Assessment of the Ecological Status of Soils Contaminated by the Copper Mining Industry in Chile: Earthworms to the Rescue

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Abstract

Soil fauna can serve as an excellent tool for ecological assessment of soil quality. The earthworm Eisenia fetida L. is widely used as a bioindicator organism to assess the toxicity of metals, metalloids, and other pollutants. Many studies have shown that the concentrations of metals and metalloids toxic to earthworms are an order of magnitude lower in artificially contaminated soils than in industrially contaminated soils. The novelty of this study is that toxicity estimates were made using native industrially contaminated soils. The results of the two experiments demonstrate the potential use of earthworms for ecological assessment of soils contaminated with metals and metalloids due to copper mining activities in central Chile. The main contaminant in these soils was copper, but arsenic, commonly found in copper ore, was also present in the contaminated soils. In the short-term bioassay, E. fetida earthworms avoided the soil in response to increasing copper content. However, in long-term experiments, arsenic proved to be more toxic to earthworm reproduction, while copper had little effect. In this study, we present toxicity thresholds for copper and arsenic to E. fetida in industrially contaminated native soils.

About the authors

A. Neaman

Departamento de Recursos Ambientales, Facultad de Ciencias Agronómicas, Universidad de Tarapacá

Author for correspondence.
Email: alexander.neaman@gmail.com
Chile, 1000000, Arica

C. Yáñez

Instituto de Biología, Pontificia Universidad Católica de Valparaíso

Email: alexander.neaman@gmail.com
Chile, 2340000, Valparaíso

References

  1. Adriano D.C. Trace Elements in Terrestrial Environments: Biogeochemistry, Bioavailability, and Risk of Metals New York, N.Y.: Springer-Verlag, 2001.
  2. Arnold R.E., Hodson M.E. Effect of time and mode of depuration on tissue copper concentrations of the earthworms Eisenia andrei, Lumbricus rubellus and Lumbricus terrestris // Environmental Pollution. 2007. V. 148. P. 21–30. https://doi.org/10.1016/j.envpol.2006.11.003
  3. Arnold R.E., Hodson M.E., Black S., Davies N.A. The influence of mineral solubility and soil solution concentration on the toxicity of copper to Eisenia fetida Savigny // Pedobiologia. 2003. V. 47. P. 622–632. https://doi.org/10.1016/s0031-4056(04)70246-2
  4. Ávila G., Gaete H., Morales M., Neaman A. Reproducción de Eisenia fetida en suelos agrícolas de áreas mineras contaminadas por cobre y arsénico. // Pesqui Agropecu Bras. 2007. V. 42. P. 435–441. https://doi.org/10.1590/S0100-204X2007000300018
  5. Bustos V., Mondaca P., Sauvé S., Gaete H., Celis-Diez J.L., Neaman A. Thresholds of arsenic toxicity to Eisenia fetida in field-collected agricultural soils exposed to copper mining activities in Chile // Ecotoxicology and Environmental Safety 2015. V. 122. P. 448–454. https://doi.org/10.1016/j.ecoenv.2015.09.009
  6. Delgadillo V., Verdejo J., Mondaca P., Verdugo G., Gaete H., Hodson M.E., Neaman A. Proposed modification to avoidance test with Eisenia fetida to assess metal toxicity in agricultural soils affected by mining activities // Ecotoxicology and Environmental Safety. 2017. V. 140. P. 230–234. https://doi.org/10.1016/j.ecoenv.2017.02.038
  7. Duffus J.H. “Heavy metals” a meaningless term? (IUPAC Technical Report) // Pure and Applied Chemistry. 2002. V. 74. P. 793–807. https://doi.org/10.1351/pac200274050793
  8. Fuentes-Arderiu X. Concentration and content // Biochemia Medica. 2013. V. 23. P. 141–142. https://doi.org/10.11613/bm.2013.017
  9. Holmstrup M., Hornum H.D. Earthworm colonisation of abandoned arable soil polluted by copper // Pedobiologia. 2012. V. 55. P. 63–65. https://doi.org/10.1016/j.pedobi.2011.08.005
  10. ISO 11268-2. Soil quality – Effects of pollutants on earthworms. Part 2: Determination of effects on reproduction of Eisenia fetida/Eisenia andrei Genève, Switzerland: International Organization for Standardization, 2012. 21 p.
  11. ISO-17512-1. Soil quality – Avoidance test for determining the quality of soils and effects of chemicals on behaviour. Part 1: Test with earthworms (Eisenia fetida and Eisenia andrei); Geneva, Switzerland, 2008.
  12. IUSS Working Group WRB. World Reference Base for Soil Resources 2014, update 2015. International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports No. 106 Rome: Food and Agricultural Organization, 2015. 192 p.
  13. Janssen R.P.T., Posthuma L., Baerselman R., DenHollander H.A., vanVeen R.P.M., Peijnenburg J.G.M. Equilibrium partitioning of heavy metals in Dutch field soils. II. Prediction of metal accumulation in earthworms // Environmental Toxicology and Chemistry. 1997. V. 16. P. 2479–2488. https://doi.org/10.1002/etc.5620161207
  14. Konečný L., Ettler V., Kristiansen S., Barros Amorim M.J., Kříbek B., Mihaljevič M., Šebek O., Nyambe I., Scott-Fordsmand J. Response of Enchytraeus crypticus worms to high metal levels in tropical soils polluted by copper smelting // J. Geochemical Exploration. 2014. V. 144. P. 427–432. https://doi.org/10.1016/j.gexplo.2013.10.004
  15. Kutner M., Nachtsheim C., Neter J. Applied Linear Regression Models Boston: McGraw-Hill Education, 2004. 701 p.
  16. Kuznetsova A.I., Lukina N.V., Tikhonova E.V., Gornov A.V., Gornova M.V., Smirnov V.E., Geraskina A.P., Shevchenko N.E., Tebenkova D.N., Chumachenko S.I. Carbon Stock in Sandy and Loamy Soils of Coniferous-Broadleaved Forests at Different Succession Stages // Eurasian Soil Sci. 2019. V. 52. P. 756–768. https://doi.org/10.1134/s1064229319070081
  17. Langdon C.J., Hodson M.E., Arnold R.E., Black S. Survival, Pb-uptake and behaviour of three species of earthworm in Pb treated soils determined using an OECD-style toxicity test and a soil avoidance test // Environmental Pollution. 2005. V. 138. P. 368–375. https://doi.org/10.1016/j.envpol.2005.03.002
  18. Laskowski R., Kramarz P., Jepson P. Selection of species for soil ecotoxicity testing. // Handbook of Soil Invertebrate Toxicity Tests. John Wiley & Sons: Chichester, England, 1998. P. 21–40.
  19. Lee B.-T., Kim K.-W. Toxicokinetics and biotransformation of As(III) and As(V) in Eisenia fetida // Hum. Ecol. Risk Assess. 2013. V. 19. P. 792–806. https://doi.org/10.1080/10807039.2012.708285
  20. Lee B.T., Kim K.W. Lysosomal membrane response of earthworm, Eisenia fetida, to arsenic contamination in soils // Environmental Toxicology. 2009. V. 24. P. 369–376. https://doi.org/10.1002/tox.20441
  21. Lock K., Janssen C.R. Toxicity of arsenate to the compostworm Eisenia fetida, the potworm Enchytraeus albidus and the springtail Folsomia candida // Bull. of Environmental Contamination and Toxicology 2002. V. 68. P. 760–765. https://doi.org/10.1007/s001280320
  22. Maraldo K., Christensen B., Strandberg B., Holmstrup M. Effects of copper on enchytraeids in the field under differing soil moisture regimes // Environmental Toxicology and Chemistry. 2006. V. 25. P. 604–612. https://doi.org/10.1897/05-076R.1
  23. Maxwell J.A. Rock and Mineral Analysis. N.Y.: Interscience Publishers, 1968. 584 p.
  24. McBride M.B., Cai M.F. Copper and zinc aging in soils for a decade: changes in metal extractability and phytotoxicity // Environmental Chemistry. 2016. V. 13. P. 160–167. https://doi.org/10.1071/en15057
  25. Mirmonsef H., Hornum H.D., Jensen J., Holmstrup M. Effects of an aged copper contamination on distribution of earthworms, reproduction and cocoon hatchability // Ecotoxicology and Environmental Safety. 2017. V. 135. P. 267–275. https://doi.org/10.1016/j.ecoenv.2016.10.012
  26. Nadporozhskaya M.A., Bykhovets S.S., Abakumov E.V. Application of the ROMUL Mathematical Model for Estimation of CO2 Emission and Dynamics of Organic Matter in the Subantarctic Lithozems // Eurasian Soil Sci. 2022. V. 55. P. 413–424. https://doi.org/10.1134/s1064229322040123
  27. Nahmani J., Hodson M.E., Black S. Effects of metals on life cycle parameters of the earthworm Eisenia fetida exposed to field-contaminated, metal-polluted soils // Environmental Pollution. 2007. V. 149. P. 44–58. https://doi.org/10.1016/j.envpol.2006.12.018
  28. Nahmani J., Hodson M.E., Black S. A review of studies performed to assess metal uptake by earthworms // Environmental Pollution. 2007. V. 145. P. 402–424. https://doi.org/10.1016/j.envpol.2006.04.009
  29. Neaman A., Valenzuela P., Tapia-Gatica J., Selles I., Novoselov A.A., Dovletyarova E.A., Yanez C., Krutyakov Y.A., Stuckey J.W. Chilean regulations on metal-polluted soils: The need to advance from adapting foreign laws towards developing sovereign legislation // Environmental Research. 2020. V. 185. P. 109429. https://doi.org/10.1016/j.envres.2020.109429
  30. O’Neill P. Arsenic // Heavy Metals in Soils. 2nd ed.; Blackie Academic & Professional: London, UK, 1995. P. 105–121.
  31. OECD-222. Guidelines for the testing of chemicals. Earthworm Reproduction Test (Eisenia fetida/Eisenia andrei); 2074-5761; Organisation for Economic Cooperation and Development: 2016.
  32. Pezzotti D., Peli M., Sanzeni A., Barontini S. Seasonality of Earthworm Macropores in a Temperate Alpine Area // Eurasian Soil Sci. 2021. V. 54. P. 1935–1944. https://doi.org/10.1134/S1064229321130032
  33. Pukalchik M.A., Terekhova V.A., Karpukhin M.M., Vavilova V.M. Comparison of Eluate and Direct Soil Bioassay Methods of Soil Assessment in the Case of Contamination with Heavy Metals // Eurasian Soil Sci. 2019. V. 52. P. 464–470. https://doi.org/10.1134/s1064229319040112
  34. Rachou J., Gagnon C., Sauvé S. Use of an ion-selective electrode for free copper measurements in low salinity and low ionic strength matrices // Environmental Chemistry. 2007. V. 4. P. 90–97. https://doi.org/10.1071/EN06036
  35. Sadzawka A., Carrasco M.A., Demanet R., Flores H., Mora M.L., Neaman A., Hernández P., Sandoval M. Métodos de análisis de lodos y de suelos. Chillán: Sociedad Chilena de la Ciencia del Suelo. Universidad de Concepción, 2015. 114 p.
  36. Sadzawka A., Carrasco M.A., Grez R., Mora M.L., Flores H., Neaman A. Métodos de análisis recomendados para los suelos de Chile. Serie actas INIA № 34 Santiago, Chile: Instituto de Investigaciones Agropecuarias, 2006. 164 p.
  37. Santa-Cruz J., Peñaloza P., Korneykova M.V., Neaman A. Thresholds of metal and metalloid toxicity in field-collected anthropogenically contaminated soils: A review // Geography, Environment, Sustainability. 2021. V. 14. P. 6–21. https://doi.org/10.24057/2071-9388-2021-023
  38. Santa-Cruz J., Vasenev I.I., Gaete H., Peñaloza P., Krutyakov Y.A., Neaman A. Metal ecotoxicity studies with spiked versus field-contaminated soils: Literature review, methodological shortcomings and research priorities // Russian J. Ecology. 2021. V. 52. P. 478–484. https://doi.org/10.1134/S1067413621060126
  39. Scott-Fordsmand J.J., Weeks J.M., Hopkin S.P. Importance of contamination history for understanding toxicity of copper to earthworm Eisenia fetida (Oligochaeta: Annelida), using neutral-red retention assay // Environmental Toxicology and Chemistry. 2000. V. 19. P. 1774–1780. https://doi.org/10.1002/etc.5620190710
  40. Sheldrick B.H., Wang C. Particle size distribution // Soil Sampling and Methods of Analysis. Canadian Society of Soil Science, Lewis Publishers: Boca Raton, FL, USA, 1993. P. 499–511.
  41. Spurgeon D.J., Hopkin S.P. Comparisons of metal accumulation and excretion kinetics in earthworms (Eisenia fetida) exposed to contaminated field and laboratory soils // Appl Soil Ecol. 1999. V. 11. P. 227–243. https://doi.org/10.1016/S0929-1393(98)00150-4
  42. Spurgeon D.J., Weeks J.M. Evaluation of factors influencing results from laboratory toxicity tests with earthworms // Advances in earthworm ecotoxicology. SETAC Technical Publications Series: Pensacola, FL, USA, 1998. P. 15–25.
  43. Stuckey J.W., Neaman A., Ravella R., Komarneni S., Martínez C.E. Highly charged swelling mica reduces free and extractable Cu levels in Cu-contaminated soils // Environmental Science & Technology. 2008. V. 42. P. 9197–9202. https://doi.org/10.1021/es801799s
  44. Tapia-Gatica J., González-Miranda I., Salgado E., Bravo M.A., Tessini C., Dovletyarova E.A., Paltseva A.A., Neaman A. Advanced determination of the spatial gradient of human health risk and ecological risk from exposure to As, Cu, Pb, and Zn in soils near the Ventanas Industrial Complex (Puchuncaví, Chile) // Environmental Pollution. 2020. V. 258. P. 113488. https://doi.org/10.1016/j.envpol.2019.113488
  45. Tapia-Gatica J., Selles I., Bravo M.A., Tessini C., Barros-Parada W., Novoselov A., Neaman A. Global issues in setting legal limits on soil metal contamination: A case study of Chile // Chemosphere. 2022. V. 290. P. 133404. https://doi.org/10.1016/j.chemosphere.2021.133404
  46. US EPA. Toxicity Relationship Analysis Program (TRAP) version 1.3 United States Environmental Protection Agency, Mid-Continent Ecology Division, 2016.
  47. Van Zwieten L., Rust J., Kingston T., Merrington G., Morris S. Influence of copper fungicide residues on occurrence of earthworms in avocado orchard soils // Science of the Total Environment. 2004. V. 329. P. 29–41. https://doi.org/10.1016/j.scitotenv.2004.02.014
  48. Vargas C., Quiroz W., Bravo M., Neaman A. Stability of arsenic during soil treatment and storage // J. the Chilean Chemical Society. 2015. V. 60. P. 2868–2871. https://doi.org/10.4067/S0717-97072015000300015

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