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Uptake and Elimination of Cadmium and Zinc by Eisenia andrei During Exposure to Low Concentrations in Artificial Soil

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Abstract

Bioaccumulation factors (BAFs) are often used in the risk assessment process to estimate trophic transfer of contaminants such as metals from soil. BAFs can be derived from laboratory studies through the determination of steady-state concentrations or kinetic estimation methods. In this study, bioaccumulation tests were performed with artificial soil spiked at low levels with cadmium or zinc to determine uptake and elimination kinetics of both metals by the compost worm Eisenia andrei. The metal-amended soils were acclimated for 21 days prior to the test, after which worms were individually incubated in the soils. The uptake phase comprised 0–21 days, after which the test organisms were transferred into clean soil and the elimination phase continued for an additional 21 days. Subsamples of soil and earthworms (whole body) were collected from independent replicates throughout the uptake phase and elimination phase and analyzed for total metal concentrations. Uptake of Cd in E. andrei increased linearly with time and did not reach steady state within the testing period. Cd uptake and excretion were described by a one-compartment first-order kinetics model. Zn concentrations rapidly increased in E. andrei after 1 day of exposure but subsequently decreased to background levels throughout the remainder of the uptake phase; internal Zn concentrations did not change from background levels during the elimination phase. Kinetic BAFs were calculated for Cd and Zn. Cd is a nonessential metal that is bioaccumulated at a relatively rapid rate, while Zn is an essential metal, and as such, it is regulated by E. andrei. Metal essentiality and concentration significantly impact bioaccumulation of metals by terrestrial invertebrates.

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References

  • Carpene E, Andreani G, Monari M, Castellani G, Isani G (2006) Distribution of Cd, Zn, Cu and Fe among selected tissues of the earthworm (Allolobophora caliginosa) and Eurasian woodcock (Scolopax rusticola). Sci Total Environ 363:126–135

    Article  CAS  Google Scholar 

  • Conder JM, Seals LD, Lanno RP (2002) Method for determining toxicologically relevant cadmium residues in the earthworm Eisenia fetida. Chemosphere 49:1–7

    Article  CAS  Google Scholar 

  • Cortet J, Gomot-De Vauflery A, Poinsot-Balaguer N, Gomot L, Texier C, Cluzeau D (1999) The use of invertebrate soil fauna in monitoring pollutant effects. Eur J Soil Biol 35:115–134

    Article  CAS  Google Scholar 

  • Demuynck S, Grumiaux F, Mottier V, Schikorski D, Lemière S, Leprêtre A (2007) Cd/Zn exposure interactions on metallothionein response in Eisenia fetida (Annelida, Oligochaeta). Comp Biochem Physiol C 145C:658–668

    CAS  Google Scholar 

  • Egeler P, Moser T, Scheffczyk A, Gilberg D (2009) Validation of a soil bioaccumulation test with terrestrial oligochaetes by an international ring test. Report to the Federal Environmental Agency (Umweltbundesamt Dessau). R&D No. 204 67 458

  • Hamers T, van den Berg JHJ, van Gestel CAM, van Schooten F-J, Murk AJ (2006) Risk assessment of metals and organic pollutants for herbivorous and carnivorous small mammal food chains in a polluted floodplain (Biesbosch, The Netherlands). Environ Pollut 144:581–595

    Article  CAS  Google Scholar 

  • Heikens A, Peijnenburg WJGM, Hendriks AJ (2001) Bioaccumulation of heavy metals in terrestrial invertebrates. Environ Pollut 113:385–393

    Article  CAS  Google Scholar 

  • Hendrickx F, Maelfait JP, Bogaert N, Tojal C, Du Laing G, Tack FMG, Verloo MG (2004) The importance of biological factors affecting trace metal concentration as revealed from accumulation patterns in co-occurring terrestrial invertebrates. Environ Pollut 127:335–341

    Article  CAS  Google Scholar 

  • Hobbelen PHF, Koolhaas JE, Van Gestel CAM (2006) Bioaccumulation of heavy metals in the earthworms Lumbricus rubellus and Aporrectodea caliginosa in relation to total and available metal concentrations in field soils. Environ Pollut 144:639–646

    Article  CAS  Google Scholar 

  • ISO (1994) Soil quality—determination of pH, No. 10390. International Organization for Standardization, Geneva

    Google Scholar 

  • Janssen RPT, Posthuma L, Baerselman R, DenHollander HA, vanVeen RPM, Peijnenburg JGM (1997) Equilibrium partitioning of heavy metals in Dutch field soils. 2. Prediction of metal accumulation in earthworms. Environ Toxicol Chem 16:2479–2488

    Article  CAS  Google Scholar 

  • Kizilkaya R (2005) The role of different organic wastes on zinc bioaccumulation by earthworm Lumbricus terrestris L. (Oligochaeta) in successive Zn added soil. Ecol Eng 25:322–331

    Article  Google Scholar 

  • Laskowski R (1991) Are the top carnivores endangered by heavy-metal biomagnification? Oikos 60:387–390

    Article  Google Scholar 

  • Laskowski R, Maryanski M (1993) Heavy-metals in epigeic fauna—trophic-level and physiological hypotheses. Bull Environ Contam Toxicol 50:232–240

    Article  CAS  Google Scholar 

  • Lock K, Janssen CR (2001) Zinc and cadmium body burdens in terrestrial oligochaetes: use and significance in environmental risk assessment. Environ Toxicol Chem 20:2067–2072

    Article  CAS  Google Scholar 

  • Lock K, Janssen CR (2003) Influence of ageing on zinc bioavailability in soils. Environ Pollut 126:371–374

    Article  CAS  Google Scholar 

  • Maenpaa KA, Kukkonen JVK, Lydy MJ (2002) Remediation of heavy metal-contaminated soils using phosphorus: evaluation of bioavailability using an earthworm bioassay. Arch Environ Contam Toxicol 43:389–398

    Article  CAS  Google Scholar 

  • Marino F, Morgan AJ (1999) The time-course of metal (Ca, Cd, Cu, Pb, Zn) accumulation from a contaminated soil by three populations of the earthworm, Lumbricus rubellus. Appl Soil Ecol 12:169–177

    Article  Google Scholar 

  • McGeer JC, Brix KV, Skeaff JM, DeForest DK, Brigham SI, Adams WJ, Green A (2003) Inverse relationship between bioconcentration factor and exposure concentration for metals: implication for hazard assessment of metals in the aquatic environment. Environ Toxicol Chem 22:1017–1037

    Article  CAS  Google Scholar 

  • Morgan JE, Morgan AJ (1988) Earthworms as biological monitors of cadmium, copper, lead and zinc in metalliferous soils. Environ Pollut 54:123–138

    Article  CAS  Google Scholar 

  • Moser T, Egeler P (2005) Minutes of the kick-off workshop on the ring test, Bioaccumulation: Soil Test Using Terrestrial Oligochaetes. Rüsselsheim, Germany, July 18–20, 2005. Federal Environmental Agency (Umweltbundesamt, UBA), Dessau-Rosslau

  • Nahmani J, Hodson ME, Black S (2007) A review of studies performed to assess metal uptake by earthworms. Environ Pollut 145:402–424

    Article  CAS  Google Scholar 

  • Neuhauser EF, Cukic ZV, Malecki MR, Loehr RC, Durkin PR (1995) Bioconcentration and biokinetics of heavy metals in the earthworm. Environ Pollut 89:293–301

    Article  CAS  Google Scholar 

  • Olchawa E, Bzowska M, Stuerzenbaum SR, Morgan AJ, Plytycz B (2006) Heavy metals affect the coelomocyte-bacteria balance in earthworms: environmental interactions between abiotic and biotic stressors. Environ Pollut 142:373–381

    Article  CAS  Google Scholar 

  • Panda R, Pati SS, Sahu SK (1999) Accumulation of zinc and its effects on the growth, reproduction and life cycle of Drawida willsi (Oligochaeta), a dominant earthworm in Indian crop fields. Biol Fertil Soils 29:419–423

    Article  CAS  Google Scholar 

  • Peijnenburg WJGM (2002) Bioavailability of metals to soil invertebrates. In: Allen HW (ed) Bioavailability of metals in terrestrial ecosystems: importance of partitioning for bioavailability to invertebrates, microbes, and plants. SETAC Press, Pensacola, FL, pp 89–112

    Google Scholar 

  • Peijnenburg WJ, Baerselman R, De Groot AC, Jager T, Posthuma L, van Veen RP (1999) Relating environmental availability to bioavailability: Soil-type-dependent metal accumulation in the Oligochaete Eisenia andrei. Ecotoxicol Environ Saf 44:294–310

    Article  CAS  Google Scholar 

  • Saxe JK, Impellitteri CA, Peijnenburg WJGM, Allen HE (2001) Novel model describing trace metal concentrations in the earthworm, Eisenia andrei. Environ Sci Technol 35:4522–4529

    Article  CAS  Google Scholar 

  • Scaps P, Grelle C, Descamps M (1997) Cadmium and lead accumulation in the earthworm Eisenia fetida (Savigny) and its impact on cholinesterase and metabolic pathway enzyme activity. Comp Biochem Physiol C 116C:233–238

    CAS  Google Scholar 

  • Sheppard SC, Evenden WG, Cornwell TC (1997) Depuration and uptake kinetics of I, Cs, Mn, Zn and Cd by the earthworm (Lumbricus terrestris) in radiotracer-spiked litter. Environ Toxicol Chem 16:2106–2112

    CAS  Google Scholar 

  • Spurgeon DJ, Hopkin SP (1995) Extrapolation of the laboratory-based OECD earthworm toxicity test to metal-contaminated field sites. Ecotoxicology 4:190–205

    Article  CAS  Google Scholar 

  • 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 Ecol 11:227–243

    Article  Google Scholar 

  • Spurgeon DJ, Lofts S, Hankard PK, Toal M, McLellan D, Fishwick S, Svendsen C (2006) Effect of pH on metal speciation and resulting metal uptake and toxicity for earthworms. Environ Toxicol Chem 25:788–796

    Article  CAS  Google Scholar 

  • Systat Software Inc. (2007) Systat 12 for Windows. Version No. 12.00.08

  • van Gestel CAM, Dirven-van Breemen EM, Baerselman R (1993) Accumulation and elimination of cadmium, chromium and zinc and effects on growth and reproduction in Eisenia andrei (Oligochaeta, Annelida). Sci Total Environ 134:585–597

    Article  Google Scholar 

  • Veltman K, Huijbregts MAJ, Vijver MG, Peijnenburg WJGM, Hobbelen PHF, Koolhaas JE, van Gestel CAM, van Vliet PCJ, Jan Hendriks A (2007a) Metal accumulation in the earthworm Lumbricus rubellus. Model predictions compared to field data. Environ Pollut 146:428–436

    Article  CAS  Google Scholar 

  • Veltman K, Huijbregts MAJ, Hamers T, Wijnhoven S, Hendriks AJ (2007b) Cadmium accumulation in herbivorous and carnivorous small mammals: Meta-analysis of field data and validation of the bioaccumulation model optimal modeling for ecotoxicological applications. Environ Toxicol Chem 26:1488–1496

    Article  CAS  Google Scholar 

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Acknowledgments

This study was performed in the frame of an international ring test sponsored by the Federal Environmental Agency (Umweltbundesamt, UBA, Dessau-Rosslau, Germany; RandD No. 204 67 458). The authors would like to thank the Federal Environmental Agency, Hélène Lalande (McGill University, Montreal, QC, Canada), Roman Kuperman (U.S. Army Edgewood Chemical Biological Center, Edgewood, MD, USA), Thomas Moser (ECT Oekotoxikologie GmbH, Floersheim, Germany), Jörg Römbke (ECT Oekotoxikologie GmbH), and the Stantec R&D Funding Program for support of this project.

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Authors and Affiliations

  1. University of Waterloo, 200 University Avenue West, Waterloo, ON, N2L 3G1, Canada

    Ben A. Smith

  2. ECT Oekotoxikologie GmbH, Boettgerstr. 2-14, 65439, Floersheim/Main, Germany

    Philipp Egeler & Daniel Gilberg

  3. Natural Resource Sciences, McGill University, 21111 Lakeshore Road, Ste. Anne de Bellevue, QC, H9X 3V9, Canada

    William Hendershot

  4. Stantec Consulting Ltd., Suite 1-70 Southgate Drive, Guelph, ON, N1G 4P5, Canada

    Gladys L. Stephenson

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  1. Ben A. Smith
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  2. Philipp Egeler
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Correspondence to Ben A. Smith.

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Smith, B.A., Egeler, P., Gilberg, D. et al. Uptake and Elimination of Cadmium and Zinc by Eisenia andrei During Exposure to Low Concentrations in Artificial Soil. Arch Environ Contam Toxicol 59, 264–273 (2010). https://doi.org/10.1007/s00244-009-9459-8

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