmercury speciation in the dissolved phase of a stratified lake using the diffusive gradient in thin film technique. Environ Pollut 157:987–993CrossRefGoogle Scholar
  10. Clarisse O, Dimock B, Hintelmann H, Best EPH (2011) Predicting net mercury methylation in sediments using diffusive gradient in thin films measurements. Environ Sci Technol 45:1506–1512CrossRefGoogle Scholar
  11. Clarisse O, Lotufo GR, Hintelmann H, Best EPH (2012) Biomonitoring and assessment of monomethylmercury exposure in aqueous systems using the DGT technique. Sci Total Environ 416:449–454CrossRefGoogle Scholar
  12. Cornel PK, Summers RS, Roberts PV (1986) Diffusion of humic acid in dilute aqueous solution. J Colloid Interface Sci 110:149–164CrossRefGoogle Scholar
  13. De Jonge M, Blust R, Bervoets L (2010) The relation between acid volatile sulfides (AVS) and metal accumulation in aquatic invertebrates: implications of feeding behavior and ecology. Environ Pollut 158:1381–1391CrossRefGoogle Scholar
  14. Desaules A (2012) Critical evaluation of soil contamination assessment methods for trace metals. Sci Total Environ 426:120–131CrossRefGoogle Scholar
  15. Duquène L, Vandenhove H, Tack F, Van Hees M, Wannijn J (2010) Diffusive gradient in thin films (DGT) compared with soil solution and labile uranium fraction for predicting uranium bioavailability to ryegrass. J Environ Radioact 101:140–147CrossRefGoogle Scholar
  16. Ernstberger H, Zhang H, Tye A, Young S, Davison W (2005) Desorption kinetics of Cd, Zn, and Ni measured in soils by DGT. Environ Sci Technol 39:1591–1597CrossRefGoogle Scholar
  17. Fernández-Martínez R, Rucandio I (2013) Assessment of a sequential extraction method to evaluate mercury mobility and geochemistry in solid environmental samples. Ecotoxicol Environ Saf 97:196–203CrossRefGoogle Scholar
  18. Hamels F, Malevé J, Sonnet P, Kleja DB, Smolders E (2014) Phytotoxicity of trace metals in spiked and field-contaminated soils: linking soil-extractable metals with toxicity. Environ Toxicol Chem 33:2479–2487CrossRefGoogle Scholar
  19. He Y, Guo C, Lv J, Hou S, Zhang Y, Zhang Y, Xu J (2018) Predicting trace metal bioavailability to chironomids in sediments by diffusive gradients in thin films. Sci Total Environ 636:134–141CrossRefGoogle Scholar
  20. Hong Y, Dan NP, Kim E, Choi H-J, Han S (2014) Application of diffusive gel-type probes for assessing redox zonation and mercury methylation in the Mekong Delta sediment. Environmental Science: Processes & Impacts 16:1799–1808Google Scholar
  21. Hong YS, Rifkin E, Bouwer EJ (2011) Combination of diffusive gradient in a thin film probe and IC-ICP-MS for the simultaneous determination of CH3Hg+ and Hg2+ in oxic water. Environ Sci Technol 45:6429–6436CrossRefGoogle Scholar
  22. Li J, Peng Q, Liang D, Liang S, Chen J, Sun H, Li S, Lei P (2016) Effects of aging on the fraction distribution and bioavailability of selenium in three different soils. Chemosphere 144:2351–2359CrossRefGoogle Scholar
  23. Liu J, Feng X, Qiu G, Anderson CWN, Yao H (2012) Prediction of methyl mercury uptake by Rice plants (Oryza sativa L.) using the diffusive gradient in thin films technique. Environ Sci Technol 46:11013–11020CrossRefGoogle Scholar
  24. Lu A, Zhang S, X-q S (2005) Time effect on the fractionation of heavy metals in soils. Geoderma 125:225–234CrossRefGoogle Scholar
  25. Noh S, Hong YS, Han S (2015) Application of diffusive gradients in thin films and core centrifugation methods to determine inorganic mercury and monomethylmercury profiles in sediment porewater. Environ Toxicol Chem 35:348–356CrossRefGoogle Scholar
  26. Noh S, Hong YS, Han S (2016) Application of diffusive gradients in thin films and core centrifugation methods to determine inorganic mercury and monomethylmercury profiles in sediment porewater. Environ Toxicol Chem 35:348–356CrossRefGoogle Scholar
  27. OECD (2016): Test no. 222: earthworm reproduction test (Eisenia fetida/Eisenia andrei) Google Scholar
  28. Pelcová P, Dočekalová H, Kleckerová A (2014) Development of the diffusive gradient in thin films technique for the measurement of labile mercury species in waters. Anal Chim Acta 819:42–48CrossRefGoogle Scholar
  29. Peng X, Fan Y, Jin J, Xiong S, Liu J, Tang C (2017) Bioaccumulation and biomagnification of ultraviolet absorbents in marine wildlife of the Pearl River Estuarine, South China Sea. Environ Pollut 225:55–65CrossRefGoogle Scholar
  30. Ren L-J, Wen T, Pan W, Y-s C, Xu L-L, Yu L-J, Yu C-Y, Zhou Y, An S-Q (2015) Nitrogen removal by ecological purification and restoration engineering in a polluted river. Clean: Soil, Air, Water 43:1565–1573Google Scholar
  31. Roig N, Sierra J, Ortiz JD, Merseburger G, Schuhmacher M, Domingo JL, Nadal M (2013) Integrated study of metal behavior in Mediterranean stream ecosystems: a case-study. J Hazard Mater 263(Part 1):122–130CrossRefGoogle Scholar
  32. Roulier S, Robinson B, Kuster E, Schulin R (2008) Analysing the preferential transport of lead in a vegetated roadside soil using lysimeter experiments and a dual-porosity model. Eur J Soil Sci 59:61–70Google Scholar
  33. Simpson SL, Yverneau H, Cremazy A, Jarolimek CV, Price HL, Jolley DF (2012) DGT-induced copper flux predicts bioaccumulation and toxicity to bivalves in sediments with varying properties. Environ Sci Technol 46:9038–9046CrossRefGoogle Scholar
  34. Sizmur T, Canário J, Gerwing TG, Mallory ML, O'Driscoll NJ (2013) Mercury and methylmercury bioaccumulation by polychaete worms is governed by both feeding ecology and mercury bioavailability in coastal mudflats. Environ Pollut 176:18–25CrossRefGoogle Scholar
  35. Skyllberg U, Bloom PR, Qian J, Lin C-M, Bleam WF (2006) Complexation of mercury(II) in soil organic matter: EXAFS evidence for linear two-coordination with reduced sulfur groups. Environ Sci Technol 40:4174–4180CrossRefGoogle Scholar
  36. Taylor DL, Linehan JC, Murray DW, Prell WL (2012) Indicators of sediment and biotic mercury contamination in a southern New England estuary. Mar Pollut Bull 64:807–819CrossRefGoogle Scholar
  37. Vandenhove H, Antunes K, Wannijn J, Duquène L, Van Hees M (2007) Method of diffusive gradients in thin films (DGT) compared with other soil testing methods to predict uranium phytoavailability. Sci Total Environ 373:542–555CrossRefGoogle Scholar
  38. 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 metals of complex contamination: implications for implementing bioavailability-based water quality criteria. Environ Sci Pollut Res 21:4502–4515CrossRefGoogle Scholar
  39. Warnken KW, Zhang H, Davison W (2006) Accuracy of the diffusive gradients in thin-films technique: diffusive boundary layer and effective sampling area considerations. Anal Chem 78:3780–3787CrossRefGoogle Scholar
  40. Wen B, Hu X-y, Liu Y, Wang W-s, Feng M-h, Shan X-q (2004) The role of earthworms (Eisenia fetida) in influencing bioavailability of heavy metals in soils. Biol Fertil Soils 40:181–187CrossRefGoogle Scholar
  41. Xu Q, Gao L, Peng W, Gao B, Xu D, Sun K (2018) Assessment of labile Zn in reservoir riparian soils using DGT, DIFS, and sequential extraction. Ecotoxicol Environ Saf 160:184–190CrossRefGoogle Scholar
  42. Yang Y, Liang L, Wang D (2008) Effect of dissolved organic matter on adsorption and desorption of mercury by soils. J Environ Sci 20:1097–1102CrossRefGoogle Scholar
  43. Yin H, Fan C (2011) Dynamics of reactive sulfide and its control on metal bioavailability and toxicity in metal-polluted sediments from Lake Taihu, China. Arch Environ Contam Toxicol 60:565–575CrossRefGoogle Scholar
  44. 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 264:184–194CrossRefGoogle Scholar
  45. Zarrouk S, Bermond A, Kolsi Benzina N, Sappin-Didier V, Denaix L (2014) Diffusive gradient in thin-film (DGT) models Cd and Pb uptake by plants growing on soils amended with sewage sludge and urban compost. Environ Chem Lett 12:191–199CrossRefGoogle Scholar
  46. Zhang H, Davison W (1995) Performance characteristics of diffusion gradients in thin films for the in situ measurement of trace metals in aqueous solution. Anal Chem 67:3391–3400CrossRefGoogle Scholar
  47. 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 72:4447–4457CrossRefGoogle Scholar
  48. Zhang H, Zhao F-J, Sun B, Davison W, McGrath SP (2001) A new method to measure effective soil solution concentration predicts copper availability to plants. Environ Sci Technol 35:2602–2607CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Earth Sciences and Environmental EngineeringGwangju Institute of Science and Technology (GIST)GwangjuRepublic of Korea
  2. 2.Department of Environmental Systems EngineeringKorea UniversitySejong CityRepublic of Korea
  3. 3.Department of Environmental EngineeringChosun UniversityGwangjuRepublic of Korea

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