Skip to main content

Advertisement

Log in

Earthworms and in vitro physiologically-based extraction tests: complementary tools for a holistic approach towards understanding risk at arsenic-contaminated sites

  • Original Paper
  • Published:
Environmental Geochemistry and Health Aims and scope Submit manuscript

Abstract

The relationship of the total arsenic content of a soil and its bioaccumulation by earthworms (Lumbricus rubellus and Dendrodrilus rubidus) to the arsenic fraction bioaccessible to humans, measured using an in vitro physiologically-based extraction test (PBET), was investigated. Soil and earthworm samples were collected at 24 sites at the former arsenic mine at the Devon Great Consols (DGC) in southwest England (UK), along with an uncontaminated site in Nottingham, UK, for comparison. Analysis of soil and earthworm total arsenic via inductively coupled plasma mass spectrometry (ICP-MS) was performed following a mixed acid digestion. Arsenic concentrations in the soil were elevated (204–9,025 mg kg−1) at DGC. The arsenic bioaccumulation factor (BAF) for both earthworm species was found to correlate positively with the human bioaccessible fraction (HBF), although the correlation was only significant (P ≤ 0.05) for L. rubellus. The potential use of both in vitro PBETs and earthworms as complementary tools is explored as a holistic and multidisciplinary approach towards understanding risk at contaminated sites. Arsenic resistant earthworm species such as the L. rubellus populations at DGC are presented as a valuable tool for understanding risk at highly contaminated sites.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • BARGE (the Bioaccessibility Research Group of Europe). (2008). Retrieved on 22 February 2008, from http://www.bgs.ac.uk/barge/home.html.

  • Blank, S., Seiter, C., & Bruce, P. (2001). Resampling stats in excel version 2. Arlington.

  • Camm, G. S., Glass, H. J., Bryce, D. W., & Butcher, A. R. (2004). Characterisation of a mining-related arsenic-contaminated site, Cornwall, UK. Journal of Geochemical Exploration, 82, 1–15.

    Article  CAS  Google Scholar 

  • Cave, M. R., Wragg, J., Palumbo, B., & Klinck, B. A. (2002). Measurement of the bioaccessibility of arsenic in UK soils. Environment Agency R&D Technical Report, P5-062/TR002.

  • Cave, M., Wragg, J., Klinck, B., Gron, C., Oomen, A., van de Wiele, T., et al. (2006). Preliminary assessment of a unified bioaccessibility method for potentially harmful elements in soils. Epidemiology, 17, 39.

    Article  Google Scholar 

  • Cotter-Howells, J., Charnock, J. M., Winters, C., Kille, P., Fry, J. C., & Morgan, A. J. (2005). Metal compartmentation and speciation in a soil sentinel: The earthworm, Dendrodrilus rubidus. Environmental Science and Technology, 39, 7731–7740.

    Article  CAS  Google Scholar 

  • Defra. (2002). The contaminated land exposure assessment model (CLEA): Technical basis and algorithms CLR10. Environment Agency.

  • Efron, B., & Tibshirani, R. J. (1993). An introduction to the bootstrap. Chapman & Hall.

  • Elteren, J., Zdenka, S., Iztok, A., & Hylke-Jan, G. (2005). An interdisciplinary physical-chemical approach for characterization of arsenic in a calciner residue dump in Cornwall (UK). Environmental Pollution, 139, 477–488.

    Google Scholar 

  • Fergusen, C., Nathanail, P., McCaffrey, C., Earl, N., Foster, N., Gillet, A., & Ogden, R. (2003). Method for deriving site-specific human health assessment criteria for contaminants in soil. Retrieved on 22 February 2000, from Scottish and Northern Ireland Forum for Environmental Research website. http://www.sniffer.org.uk/results.asp.

  • Green, K. A., Chenery, S. R., Barlow, T. S., Taylor, H., & Cook, J. M. (2006). A high productivity sample digestion and analysis methodology for the determination of major and trace elements by ICP, poster presentation. In 13th Biennial National Atomic Spectroscopy Symposium, Glasgow, UK.

  • Hamilton, E. I. (2000). Environmental variables in a holistic evaluation of land contaminated by historic mine wastes: A study of multi-element mine wastes in West Devon, England using arsenic as an element of potential concern to human health. Science of the Total Environment, 249, 171–221.

    Article  CAS  Google Scholar 

  • Hutton, C., Bryce, D. W., Russeau, W., Glass, H. J., Jenkin, L. E. T., Corns, W. T., et al. (2005). Aqueous and solid-phase speciation of arsenic in Cornish soils. Mineralogical Magazine, 69, 577–589.

    Article  CAS  Google Scholar 

  • Intawongse, M., & Dean, J. R. (2006). In-vitro testing for assessing oral bioaccessibility of trace metals in soil and food samples. TrAC—Trends in Analytical Chemistry, 25, 876–886.

    Article  CAS  Google Scholar 

  • Kavanagh, P. J., Farago, M. E., Thornton, I., & Braman, R. S. (1997). Bioavailability of arsenic in soil and mine wastes of the Tamar valley, SW England. Chemical Speciation and Bioavailability, 9, 77–81.

    CAS  Google Scholar 

  • Klinck, B. A., Palumbo, B., Cave, M. R., & Wragg, J. (2002). Arsenic dispersal and bioaccessibility in mine contaminated soils: A case study from an abandoned arsenic mine in Devon, UK. British Geological Survey, Research Report RR/04/003.

  • Langdon, C. J., Piearce, T. G., Black, S., & Semple, K. T. (1999). Resistance to arsenic-toxicity in a population of the earthworm Lumbricus rubellus. Soil Biology and Biochemistry, 31, 1963–1967.

    Article  CAS  Google Scholar 

  • Langdon, C. J., Piearce, T. G., Meharg, A. A., & Semple, K. T. (2001). Survival and behaviour of the earthworms Lumbricus rubellus and Dendrodrilus rubidus from arsenate-contaminated and non-contaminated sites. Soil Biology and Biochemistry, 33, 1239–1244.

    Article  CAS  Google Scholar 

  • Langdon, C. J., Meharg, A. A., Feldmann, J., Balgar, T., Charnock, J., Farquhar, M., et al. (2002). Arsenic-speciation in arsenate-resistant and non-resistant populations of the earthworm, Lumbricus rubellus. Journal of Environmental Monitoring, 4, 603–608.

    Article  CAS  Google Scholar 

  • Langdon, C. J., Piearce, T. G., Meharg, A. A., & Semple, K. T. (2003). Interactions between earthworms and arsenic in the soil environment: A review. Environmental Pollution, 124, 361–373.

    Article  CAS  Google Scholar 

  • Mariño, F., & Morgan, A. J. (1998). Equilibrated body metal concentrations in laboratory exposed earthworms: Can they be used to screen candidate metal-adapted populations? Applied Soil Ecology, 12, 179–189.

    Article  Google Scholar 

  • Mariño, F., & Morgan, A. J. (1999). The time-course of metal (Ca, Cd, Cu, Pb, Zn) accumulation from a contaminated soil by three populations of the earthworm, Lumbricus rubellus. Applied Soil Ecology, 12, 169–177.

    Article  Google Scholar 

  • Morgan, J. E., & Morgan, A. J. (1999). The accumulation of metals (Cd, Cu, Pb, Zn and Ca) by two ecologically contrasting earthworm species (Lumbricus rubellus and Aporrectodea caliginosa): Implications for ecotoxicological testing. Applied Soil Ecology, 13, 9–20.

    Article  Google Scholar 

  • Morgan, A. J., Winters, C., & Yarwood, A. (1994). Speed-mapping of arsenic distribution in the tissues of earthworms inhabiting arsenious soil. Cell Biology International, 18, 911–914.

    Article  CAS  Google Scholar 

  • Neuhauser, E. F., Cukic, Z. V., Malecki, M. R., Loehr, R. C., & Durkin, P. R. (1995). Bioconcentration and biokinetics of heavy metals in the earthworm. Environmental Pollution, 89, 293–301.

    Article  CAS  Google Scholar 

  • Oomen, A. G., Hack, A., Minekus, M., Zeijdner, E., Cornelis, C., Schoeters, G., et al. (2002). Comparison of five in vitro digestion models to study the bioaccessibility of soil contaminants. Environmental Science and Technology, 36, 3326–3334.

    Article  CAS  Google Scholar 

  • Palumbo-Roe, B., & Klinck, B. (2007). Bioaccessibility of arsenic in mine waste-contaminated soils: A case study from an abandoned arsenic mine in SW England (UK). Journal of Environmental Science and Health—Part A Toxic/Hazardous Substances and Environmental Engineering, 42, 1251–1261.

    CAS  Google Scholar 

  • Palumbo-Roe, B., Cave, M. R., Klinck, B. A., Wragg, J., Taylor, H., O’Donnell, K. E., et al. (2005). Bioaccessibility of arsenic in soils developed over Jurassic ironstones in eastern England. Environmental Geochemistry and Health, 27, 121–130.

    Article  CAS  Google Scholar 

  • Piearce, T. G., Langdon, C. J., Meharg, A. A., & Semple, K. T. (2002). Yellow earthworms: Distinctive pigmentation associated with arsenic- and copper-tolerance in Lumbricus rubellus. Soil Biology and Biochemistry, 34, 1833–1838.

    Article  CAS  Google Scholar 

  • Royal Society of Chemistry: A simple fitness-for-purpose control chart based on duplicate results obtained from routine test materials: Analytical Methods Committee Technical brief number 9. (2002). Retrieved on 22 February 2008 from http://www.rsc.org/images/brief9_tcm18-25951.pdf.

  • Sample, B. E., Suter Ii, G. W., Beauchamp, J. J., & Efroymson, R. A. (1999). Literature-derived bioaccumulation models for earthworms: Development and validation. Environmental Toxicology and Chemistry, 18, 2110–2120.

    Article  CAS  Google Scholar 

  • Schultz, A. C., & Biksey, T. M. (2003). Arsenic speciation and its effect on soil cleanup standards. Environmental Claims Journal, 15, 107–118.

    Article  Google Scholar 

  • Spurgeon, D. J., & Hopkin, S. P. (1996). The effects of metal contamination on earthworm populations around a smelting works: Quantifying species effects. Applied Soil Ecology, 4, 147–160.

    Article  Google Scholar 

  • Van Vliet, P. C. J., Didden, W. A. M., Van der Zee, S. E. A. T. M., & Peijnenburg, W. J. G. M. (2006). Accumulation of heavy metals by enchytraeids and earthworms in a floodplain. European Journal of Soil Biology, 42, S117–S126.

    Google Scholar 

  • Wragg, J., Cave, M., & Nathanail, P. (2007). A study of the relationship between arsenic bioaccessibility and its solid-phase distribution in soils from Wellingborough, UK. Journal of Environmental Science and Health—Part A Toxic/Hazardous Substances and Environmental Engineering, 42, 1303–1315.

    CAS  Google Scholar 

  • Worm Watch Canada: Key to reproductively mature earthworms. (2008). Retrieved on 22 February 2008 from http://www.naturewatch.ca/english/wormwatch/resources/key/taxonomic.html.

Download references

Acknowledgements

The authors wish to thank the British Geological Survey University Funding Initiative (BUFI) for funding this research as part of a PhD studentship. We are also grateful to Joanna Wragg of the British Geological Survey for reviewing the manuscript and the late Tim Brewer for his guidance early on in the studentship. We would also like to thank the Tavistock estate for granting permission to access the Devon Great Consols site.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael J. Watts.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Button, M., Watts, M.J., Cave, M.R. et al. Earthworms and in vitro physiologically-based extraction tests: complementary tools for a holistic approach towards understanding risk at arsenic-contaminated sites. Environ Geochem Health 31, 273–282 (2009). https://doi.org/10.1007/s10653-008-9208-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10653-008-9208-3

Keywords

Navigation