The Determination of Earthworm Species Sensitivity Differences to Lead Using the Lipid Peroxidation and Total Antioxidant Capacity Levels

Document Type : Animal environment

Authors

1 Department of Environment, Natural Resource and Environment Faculty, Malayer University, Malayer, Iran

2 Department of Molecular and Cell Biology, Faculty of Basic Sciences, University of Mazandaran, Babolsar, Mazandaran

Abstract

Earthworms widely used as biological indicators by many researchers to evaluate the risk of environmental pollutants. On the other hand, the existence of earthworm species in a region, as well as its sensitivity to a specific pollutant is different. The purpose of the study is to investigate the effects of lead on the morphology, biomass, lipid peroxidation and total antioxidant capacity as biomarkers in Aporrectodea rosea, Aporrectodea caliginosa, Dendrobaena hortensis and Eisenia fetida earthworm species in order to determine more Inherent sensitive species to lead. In this study, acute toxicity test carry out according to: organization for economic co-operation and development (OECD) guideline number 207. TAC and LPo levels were assayed by ferric reducing antioxidant power and thiobarbituric acid methods, respectively. The severity of morphological and physiological symptoms such as elongation of the body, body constriction and segmental bulging, cuticle rupture, vesicle seminal constriction, were A. rosea> A. caliginosa > D. hortensis> E. fetida, respectively. Also the species of A. rosea exposed to different concentrations of lead has was more sensitive in stand of biomass loss, MDA and TAC levels. Therefor it seems A. rosea earthworm can be used as suitable biomarkers against to soil lead pollution.

Keywords


  1. Barata, C.; Varo, I.; Navarro, J.C.; Arun, S. and Porte, C., 2005. Antioxidant enzyme activities and lipid peroxidation in the freshwater cladoceran Daphnia magna exposed to redox cycling compounds. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. Vol. 140, No. 2, pp: 175-186.
  2. Bartsch, H. and Nair, J., 2000. Ultrasensitive and specific detection methods for exocylic DNA adducts: markers for lipid peroxidation and oxidative stress. Toxicology. Vol. 153, No. 1, pp: 105-114.
  3. Benzie, I.F. and Strain, J.J., 1996. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Analytical biochemistry. Vol. 239, No. 1, pp: 70-76.
  4. Bierkens, J.; Klein, G.; Corbisier, P.; Van Den Heuvel, R.; Verschaeve, L.; Weltens, R. and Schoeters, G., 1998. Comparative sensitivity of 20 bioassays for soil quality. Chemosphere. Vol. 37, No. 14, pp: 2935-2947.
  5. Bouché, M.B., 1992. Earthworm species and ecotoxicological studies. In: Greig- Smith, P.W., Becker, H., Edwards, P.J., Heimbach, F. (Eds.), Ecotoxicology of Earthworms. Intercept Press, Andover. pp. 20-35.
  6. Chen, C.; Zhou, Q.; Liu, S.and Xiu, Z., 2011. Acute toxicity, biochemical and gene expression responses of the earthworm Eisenia fetida exposed to polycyclic musks. Chemosphere. Vol. 83, No. 8, pp: 1147-1154.
  7. Csuzdi, C. and Zicsi, A., 2003. Earthworms of Hungary: Annelida: Oligochaeta, Lumbricidae. Hungarian Natural History Museum. 272 p.
  8. Domínguez-Crespo, M.A.; Sánchez-Hernández, Z.E.; Torres-Huerta, A.M.; Negrete, M.D.L.L.X.; Conde Barajas, E. and Flores-Vela, A., 2012. Effect of the heavy metals Cu, Ni, Cd and Zn on the growth and reproduction of epigeic earthworms (E. fetida) during the vermistabilization of municipal sewage sludge. Water, Air & Soil Pollution. Vol. 223, No. 2, pp: 915-931.
  9. Edwards, C.A. and Coulson, J.M., 1992. Choice of earthworm species for laboratory tests. p 36-43. In: Greig-Smith PW, Becker H, Edwards PJ, Heimbach F (eds). Ecotoxicology of Earthworms. Intercept Ltd, Andover, UK.
  10. Fitzgerald, D.G.; Warner, K.A.; Lanno, R.P. and Dixon, D.G., 1996. Assessing the effects of modifying factors on pentachlorophenol toxicity to earthworms: applications of body residues. Environmental toxicology and chemistry. Vol. 15, No.12, pp: 2299-2304.
  11. Fourie, F.; Reinecke, S.A. and Reinecke, A.J., 2007. The determination of earthworm species sensitivity differences to cadmium genotoxicity using the comet assay. Ecotoxicology and Environmental Safety. Vol. 67, No. 3, pp: 361-368.
  12. Gopal, V.; Clement, T. and Nagarajan, K., 1998. Potential of Megascolex pumilio in biomonitoring environmental pollution. Indian Journal of Environmental Health. Vol. 28, No. 3, pp: 194-199.
  13. Gupta, S.K. and Sundararaman, V., 1990. Biological response of earthworm Pheretima posthuma to inorganic cadmium. Indian journal of experimental biology. New Delhi. Vol. 28, No. 1, pp: 71-73.
  14. ISO, 17512-1. 2008. 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: International Organiza tion for Standardization.
  15. Kalaiselvan, K.; Prince, S.P.M. and Subburam, W.V., 1996. Toxicity of lead to the earthworm Drawida ramnadana (Michaelsen). Pollution Research. Vol. 15, pp:15-18.
  16. Kula, H., 1995. Comparison of laboratory and field testing for the assessment of pesticide side effects on earthworms. Acta Zoologica Fennica. Vol.  196, pp: 338-341.
  17. Lin, D.; Zhou, Q.; Xie, X. and Liu, Y., 2010. Potential biochemical and genetic toxicity of triclosan as an emerging pollutant on earthworms (Eisenia fetida). Chemosphere. Vol. 81, No. 10, pp:1328-1333.
  18. Liu, J.; Xiong, K.; Ye, X.; Zhang, J.; Yang, Y. and Ji, L., 2015. Toxicity and bioaccumulation of bromadiolone to earthworm Eisenia fetida. Chemosphere. Vol. 135, pp: 250-256.
  19. Lowe, C.N. and Butt, K.R., 2005. Culture techniques for soil dwelling earthworms: a review. Pedobiologia. Vol. 49, No. 5, pp: 401-413.
  20. Miyazaki, A.; Amano, T.; Saito, H. and Nakano, Y., 2002.Acute toxicity of chlorophenols to earthworms using a simple paper contact method and comparison with toxicities to fresh water organisms. Chemosphere. Vol. 47, pp: 65-69.
  21. Morgan, J.E.; Norey, C.G.; Morgan, A.J. and Kay, J., 1989. A comparison of the cadmium-binding proteins isolated from the posterior alimentary canal of the earthworms Dendrodrilus rubidus and Lumbricus rubellus. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology. Vol. 92, No. 1, pp: 15-21.
  22. Nordberg, J. and Arner, E.S., 2001. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free radical biology and medicine. Vol. 31, No. 11, pp: 1287-1312.
  23. Nursita, A.I.; Singh, B. and Lees, E., 2005. The effects of cadmium, copper, lead, and zinc on the growth and reproduction of Proisotoma minuta Tullberg (Collembola). Ecotoxicology and environmental safety. Vol. 60, No. 3, 
    pp: 306-314.
  24. OECD. 1984. Earthworm, Acute Toxicity Tests. OECD Guidelines for the Testing of Chemicals. Vol. 1, pp: 1-9.
  25. OECD. 2004. Earthworm Reproduction Test (Eisenia fetida/andrei). OECD Guideline for Testing Chemicals. 
    Vol. 1, pp: 1-18.
  26. Ohkawa, H.; Ohishi, N. and Yagi, K., 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal biochem. Vol. 95, No. 2, pp: 351-358.
  27. Regoli, F.; Gorbi, S.; Fattorini, D.; Tedesco, S.; Notti, A.; Machella, N. and Piva, F., 2006. Use of the land snail Helix aspersa as sentinel organism for monitoring ecotoxicologic effects of urban pollution: an integrated approach. Environmental health perspectives. pp: 63-69.
  28. Roberts, B.L. and Dorough, H.W., 1985. Hazards of chemicals to earthworms. Environmental Toxicology and Chemistry. Vol. 4, No. 3, pp: 307-323.
  29. Roberts, B.L. and Wyman Dorough, H., 1984. Relative toxicities of chemicals to the earthworm Eisenia foetida. Environmental Toxicology and Chemistry. Vol. 3, No. 1, pp: 67-78.
  30. Rozman, K.K. and Klaassen, C.D., 2001. Absorption, distribution and excretion of toxicants. In: Klaassen, K.D. (Ed.), Casarett and Doull’s Toxicology. The Basic Science of Poisons. McGraw-Hill, New York. pp: 107-132.
  31. Shalata, A. and Tal, M., 1998. The effect of salt stress on lipid peroxidation and antioxidants in the leaf of the cultivated tomato and its wild salt‐tolerant relative Lycopersicon pennellii. Physiologia Plantarum. Vol. 104, 
    No. 2, pp: 169-174.
  32. Sivakumar, S., 2015. Effects of metals on earthworm life cycles: a review. Environmental monitoring and assessment. Vol. 187, No. 8, pp:1-16.
  33. Sivakumar, S. and Subbhuraam, C.V., 2005. Toxicity of chromium (III) and chromium (VI) to the earthworm Eisenia fetida. Ecotoxicology and environmental safety. Vol. 62, No. 1, pp: 93-98.
  34. Sivakumar, S.; Kavitha, K.; Rejeshwari, S.; Prabha, D. and Subburam, V., 2003. Effect of cadmium and mercury on the survival morphology and burrowing behaviour of the earthworm Lambito Mauritii (Kinberg). Indian Journal of Environmental Protection. Vol. 23, pp: 799-992.
  35. Spurgeon, D.J. and Hopkin, S.P., 1996. Effects of variations of the organic matter content and pH of soils on the availability and toxicity of zinc to the earthworm Eisenia fetida. Pedobiologia. Vol. 40, No.1, pp: 80-96.
  36. Stenersen, J., 1979. Action of pesticides on earthworms.1. Toxicity of cholinesterase- inhibiting insecticides to earthworms as evaluated by laboratory tests. Journal of Pesticide Science. Vol. 10, pp: 66-74.
  37. Stohs, S.J. and Bagchi, D., 1995. Oxidative mechanisms in the toxicity of metal ions. Free radical biology and medicine. Vol. 18, No. 2, pp: 321-336.
  38. Subramaniam, S.; Thangavel, P. and Subburam, V., 1991. Behavioral, morphological and toxic effects of Zn in the earthworm, Lambito mauritii (kinberg) in water and soil media. Indian Biologist. Vol. 24, pp: 1-7.
  39. Sun, Y.; Yin, Y.; Zhang, J.; Yu, H. and Wang, X., 2007. Bioaccumulation and ROS generation in liver of freshwater fish, goldfish Carassius auratus under HC Orange No. 1 exposure. Environmental toxicology. Vol. 22, No. 3, pp: 256-263.
  40. Veerabahu, S.; Prince, S.P.M.W. and Subburam, 
    V., 1995. 
    Toxicity of cadmium to the earthworm Drawida ramnadana (Michaelsen). Journal of Environmental Pollution. Vol. 2, pp: 55-58.
  41. Wang, Z.; Cui, Z.; Liu, L.; Ma, Q. and Xu, X., 2016. Toxicological and biochemical responses of the earthworm Eisenia fetida exposed to contaminated soil: Effects of arsenic species. Chemosphere. Vol. 154, pp: 161-170.
  42. Xu, X.B.; Shi, Y.J.; Lu, Y.L.; Zheng, X.Q. and Ritchie, R.J., 2015. Growth inhibition and altered gene transcript levels in earthworms (Eisenia fetida) exposed to 2, 2′, 4, 4′-tetrabromodiphenyl ether. Archives of environmental contamination and toxicology. Vol. 69, No. 1, pp: 1-7.
  43. Xue, Y.; Gu, X.; Wang, X.; Sun, C.; Xu, X.; Sun, J. and Zhang, B., 2009. The hydroxyl radical generation and oxidative stress for the earthworm Eisenia fetida exposed to tetrabromobisphenol A. Ecotoxicology. Vol. 18, No. 6, 
    pp: 693-699.
  44. Yasmin, S. and D’Souza, D., 2007. Effect of pesticides on the reproductive output of Eisenia fetida. Bulletin of environmental contamination and toxicology. Vol. 79, No. 5, pp: 529-532.
  45. Žaltauskaitė, J. and Sodienė, I., 2014. Effects of cadmium and lead on the life-cycle parameters of juvenile earthworm Eisenia fetida. Ecotoxicology and environmental safety. 
    Vol. 103, pp: 9-16.
  46. Zelikoff, J.T.; Wang, W.; Islam, N. and Flescher, E., 1996. Assays of reactive oxygen intermediates and antioxidant enzymes in medaka (Oryzias latipes): potential biomarkers for predicting the effects of environmental pollution. Techniques in Aquatic Toxicology. CRC Press, Boca Raton, Florida. pp: 178-206.
  47. Zhang, W.; Liu, K.; Li, J.; Chen, L. and Lin, K., 2015. Uptake and depuration kinetics of lead (Pb) and biomarker responses in the earthworm Eisenia fetida after simultaneous exposure to decabromodiphenyl ether (BDE209). Ecotoxicology and environmental safety. Vol. 113, pp: 45-51.
  48. Zhang, W.; Song, Y.F.; Sun, T.H.; Song, X.Y.; Zhou, Q.X. and Zheng, S.L., 2007. Effects of phenanthrene and pyrene on cytochrome P450 and antioxidant enzymes of earthworms (Eisenia fetida). Environmental Chemistry. Vol. 26, pp: 202-207 (in Chinese).