Skip to main content

Joint toxicity of chlorpyrifos, atrazine, and cadmium at lethal concentrations to the earthworm Eisenia fetida

Abstract

Contaminants in the environment often occur as complex mixtures, and their combined effect may exhibit toxicity to organisms. Risk assessments based on individual components tend to underestimate the effects associated with toxic action of mixtures. Toxicity studies on chemical mixtures are urgently required to assess their potential combined toxicities. The combination index (CI)-isobologram method was used to study chemical interactions to determine the nature of toxicological interactions of two pesticides chlorpyrifos and atrazine and a heavy metal cadmium toward earthworm Eisenia fetida by artificial soil and filter paper acute toxicity tests. The results showed that the binary mixture of chlorpyrifos and atrazine was antagonistic toward E. fetida at all f a levels in an artificial soil test. The combination of atrazine and Cd exhibited a slight degree of synergism throughout the exposure range, while chlorpyrifos plus Cd combination led to dual antagonistic/synergistic behavior. The nature of binary combinations in filter paper displayed opposite interaction to that in the artificial soil test, and the toxicity of ternary mixtures was not significantly synergistic than their binaries. The combination index (CI)-isobologram equation method could determine the interaction types for a series of effect levels of three chemicals in binary and ternary combinations in two types of acute earthworm tests. However, the nature of these interactions was not uniform along the f a level range in any of the two tests. Bioavailability, the nature of toxicological interaction, and the test organism need to be considered for understanding exposures and chemical measures. The synergistic effect for the particular binary combination suggests that a potential risk associated with the co-occurrence of these pollutants may still exist, which may have implications in risk assessment for the terrestrial environment. The combined effects between different contaminants might be influenced by the category of chemical, as well as the bioassay procedures. More studies of combined toxicities among these contaminants in the terrestrial environment should be conducted to identify the mixtures exhibiting synergistic pattern of interactions.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Altenburger R, Backhaus T, Boedeker W, Faust M, Scholze M, Grimme LH (2000) Predict ability of the toxicity of multiple chemical mixtures to Vibrio fischeri: mixtures composed of similarly acting chemicals. Environ Toxicol Chem 19:2341–2347

    CAS  Article  Google Scholar 

  • Anderson TD, Lydy MJ (2002) Increased toxicity to invertebrates associated with a mixture of atrazine and organophosphate insecticides. Environ Toxicol Chem 21:1507–1514

    CAS  Article  Google Scholar 

  • Barata C, Baird DJ, Nogueira AJ, Soares AM, Riva MC (2006) Toxicity of binary mixtures of metals and pyrethroid insecticides to Daphnia magna Straus. Implications for multi-substance risks assessment. Aquat Toxicol 78:1–14

    CAS  Article  Google Scholar 

  • Bjergager MB, Hanson ML, Solomon KR, Cedergreen N (2012) Synergy between prochloraz and esfenvalerate in Daphnia magna from acute and subchronic exposures in the laboratory and microcosms. Aquat Toxicol 110–111:17–24

    Article  Google Scholar 

  • Boltes K, Rosal R, García-Calvo E (2012) Toxicity of mixtures of perfluorooctane sulphonic acid with chlorinated chemicals and lipid regulators. Chemosphere 86:24–29

    CAS  Article  Google Scholar 

  • Boundy-Mills KL, de Souza ML, Mandelbaum RT, Wackett LP, Sadowsky MJ (1997) The atzB gene of Pseudomonas sp strain ADP encodes the second enzyme of a novel atrazine degradation pathway. Appl Environ Microbiol 63:916–923

    CAS  Google Scholar 

  • Cedergreen N, Kudsk P, Mathiassen SK, Sørensen H, Streibig JC (2007) Reproducibility of binary-mixture toxicity studies. Environ Toxicol Chem 26:149–156

    CAS  Article  Google Scholar 

  • Chen C, Wang Y, Zhao X, Wang Q, Qian Y (2014) Combined toxicity of butachlor, atrazine and λ-cyhalothrin on the earthworm Eisenia fetida by combination index (CI)-isobologram method. Chemosphere 112:393–401

    CAS  Article  Google Scholar 

  • Chou TC (2006) Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 58:621–681

    CAS  Article  Google Scholar 

  • Chou TC, Martin N (2005) CompuSyn for Drug Combinations: PC Software and User’s Guide: A Computer Program for Quantification of Synergism and Antagonism in Arug Aombinations and the Determination of IC50 and ED50 and LD50 Values. ComboSyn Inc, Paramus NJ

    Google Scholar 

  • Chou TC, Talalay P (1984) Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzym Regul 22:27–55

    CAS  Article  Google Scholar 

  • Choung CB, Hyne RV, Stevens MM, Hose GC (2013) The ecological effects of a herbicide-insecticide mixture on an experimental freshwater ecosystem. Environ Pollut 172:264–274

    CAS  Article  Google Scholar 

  • Cleuvers M (2003) Aquatic ecotoxicity of pharmaceuticals including the assessment of combination effects. Toxicol Lett 142:185–194

    CAS  Article  Google Scholar 

  • Dalton R (2002) Frogs put in the gender blender by America’s favorite herbicides. Nature 416:665–666

    CAS  Article  Google Scholar 

  • Fent K, Escher C, Caminada D (2006) Estrogenic activity of pharmaceuticals and pharmaceutical mixtures in a yeast reporter gene system. Reprod Toxicol 22:175–185

    CAS  Article  Google Scholar 

  • Fourie F, Reinecke SA, Reinecke AJ (2007) The determination of earthworm species sensitivity differences to cadmium genotoxicity using the comet assay. Ecotoxicol Environ Saf 67:361–368

    CAS  Article  Google Scholar 

  • Gomez-Eyles JL, Svendsen C, Lister L, Martin H, Hodson ME, Spurgeon DJ (2009) Measuring and modelling mixture toxicity of imidacloprid and thiacloprid on Caenorhabditis elegans and Eisenia fetida. Ecotoxicol. Environ Saf 72:71–79

    CAS  Article  Google Scholar 

  • González-Pleiter M, Gonzalo S, Rodea-Palomares I, Leganés F, Rosal R, Boltes K, Marco E, Fernández-Piñas F (2013) Toxicity of five antibiotics and their mixtures towards photosynthetic aquatic organisms: implications for environmental risk assessment. Water Res 47:2050–2064

    Article  Google Scholar 

  • Harabawy AS, Ibrahim AT (2014) Sublethal toxicity of carbofuran pesticide on the African catfish Clarias gariepinus (Burchell, 1822): Hematological, biochemical and cytogenetic response. Ecotoxicol Environ Saf 103:61–67

    CAS  Article  Google Scholar 

  • IARC (1994) IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, vol. 58. Beryllium, Cadmium, Mercury, and Exposures in the Glass Manufacturing Industry. http://monographs.iarc.fr/ENG/Monographs/vol58/. Accessed 9-16 February 1993

  • ISO (1993) Soil-quality-effects of Pollutants on Earthworms (Eisenia fetida). Part 1 Determination of Acute Toxicity using Artificial Soil Substrate. International Standardization Organization, Geneva, Switzerland, ISO, 11268-1. http://www.iso.org/iso/iso_catalogue/catalogue_ics/catalogue_detail_ics.htm?csnumber=19246

  • Jin-Clark Y, Lydy MJ, Zhu K (2002) Effects of atrazine and cyanazine on chlorpyrifos toxicity in Chironomus tentans (Diptera: Chironomidae). Environ Toxicol Chem 21:598–603

    CAS  Article  Google Scholar 

  • Lanno R, Wells J, Conder J, Bradham K, Basta N (2004) The bioavailability of chemicals in soil for earthworms. Ecotoxicol Environ Saf 57:39–47

    CAS  Article  Google Scholar 

  • Mahía J, Martín A, Díaz-Raviña M (2008) Extractable atrazine and its metabolites in agricultural soils from the temperate humid zone. Environ Geochem Health 30:147–152

    Article  Google Scholar 

  • Meng Z, Carper WR (2000) Effects of hydration on the molecular structure of metal ion-atrazine dimer complexes: A MOPAC (PM3) study. J Mol Struct Theochem 531:89–98

    CAS  Article  Google Scholar 

  • Munkegaard M, Abbaspoor M, Cedergreen N (2008) Organophosphorous insecticides as herbicide synergists on the green algae Pseudokirchneriella subcapitata and the aquatic plant Lemna minor. Ecotoxicology 17:29–35

    CAS  Article  Google Scholar 

  • OECD (1984) OECD Guideline for Testing of Chemicals, Earthworm Acute Toxicity. OECD, Paris, France. No. 207. http://www.oecd.org/chemicalsafety/risk-assessment/1948293.pdf. Accessed 4 April 1984

  • OECD (2004) OECD Guideline for Testing of Chemicals, Earthworm Reproduction Test (Eisenia fetida /Eisenia andrei). OECD, Paris, France. No. 222. http://www.oecd-ilibrary.org/environment/test-no-222-earthworm-reproduction-test-eisenia-fetida-eisenia-andrei_9789264070325-en. Accessed 23 Nov 2004

  • Pape-Lindstrom PA, Lydy MJ (1997) Synergistic toxicity of atrazine and organophosphate insecticides contravenes the response addition mixture model. Environ Toxicol Chem 16:2415–2420

    CAS  Article  Google Scholar 

  • Rodea-Palomares I, Petre AL, Boltes K, Legans F, Perdigón-Melón JA, Rosal R, Fernández-Piñas F (2010) Application of the combination index (CI)-isobologram equation to study the toxicological interactions of lipid regulators in two aquatic bioluminescent organisms. Water Res 44:427–438

    CAS  Article  Google Scholar 

  • Rodea-Palomares I, Leganés F, Rosal R, Fernández-Piñas F (2012) Toxicological interactions of perfluorooctane sulfonic acid (PFOS) and perfluorooctanoic acid (PFOA) with selected pollutants. J Hazard Mater 201–202:209–218

    Article  Google Scholar 

  • Rosal R, Rodea-Palomares I, Boltes K, Fernández-Piñas F, Leganés F, Petre A (2010a) Ecotoxicological assessment of surfactants in the aquatic environment: combined toxicity of docusate sodium with chlorinated pollutants. Chemosphere 81:288–293

    CAS  Article  Google Scholar 

  • Rosal R, Rodea-Palomares I, Boltes K, Fernández-Piñas F, Leganés F, Gonzalo S, Petre A (2010b) Ecotoxicity assessment of lipid regulators in water and biologically treated wastewater using three aquatic organisms. Environ Sci Pollut Res 17:135–144

    CAS  Article  Google Scholar 

  • Santos MJG, Ferreira NG, Soares AMVM, Loureiro S (2010) Toxic effects of molluscicidal baits to the terrestrial isopod Porcellionides pruinosus (Brandt, 1833). J Soil Sediments 10:1335–1343

    CAS  Article  Google Scholar 

  • Schnug L, Leinaas HP, Jensen J (2014) Synergistic sub-lethal effects of a biocide mixture on the springtail Folsomia fimetaria. Environ Pollut 186:158–164

    CAS  Article  Google Scholar 

  • Song Y, Zhu LS, Wang J, Wang JH, Liu W, Xie H (2009) DNA damage and effects on antioxidative enzymes in earthworm (Eisenia fetida) induced by atrazine. Soil Biol Biochem 41:905–909

    CAS  Article  Google Scholar 

  • Taylor P, Brown JH (1999) Acetylcholine. In: Sielgel GJ, Agranoff BW, Albers RW, Fisher SK, Uhler MD (eds) Basic neurochemistry molecular, cellular and medical aspects, 6th edn. Lippincott Wililiam & Wilkins, New York, pp 213–242

    Google Scholar 

  • Teuschler LK (2007) Deciding which chemical mixtures risk assessment methods work best for what mixtures. Toxicol Appl Pharmacol 223:139–147

    CAS  Article  Google Scholar 

  • Waisberg M, Joseph P, Hale B, Beyersmann D (2003) Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 192:95–117

    CAS  Article  Google Scholar 

  • Wang J, Zhu L, Meng Y, Wang J, Xie H, Zhang QM (2012a) The combined stress effects of atrazine and cadmium on the earthworm Eisenia fetida. Environ Toxicol Chem 31:2035–2040

    CAS  Article  Google Scholar 

  • Wang Y, Cang T, Zhao X, Yu R, Chen L, Wu C, Wang Q (2012b) Comparative acute toxicity of twenty-four insecticides to earthworm, Eisenia fetida. Ecotoxicol Environ Saf 9:122–128

    CAS  Article  Google Scholar 

Download references

Acknowledgments

The research was supported by the Zhejiang Province Major Bidding Project (Grant No. 2014C02002), Science and Technology Innovation Program of Chinese Academy of Agricultural Sciences, and the Innovation Project of Zhejiang Academy of Agricultural Sciences.

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Yongzhong Qian or Qiang Wang.

Additional information

Guiling Yang and Chen Chen contributed equally to this study.

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yang, G., Chen, C., Wang, Y. et al. Joint toxicity of chlorpyrifos, atrazine, and cadmium at lethal concentrations to the earthworm Eisenia fetida . Environ Sci Pollut Res 22, 9307–9315 (2015). https://doi.org/10.1007/s11356-015-4097-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-4097-3

Keywords

  • Insecticide
  • Herbicide
  • Heavy metal
  • Eisenia fetida
  • Acute mixture toxicity
  • Combination index