Advertisement

Toxicity prediction and assessment of an environmentally realistic pesticide mixture to Daphnia magna and Raphidocelis subcapitata

  • E. Silva
  • C. Martins
  • A. S. Pereira
  • S. Loureiro
  • M. J. Cerejeira
Article

Abstract

In a regulatory perspective addressing the cumulative effect of co-occurring chemicals is the first and most important step in providing a more realistic hazard assessment of chemical cocktails to both man and environment. This study was conducted to show if joint effects on the immobilisation of the crustacean Daphnia magna and on the growth inhibition of algae Raphidocelis subcapitata follow additivity (concentration addition (CA) or independent action (IA) predictions) or if there is an interaction between chemicals in the organisms upon exposure to an environmentally realistic mixture of chlorpyrifos and terbuthylazine, with expected different molecular sites of action. A pattern of antagonism at lower doses and synergism at higher doses was found for acute immobility data, while no deviation from the additive conceptual models was observed in the algae inhibition test. Results in relation to the relevant set of regulatory acceptable concentrations (RACs) and environmental quality standards (EQSs) derived for individual chlorpyrifos and terbuthylazine were evaluated.

Keywords

Mixture Insecticide Herbicide Daphnia magna Raphidocelis subcapitata Toxicity 

Notes

Acknowledgements

This work was supported by national funds from Fundação para a Ciência e a Tecnologia through the research unit UID/AGR/04129/2013 (LEAF).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Amorim MJB, Pereira C, Menezes-Oliveira VB, Campos B, Soares AMVM, Loureiro S (2012) Assessing single and joint effects of chemicals on the survival and reproduction of Folsomia candida (Collembola) in soil. Environ Pollut 160(1):145–152.  https://doi.org/10.1016/j.envpol.2011.09.005 CrossRefGoogle Scholar
  2. Anderson TD, Lydy MJ (2002) Increased toxicity to invertebrates associated with a mixture of atrazine and organophosphate insecticides. Environ Toxicol Chem 21(7):1507–1514.  https://doi.org/10.1002/etc.5620210724 CrossRefGoogle Scholar
  3. Anderson TD, Zhu KY (2004) Synergistic and antagonistic effects of atrazine on the toxicity of organophosphorodithioate and organophosphorothioate insecticides to Chironomus tentans (Diptera: Chironomidae). Pestic Biochem Physiol 80(1):54–64.  https://doi.org/10.1016/j.pestbp.2004.06.003 CrossRefGoogle Scholar
  4. Banks KE, Turner PK, Wood SH, Matthews C (2005) Increased toxicity to Ceriodaphnia dubia in mixtures of atrazine and diazinon at environmentally realistic concentrations. Ecotoxicol Environ Saf 60(1):28–36.  https://doi.org/10.1016/j.ecoenv.2003.12.016 CrossRefGoogle Scholar
  5. Belden JB, Brain RA (2018) Incorporating the joint toxicity of co-applied pesticides into the ecological risk assessment process. Integr Environ Assess Manag 14(1):79–91.  https://doi.org/10.1002/ieam.1957 CrossRefGoogle Scholar
  6. Belden JB, Gilliom RJ, Lydy MJ (2007) How well can we predict the toxicity of pesticide mixtures to aquatic life? Integr Environ Assess Manag 3(3):364–372.  https://doi.org/10.1002/ieam.5630030326 CrossRefGoogle Scholar
  7. Belden JB, Lydy MJ (2000) Impact of atrazine on organophosphate insecticide toxicity. Environ Toxicol Chem 19(9):2266–2274.  https://doi.org/10.1002/etc.5620190917 CrossRefGoogle Scholar
  8. Bjergager M-BA, Dalhoff K, Kretschmann A, Nørgaard KB, Mayer P, Cedergreen N (2017) Determining lower threshold concentrations for synergistic effects. Aquat Toxicol 182:79–90.  https://doi.org/10.1016/j.aquatox.2016.10.020 CrossRefGoogle Scholar
  9. Bliss CI (1939) The toxicity of poisons applied jointly. Ann Appl Biol 26(3):585–615.  https://doi.org/10.1111/j.1744-7348.1939.tb06990.x CrossRefGoogle Scholar
  10. Ccanccapa A, Masiá A, Andreu V, Picó Y (2016a) Spatio-temporal patterns of pesticide residues in the Turia and Júcar Rivers (Spain). Sci Total Environ 540:200–210.  https://doi.org/10.1016/j.scitotenv.2015.06.063 CrossRefGoogle Scholar
  11. Ccanccapa A, Masiá A, Navarro-Ortega A, Picó Y, Barceló D (2016b) Pesticides in the Ebro River basin: occurrence and risk assessment. Environ Pollut 211:414–424.  https://doi.org/10.1016/j.envpol.2015.12.059 CrossRefGoogle Scholar
  12. Cedergreen N (2014) Quantifying synergy: a systematic review of mixture toxicity studies within environmental toxicology. PLoS One 9(5):e96580.  https://doi.org/10.1371/journal.pone.0096580 CrossRefGoogle Scholar
  13. Cedergreen N, Streibig JC (2005) The toxicity of herbicides to non-target aquatic plants and algae: assessment of predictive factors and hazard. Pest Manag Sci 61(12):1152–1160.  https://doi.org/10.1002/ps.1117 CrossRefGoogle Scholar
  14. Cedergreen N, Svendsen C, Backhaus T (2013) Toxicity prediction of chemical mixtures. In: Jorgensen SE (ed) Encyclopedia of Environmental Management, Taylor and Francis: New York, 2572–2581. https://doi.org/10.1081/E-EEM-120046684
  15. DeLorenzo ME, Serrano L (2003) Individual and mixture toxicity of three pesticides; atrazine, chlorpyrifos, and chlorothalonil to the marine phytoplankton species Dunaliella tertiolecta. J Environ Sci Health B 38(5):529–538.  https://doi.org/10.1081/PFC-120023511 CrossRefGoogle Scholar
  16. Dong X, Zhu L, Wang J, Wang J, Xie H, Hou X, Jia W (2009) Effects of atrazine on cytochrome P450 enzymes of zebrafish (Danio rerio). Chemosphere 77(3):404–412.  https://doi.org/10.1016/j.chemosphere.2009.06.052. Epub 2009 Jul 31CrossRefGoogle Scholar
  17. EC (2001) Commission Directive 2001/59/EC of 6 August 2001 adapting to technical progress for the 28th time Council Directive 67/548/EEC on the approximation of the laws, regulations and administrative provisions relating to the classification, packaging and labelling of dangerous substances. Official Journal L 225 of 21.08.2001, pp 1–333Google Scholar
  18. EC (2009) Regulation (EC) No 1107/2009 of the European Parliament and of the Council of 21 October 2009 concerning the placing of plant protection products on the market and repealing Council Directives 79/117/EEC and 91/414/EEC. Official Journal of the European Union L 309 of 24.11.2009, pp 1–50Google Scholar
  19. EC (2013) Directive 2013/39/EU of the European Parliament and of the Council of 12 August 2013 amending Directives 2000/60/EC and 2008/105/EC as regards priority substances in the field of water policy. Official Journal of the European Union L 226 of 24.08.2013, pp. 1–17Google Scholar
  20. Eurostat (2013) Agriculture, forestry and fishery statistics, 2013 edition. European Union, LuxembourgGoogle Scholar
  21. Faust M, Altenburger R, Backhaus T, Blanck H, Boedeker W, Gramatica P, Hamer V, Scholze M, Vighi M, Grimme LH (2001) Predicting the joint algal toxicity of multi-component s-triazine mixtures at low-effect concentrations of individual toxicants. Aquat Toxicol 56(1):13–32. doi: 10.1016/S0166-445X(01)00187-4CrossRefGoogle Scholar
  22. FOOTPRINT (2017) The FOOTPRINT pesticide properties database. http://sitem.herts.ac.uk/aeru/iupac/index.htm. Accessed 1 Aug 2017
  23. Fu Y, Li M, Liu C, Qu JP, Zhu WJ, Xing HJ, Xu SW, Li S (2013) Effect of atrazine and chlorpyrifos exposure on ctochrome P450 contents and enzyme activities in common carp gills. Ecotoxicol Environ Saf 94:28–36.  https://doi.org/10.1016/j.ecoenv.2013.04.018 CrossRefGoogle Scholar
  24. Herrero-Hernández E, Rodríguez-Cruz MS, Pose-Juan E, Sánchez-González S, Andrades MS, Sánchez-Martín MJ (2017) Seasonal distribution of herbicide and insecticide residues in the water resources of the vineyard region of La Rioja (Spain). Sci Total Environ 609:161–171.  https://doi.org/10.1016/j.scitotenv.2017.07.113 CrossRefGoogle Scholar
  25. ISO (International Organization for Standardization) (2005) ISO/IEC 17025: General Requirements for the Competence of Testing and Calibration Laboratories. ISO, GenevaGoogle Scholar
  26. ISO (International Organization for Standardization) (2012a) ISO 6341: Water quality - Determination of the inhibition of the mobility of Daphnia magna Straus (Cladocera, Crustacea) - Acute toxicity test. ISO, GenevaGoogle Scholar
  27. ISO (International Organization for Standardization) (2012b) ISO 8692: Water quality - Fresh water algal growth inhibition test with unicellular green algae. ISO, GenevaGoogle Scholar
  28. Jin-Clark Y, Lydy M, Zhu K (2002) Effects of atrazine and cyanazine on chlorpyrifos toxicity in Chironomus tentans (Diptera: Chironomidae). Environ Toxicol Chem 21(3):598–603.  https://doi.org/10.1002/etc.5620210319 CrossRefGoogle Scholar
  29. Jonker MJ, Svendsen C, Bedaux JJ, Bongers M, Kammenga JE (2005) Significance testing of synergistic/antagonistic, dose level-dependent, or dose ratio-dependent effects in mixture dose-response analysis. Environ Toxicol Chem 24(10):2701–2713.  https://doi.org/10.1897/04-431R.1 CrossRefGoogle Scholar
  30. Junghans M, Backhaus T, Faust M, Scholze M, Grimme LH (2006) Application and validation of approaches for the predictive hazard assessment of realistic pesticide mixtures. Aquat Toxicol 76(2):93–110.  https://doi.org/10.1016/j.aquatox.2005.10.001 CrossRefGoogle Scholar
  31. Kienzler A, Berggren E, Bessems J, Bopp S, van der Linden S, Worth A (2014) Assessment of Mixtures - Review of Regulatory Requirements and Guidance. Joint Research Centre, Science and Policy Report. Publications Office of the European Union, Luxembourg, https://doi.org/10.2788/84264Google Scholar
  32. Kienzler A, Bopp SK, van der Linden S, Berggren E, Worth A (2016) Regulatory assessment of chemical mixtures: requirements, current approaches and future perspectives. Regul Toxicol Pharm 80:321–334.  https://doi.org/10.1016/j.yrtph.2016.05.020 CrossRefGoogle Scholar
  33. Kikuchi M, Sasaki Y, Wakabayashi M (2000) Screening of organophosphate insecticide pollution in water by using Daphnia magna. Environ Toxicol 47(3):239–245.  https://doi.org/10.1006/eesa.2000.1958 Google Scholar
  34. Loewe S, Muischnek H (1926) Über Kombinationswirkungen. H Arch F Exp Pathol U Pharmakol 114(5-6):313–326.  https://doi.org/10.1007/BF01952257 CrossRefGoogle Scholar
  35. Løkke H, Ragas AMJ, Holmstrup M (2013) Tools and perspectives for assessing chemical mixtures and multiple stressors. Toxicology 313(2-3):73–82.  https://doi.org/10.1016/j.tox.2012.11.009 CrossRefGoogle Scholar
  36. Loureiro S, Amorim MJ, Campos B, Rodrigues SMG, Soares AMVM (2009) Assessing joint toxicity of chemicals in Enchytraeus albidus (Enchytraeidae) and Porcellionides pruinosus (Isopoda) using avoidance behaviour as an endpoint. Environ Pollut 157(2):625–636.  https://doi.org/10.1016/j.envpol.2008.08.010 CrossRefGoogle Scholar
  37. Loureiro S, Svendsen C, Ferreira ALG, Pinheiro C, Ribeiro F, Soares AMVM (2010) Toxicity of three binary mixtures to Daphnia magna: comparing chemical modes of action and deviations from conceptual models. Environ Toxicol Chem 29(8):1716–1726.  https://doi.org/10.1002/etc.198 CrossRefGoogle Scholar
  38. Lydy MJ, Austin KR (2004) Toxicity assessment of pesticide mixtures typical of the Sacramento-San Joaquin Delta using Chironomus tentans. Arch Environ Contam Toxicol 48(1):49–55.  https://doi.org/10.1007/s00244-004-0056-6 CrossRefGoogle Scholar
  39. Lydy MJ, Linck SL (2003) Assessing the impact of triazine herbicides on organophosphate insecticide to the earthworm Eisenia fetida. Arch Environ Contam Toxicol 45(3):343–349.  https://doi.org/10.1007/s00244-002-0218-y CrossRefGoogle Scholar
  40. Marchini S, Passerini L, Cesareo D, Tosato ML (1988) Herbicidal triazines: acute toxicity on Daphnia, fish, and plants and analysis of its relationships with structural factors Ecotoxicol Environ Saf 16(2):148–157. https://doi.org/10.1016/0147-6513(88)90029-2CrossRefGoogle Scholar
  41. McBean C (2012) A world compendium. The pesticide manual, sixteenth edition, British Crop Protection Council, Alton, UKGoogle Scholar
  42. 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(1):29–35.  https://doi.org/10.1007/s10646-007-0173-x CrossRefGoogle Scholar
  43. Neter J, Kutner MH, Nachtsheim CJ, Wasserman W (1996) Applied linear statistical models. McGraw-Hill, Irwin, ChicagoGoogle Scholar
  44. OECD (Organisation for Economic Co-operation and Development (2002) Guidance Document on Aquatic Toxicity Testing of Difficult Substances and Mixtures. OECD Publishing, Paris, https://doi.org/10.1787/9789264078406-enGoogle Scholar
  45. OECD (Organisation for Economic Co-operation and Development (2004) Test No. 202: Daphnia sp. Acute Immobilisation Test. OECD Publishing, Paris, https://doi.org/10.1787/9789264069947-enGoogle Scholar
  46. OECD (Organisation for Economic Co-operation and Development (2011) Test No. 201: Freshwater Alga and Cyanobacteria, Growth Inhibition Test. OECD Publishing, Paris, https://doi.org/10.1787/9789264069923-enGoogle Scholar
  47. Okamura H, Aoyama I, Liu D, Maguire RJ, Pacepavicius GJ, Lau YL (2000) Fate and ecotoxicity of the new antifouling compound Irgarol 1051 in the aquatic environment Water Res 34(14):3523–3530. https://doi.org/10.1016/S0043-1354(00)00095-6CrossRefGoogle Scholar
  48. Palma P, Palma VL, Fernandes RM, Soares AM, Barbosa IR (2008) Acute toxicity of atrazine, endosulfan sulphate and chlorpyrifos to Vibrio fischeri, Thamnocephalus platyurus and Daphnia magna, relative to their concentrations in surface waters from the Alentejo region of Portugal. Bull Environ Contam Toxicol 81(5):485–489.  https://doi.org/10.1007/s00128-008-9517-3 CrossRefGoogle Scholar
  49. Papadakis EN, Tsaboula A, Kotopoulou A, Kintzikoglou K, Vryzas Z, Papadopoulou-Mourkidou E (2015) Pesticides in the surface waters of Lake Vistonis Basin, Greece: occurrence and environmental risk assessment. Sci Total Environ 536:793–802.  https://doi.org/10.1016/j.scitotenv.2015.07.099 CrossRefGoogle Scholar
  50. Papadakis EN, Tsaboula A, Vryzas Z, Kotopoulou A, Kintzikoglou K, Papadopoulou-Mourkidou E (2018) Pesticides in the rivers and streams of two river basins in northern Greece. Sci Total Environ 624:732–743.  https://doi.org/10.1016/j.scitotenv.2017.12.074 CrossRefGoogle Scholar
  51. Pape-Lindstrom PA, Lydy MJ (1997) Synergistic toxicity of atrazine and organophosphate insecticides contravenes the response addition mixture model. Environ Toxicol Chem 16(11):2415–2420.  https://doi.org/10.1002/etc.5620161130 CrossRefGoogle Scholar
  52. Pereira AS, Cerejeira MJ, Daam MA (2017a) Evaluation of FOCUS surface water pesticide concentration predictions and risk assessment of field-measured pesticide mixtures-a crop-based approach under Mediterranean conditions. Environ Sci Pollut Res 24(21):17394–17406.  https://doi.org/10.1007/s11356-017-9393-7 CrossRefGoogle Scholar
  53. Pereira AS, Cerejeira MJ, Daam MA (2017b) Toxicity of environmentally realistic concentrations of chlorpyrifos and terbuthylazine in indoor microcosms. Chemosphere 182:348–355.  https://doi.org/10.1016/j.chemosphere.2017.05.032 CrossRefGoogle Scholar
  54. Pérez J, Domingues I, Monteiro M, Soares AM, Loureiro S (2013a) Synergistic effects caused by atrazine and terbuthylazine on chlorpyrifos toxicity to early-life stages of the zebrafish Danio rerio. Environ Sci Pollut Res 20(7):4671–4680.  https://doi.org/10.1007/s11356-012-1443-6 CrossRefGoogle Scholar
  55. Pérez J, Domingues I, Soares AM, Loureiro S (2011) Growth rate of Pseudokirchneriella subcapitata exposed to herbicides found in surface waters in the Alqueva reservoir (Portugal): a bottom-up approach using binary mixtures. Ecotoxicology 20(6):1167–1175.  https://doi.org/10.1007/s10646-011-0661-x CrossRefGoogle Scholar
  56. Pérez J, Monteiro M, Quintaneiro C, Soares AM, Loureiro S (2013b) Characterization of cholinesterases in Chironomus riparius and the effects of three herbicides on chlorpyrifos toxicity. Aquat Toxicol 144-145:296–302.  https://doi.org/10.1016/j.aquatox.2013.10.014 CrossRefGoogle Scholar
  57. Ritz C (2010) Toward a unified approach to dose-response modeling in ecotoxicology. Environ Toxicol Chem 29(1):220–229.  https://doi.org/10.1002/etc.7 CrossRefGoogle Scholar
  58. RIVM (2017) Zoeksysteem Risico’s van stoffen. https://rvs.rivm.nl/zoeksysteem/. Accessed 1 Aug 2017
  59. Rodney SI, Teed RS, Moore DRJ (2013) Estimating the toxicity of pesticide mixtures to aquatic organisms: a review. Hum Ecol Risk Assess 19(6):1557–1575.  https://doi.org/10.1080/10807039.2012.723180 CrossRefGoogle Scholar
  60. Rubach MN, Crum SJH, van den Brink PJ (2011) Variability in the dynamics of mortality and immobility responses of freshwater arthropods exposed to chlorpyrifos. Arch Environ Contam Toxicol 60(4):708–721.  https://doi.org/10.1007/s00244-010-9582-6 CrossRefGoogle Scholar
  61. Schreiner VC, Szöcs E, Bhowmik AK, Vijver MG, Schäfer RB (2016) Pesticide mixtures in streams of several European countries and the USA. Sci Tot Environ 573:680–689.  https://doi.org/10.1016/j.scitotenv.2016.08.163 CrossRefGoogle Scholar
  62. Schuler LJ, Trimble AJ, Belden JB, Lydy MJ (2005) Joint toxicity of triazine herbicides and organophosphate insecticides to the midge Chironomus tentans. Arch Environ Contam Toxicol 49(2):173–177.  https://doi.org/10.1007/s00244-004-0224-8 CrossRefGoogle Scholar
  63. Silva E, Daam MA, Cerejeira MJ (2015) Aquatic risk assessment of priority and other river basin specific pesticides in surface waters of Mediterranean river basins. Chemosphere 135:394–402.  https://doi.org/10.1016/j.chemosphere.2015.05.013 CrossRefGoogle Scholar
  64. Silva E, Mendes MP, Ribeiro L, Cerejeira MJ (2012a) Exposure assessment of pesticides in a shallow groundwater of the Tagus vulnerable zone (Portugal): a multivariate statistical approach (JCA). Environ Sci Pollut Res 19(7):2667–2680.  https://doi.org/10.1007/s11356-012-0761-z CrossRefGoogle Scholar
  65. Silva E, Pereira AC, Estalagem SP, Moreira-Santos M, Ribeiro R, Cerejeira MJ (2012b) Assessing the quality of freshwaters in a protected area within the Tagus river basin district (central Portugal). J Environ Qual 41(5):1413–1426.  https://doi.org/10.2134/jeq2012.0010 CrossRefGoogle Scholar
  66. SOP (2003) Standard Operational Procedure Daphtoxkit F™ magna, crustacean toxicity screening test for freshwater. MicroBioTests, Inc., Mariakerke, Gent, BelgiumGoogle Scholar
  67. SOP (2004) Standard Operational Procedure Algaltoxkit F™, freshwater toxicity test with microalgae. MicroBioTests, Inc., Mariakerke, Gent, BelgiumGoogle Scholar
  68. Sousa JCG, Ribeiro AR, Barbosa MO, Pereira MFR, Silva AMT (2018) A review on environmental monitoring of water organic pollutants identified by EU guidelines. J Hazard Mater 344:146–162.  https://doi.org/10.1016/j.jhazmat.2017.09.058 CrossRefGoogle Scholar
  69. Stehle S, Schulz R (2015) Pesticide authorization in the EU-environment unprotected? Environ Sci Pollut Res 22(24):19632–19647.  https://doi.org/10.1007/s11356-015-5148-5 CrossRefGoogle Scholar
  70. Svendsen C, Siang P, Lister LJ, Rice A, Spurgeon DJ (2010) Similarity, independence, or interaction for binary mixture effects of nerve toxicants for the nematode Caenorhabditis elegans. Environ Toxicol Chem 29(5):1182–1191.  https://doi.org/10.1002/etc.140 Google Scholar
  71. Systat (2017) SigmaPlot version 13.0, from Systat Software, Inc., San Jose, CA, USA www.systatsoftware.com. Accessed 1 Aug 2017
  72. Tasca AL, Puccini M, Fletcher A (2018) Terbuthylazine and desethylterbutylazine: Recent occurrence, mobility and removal techniques. Chemosphere 202:94–104.  https://doi.org/10.1016/j.chemosphere.2018.03.091 CrossRefGoogle Scholar
  73. Trimble AJ, Lydy MJ (2006) Effects of triazine herbicides on organophosphate insecticide toxicity in Hyalella azteca. Arch Environ Contam Toxicol 51(1):29–34.  https://doi.org/10.1007/s00244-005-0176-7 CrossRefGoogle Scholar
  74. Tsaboula A, Papadakis EN, Vryzas Z, Kotopoulou A, Kintzikoglou K, Papadopoulou-Mourkidou E (2016) Environmental and human risk hierarchy of pesticides: a prioritization method, based on monitoring, hazard assessment and environmental fate. Environ Int 91:78–93.  https://doi.org/10.1016/j.envint.2016.02.008 CrossRefGoogle Scholar
  75. van der Werf HMG (1996) Assessing the impact of pesticides on the environment Agric Ecosyst Environ 60(2-3):81–96. https://doi.org/10.1016/S0167-8809(96)01096-1CrossRefGoogle Scholar
  76. Verbruggen EMJ, van den Brink PJ (2010) Review of recent literature concerning mixture toxicity of pesticides to aquatic organisms. Report 601400001/2010, RIVM, the NetherlandsGoogle Scholar
  77. Vighi M, Altenburger R, Arrhenius Å, Backhaus T, Bödeker W, Blanck H, Consolaro F, Faust M, Finizio A, Froehner K, Gramatica P, Grimme LH, Grönvall F, Hamer V, Scholze M, Walter H (2003) Water quality objectives for mixtures of toxic chemicals: problems and perspectives Ecotoxicol Environ Saf 54(2):139–150. https://doi.org/10.1016/S0147-6513(02)00047-7CrossRefGoogle Scholar
  78. Wacksman MN, Maul JD, Lydy MJ (2006) Impact of atrazine on chlorpyrifos toxicity in four aquatic vertebrates. Arch Environ Contam Toxicol 51(4):681–689.  https://doi.org/10.1007/s00244-005-0264-8 CrossRefGoogle Scholar
  79. Xing H, Wang C, Wu H, Chen D, Li S, Xu S (2015) Effects of atrazine and chlorpyrifos on DNA methylation in the brain and gonad of the common carp. Comp Biochem Physiol C Toxicol Pharmacol 168:11–19.  https://doi.org/10.1016/j.cbpc.2014.11.002 CrossRefGoogle Scholar
  80. Yang G, Chen C, Wang Y, Cai L, Kong X, Qian Y, Wang Q (2015) Joint toxicity of chlorpyrifos, atrazine, and cadmium at lethal concentrations to the earthworm Eisenia fetida. Environ Sci Pollut Res 22(12):9307–9315.  https://doi.org/10.1007/s11356-015-4097-3 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.LEAF, Linking Landscape, Environment, Agriculture and Food, Instituto Superior de AgronomiaUniversidade de LisboaLisboaPortugal
  2. 2.Department of Biology and CESAMUniversity of AveiroAveiroPortugal

Personalised recommendations