Skip to main content
Log in

Lethal critical body residues as measures of Cd, Pb, and Zn bioavailability and toxicity in the earthwormEisenia fetida

  • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

An Erratum to this article was published on 01 May 2003

Abstract

Background. Earthworm heavy metal concentrations (critical body residues, CBRs) may be the most relevant measures of heavy metal bioavailability in soils and may be linkable to toxic effects in order to better assess soil ecotoxicity. However, as earthworms possess physiological mechanisms to secrete and/or sequester absorbed metals as toxicologically inactive forms, total earthworm metal concentrations may not relate well with toxicity.

Objective

The objectives of this research were to: i) develop LD50s (total earthworm metal concentration associated with 50% mortality) for Cd, Pb, and Zn; ii) evaluate the LD50 for Zn in a lethal Zn-smelter soil; iii) evaluate the lethal mixture toxicity of Cd, Pb, and Zn using earthworm metal concentrations and the toxic unit (TU) approach; and iv) evaluate total and fractionated earthworm concentrations as indicators of sublethal exposure.

Methods

Earthworms (Eisenia fetida (Savigny)) were exposed to artificial soils spiked with Cd, Pb, Zn, and a Cd-Pb-Zn equitoxic mixture to estimate lethal CBRs and mixture toxicity. To evaluate the CBR developed for Zn, earthworms were also exposed to Zn-contaminated field soils receiving three different remediation treatments. Earthworm metal concentrations were measured using a procedure devised to isolate toxicologically active metal burdens via separation into cytosolic and pellet fractions.

Results and Discussion

Lethal CBRs inducing 50% mortality (LD50, 95% CI) were calculated to be 5.72 (3.54-7.31), 3.33 (2.97-3.69), and 8.19 (4.78-11.6) mmol/kg for Cd, Pb, and Zn, respectively. Zn concentrations of dead earthworms exposed to a lethal remediated Zn-smelter soil were 3-fold above the LD50 for Zn and comparable to earthworm concentrations in lethal Zn-spiked artificial soils, despite a 14-fold difference in total soil Zn concentration between lethal field and artificial soils. An evaluation of the acute mixture toxicity of Cd, Pb, and Zn in artificial soils using the Toxic Unit (TU) approach revealed an LD50 (95% CI) of 0.99 (0.57-1.41) TU, indicating additive toxicity.

Conclusions

Total Cd, Pb, and Zn concentrations in earthworms were good indicators of lethal metal exposure, and enabled the calculation at LD50s for lethality. The Zn-LD50 developed in artificial soil was applicable to earthworms exposed to remediated Zn-smelter soil, despite a 14-fold difference in total soil Zn concentrations. Mixture toxicity evaluated using LD50s from each single metal test indicated additive mixture toxicity among Cd, Pb, and Zn. Fractionation of earth worm tissues into cytosolic and pellet digests yielded mixed results for detecting differences in exposure at the sublethal level

Recommendation and Outlook

CBRs are useful in describing acute Cd, Pb, and Zn toxicity in earthworms, but linking sublethal exposure to total and/or fractionated residues may be more difficult. More research on detoxification, regulation, and tissue and subcellular partitioning of heavy metals in earthworms and other invertebrates is needed to establish the link between body residue and sublethal exposure and toxicity. Keywords: Bioavailability; Cd; critical body residues; earthworms; metals; Pb; soil; Zn

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.

Institutional subscriptions

Similar content being viewed by others

References

  1. Lanno RP, McCarty LS (1997): Earthworm bioassays: adopting techniques from aquatic toxicity testing. Soil Bio Biochem29, 693–697

    Article  CAS  Google Scholar 

  2. Lanno RP, Conder JM, Seals L (1999): Critical limits for heavy metals in soils and surface waters. In: Gregor H, Mohaupt-Jahr B, Hönerbach F, Eds, Workshop on Effects-based Approaches for Heavy Metals. Federal Environmental Agency (Umweltbundesamt), Berlin, Germany. pp 49–55

    Google Scholar 

  3. Morgan AJ, Morgan JE, Turner M, Winters C, Yarwood A (1993): Metal relationships of earthworms. In: Dallinger R, Rainbow PS, Eds, Ecotoxicology of Metals in Invertebrates. Lewis Publishers, Boca Raton, FL, USA. pp 333–358

    Google Scholar 

  4. van Gestel CAM, Posthuma L, Smit CE, Notenboom J, Eijsackers HJP (1998): General Discussion. In: Posthuma L, van Gestel CAM, Smit CE, Bakker DJ, Vonk FW, Eds, Validation of toxicity data and risk limits for soils: final report. National Institute of Public Health and the Environment (RIVM), Bilthoven, the Netherlands. pp 163–198

    Google Scholar 

  5. Peijnenburg WJGM, Posthuma L, Eijsackers HJP, Allen HE (1997): A conceptual framework for implementation of bio-availability of metals for environmental management purposes. Ecotox Environ Safety37, 163–172

    Article  CAS  Google Scholar 

  6. McCarty LS (1991): Toxicant body residues: Implications for aquatic bioassays with some organic chemicals. In: Mayes MA, Barron MG, Eds, Aquatic Toxicology and Risk Assessment: Fourteenth Volume, ASTM STP 1124. American Society for Testing and Materials, Philadelphia, PA, USA. pp 183–192

    Google Scholar 

  7. Lanno RP, Le Blanc SC, Knight BL, Tymowski R, Fitzgerald DG (1998): Application of body residues as a tool in the assessment of soil toxicity. In: Sheppard SC, Bembridge JD, Holmstrup M, Posthuma L, Eds, Advances in Earthworm Ecotoxicology. Society of Environmental Toxicology and Chemistry, Pensacola, FL, USA. pp 41–53

    Google Scholar 

  8. Marinussen MPJC, van der Zee SEATM, de Haan FAM (1997): Effect of Cd or Pb addition to Cu-contaminated soil on tissue Cu accumulation in the earthworm,Dendrobaena veneta. Ecotox Environ Safety38, 309–315

    Article  CAS  Google Scholar 

  9. Peijnenburg WJGM, Posthuma L, Zweers PGPC, Baerselman R, de Groot AC, van Veen RPM, Jager T (1999): Prediction of metal bioavailability in Dutch field soils for the OligochaeteEnchytraeus crypticus. Ecotox Environ Safety43B, 170–186

    Article  Google Scholar 

  10. Spurgeon DJ, Hopkin SP (1996): Effects of variations of the organic matter content and pH of soils on the availability and toxicity of zinc to the earthwormEisenia fetida. Pedobio-logia40, 80–96

    CAS  Google Scholar 

  11. van Gestel CAM, Dirven-van Breeman EM, Baerselman R (1993): Accumulation and elimination of cadmium, chromium and zinc and the effects on growth and reproduction ofEisenia andrei (Oligochaeta, Annelida). Sci Total Environ 1993 Supplement, 585-59

  12. Dallinger R (1993): Strategies of metal detoxification in terrestrial invertebrates. In: Dallinger R, Rainbow PS, Eds, Ecotoxicology of Metals in Invertebrates, Lewis Publishers, Boca Raton, FL, USA. pp 245–289

    Google Scholar 

  13. Melancon M J, Alscher R, Benson W, Kruzynski G, Lee RF, Sikka HC, Spies RB (1992): Metabolic products as biomarkers. In: Huggett RJ, Kimerle RA, Mehrle PM Jr, Bergman HL, Eds, Biomarkers: Biochemical, Physiological, and Histological Markers of Anthropogenic Stress. Society of Environmental Toxicology and Chemistry, Boca Raton, FL, USA. pp 87–123

    Google Scholar 

  14. Reinecke SA, Prinsloo MW, Reinecke AJ (1999): Resistance ofEisenia fetida (Oligochaeta) to cadmium after long-term exposure. Ecotox Environ Safety42B, 75–80

    Article  Google Scholar 

  15. Spurgeon DJ, Hopkin SP (1999): Comparisons of metal accumulation and excretion kinetics in earthworms(Eisenia fetida) exposed to contaminated field and laboratory soils. Appl Soil Ecol11, 227–243

    Article  Google Scholar 

  16. Morgan AJ, Morris B (1982): The accumulation and intrac-ellular compartmentation of cadmium, lead, zinc and calcium in two earthworm species(Dendrobaena rubida andLumbricus rubellus) living in highly contaminated soil. Histochemistry75, 269–285

    Article  CAS  Google Scholar 

  17. Morgan JE, Norey CG, Morgan AJ, Kay J (1989): A comparison of the cadmium-binding proteins isolated from the posterior alimentary canal of the earthwormsDendrodrilus rubidus andLumbricus rubellus. Comp Biochem Physiol92C, 15–21

    CAS  Google Scholar 

  18. Morgan JE, Morgan AJ (1989): Zinc sequestration by earthworm (Annelida: Oligochaeta) chloragocytes. Histochemistry90, 405–411

    Article  CAS  Google Scholar 

  19. Ireland MP (1975): Distribution of lead, zinc and calcium inDendrobaena rubida (Oligochaeta) living in soil contaminated by base metal mining in Wales. Comp Biochem Physiol52B, 551–555

    Google Scholar 

  20. Ireland MP, Richards KS (1977): The occurrence and localization of heavy metals and glycogen in the earthwormsLumbricus rubellus andDendrobaena rubida from a heavy metal site. Histochemistry51, 153–166

    Article  CAS  Google Scholar 

  21. Morgan JE (1985): The interactions of exogenous and endogenous factors on the uptake of heavy metals by the earthwormLurnbricus rubellus. International Conference on Heavy Metals in the Environment, pp 736-739

  22. Morgan JE, Morgan AJ (1989): The effect of lead incorporation on the elemental composition of earthworm (Annelida, Oligochaeta) chloragosome granules. Histochemistry92, 237–241

    Article  CAS  Google Scholar 

  23. Conder JM, Seals LD, Lanno RP (2002): Method for determining toxicologically relevant cadmium residues in the earthwormEisenia fetida. Chemosphere47, 1–7

    Article  Google Scholar 

  24. Honeycutt ME, Roberts BL, Roane DS (1995): Cadmium disposition in the earthwormEisenia fetida. Ecotox Environ Safety30, 143–150

    Article  CAS  Google Scholar 

  25. Jenkins KD, Mason AZ (1988): Relationships between sub-cellular distributions of cadmium and perturbations in reproduction in the polychaeteNeanthes arenaceodentata. Aqnat Toxicol12, 229–244

    Article  CAS  Google Scholar 

  26. Sprague JB (1970): Measurement of pollutant toxicity to fish. II. Utilizing and applying bioassay results. Wat Res4, 3–32

    Article  CAS  Google Scholar 

  27. Conder JM, Lanno RP (2000): Evaluation of surrogate measures of cadmium, lead, and zinc bioavailability toEisenia fetida. Chemosphere41, 1659–1668

    Article  CAS  Google Scholar 

  28. Conder JM, Lanno RP, Basra NT (2001): Assessment of metal availability in smelter soil using earthworms and chemical extractions. J Environ Qua130, 1231–1237

    CAS  Google Scholar 

  29. Basra NT, Gradwohl R, Snethen KL, Schroder JL (2001): Chemical immobilization of Pb, Zn, and Cd in smelter-contaminated soils using biosolids and rock phosphate. J Environ Qua130, 1222–1230

    Google Scholar 

  30. Hamilton MA, Russo RC, Thurston RV (1977): Trimmed Spear-man-Karber method for estimating median lethal concentrations in toxicity bioassays. Env Sci Technol11, 714–719

    Article  CAS  Google Scholar 

  31. Posthuma L, Baerselman R (1998): Field relevance of theEisenia andrei reproduction soil toxicity test. In Posthuma L, van Gestel CAM, Smit CE, Bakker DJ, Vonk JW Eds, Validation of toxicity data and risk limits for soils: final report. National Institute of Public Health and the Environment (RIVM), Bilthoven, the Netherlands. pp 95–110

    Google Scholar 

  32. Spurgeon DJ, Hopkin SP (1999): Tolerance to zinc in populations of the earthwormLumbricus rubellus from un-contaminated and metal-contaminated ecosystems. Arch Environ Contam Toxicol37, 332–337

    Article  CAS  Google Scholar 

  33. Marinussen MPJC, van der Zee SEATM, de Haan FAM, Bouwman LM, Hefting MM (1997): Heavy metal (copper, lead, and zinc) accumulation and excretion by the earthworm,Dendrobaena veneta. J Environ Qua126, 278–284

    CAS  Google Scholar 

  34. Weltje L (1998): Mixture toxicity and tissue interactions of Cd, Cu, Pb and Zn in earthworms (Oligochaeta) in laboratory and field soils: A critical evaluation of data. Chemosphere36, 2643–2660

    Article  CAS  Google Scholar 

  35. Janssen RPT, Posthuma L, Baerselman R, den Hollander HA, van Veen RPM, Peijnenburg WJGM (1997): Equilibrium partitioning of heavy metals in Dutch field soils. II. Prediction of metal accumulation in earthworms. Environ Toxicol Chem16, 2479–2488

    Article  CAS  Google Scholar 

  36. Neuhauser EF, Cukic ZV, Malecki MR, Loehr RC, Durkin PR (1995): Bioconcentration and biokinetics of heavy metals in the earthworm. Environ Pollut89, 293–301

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Jason M. Conder or Roman P. Lanno.

Additional information

An erratum to this article is available at http://dx.doi.org/10.1007/BF03038813.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Conder, J.M., Lanno, R.P. Lethal critical body residues as measures of Cd, Pb, and Zn bioavailability and toxicity in the earthwormEisenia fetida . J Soils & Sediments 3, 13–20 (2003). https://doi.org/10.1007/BF02989463

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02989463

Keywords

Navigation