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Assessing interactive mixture toxicity of carbamate and organophosphorus insecticides in the yabby (Cherax destructor)

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Abstract

Carbamate (CB) and organophosphorus (OP) pesticides are commonly detected in aquatic ecosystems and predominantly occur as mixtures of varying complexity. These pesticides inhibit the activity of total cholinesterase (ChE) and thus have the potential to interfere with behaviours that may be essential for the survival of aquatic species. Although the effects of individual ChE insecticides on aquatic species have been reported for decades, the neurotoxicity of mixtures is still poorly understood. This study examined the chronic toxicities of two OP insecticides (chlorpyrifos (CPF) and malathion (MAL)) and one carbamate insecticide (methomyl (METH)) in binary and ternary mixtures on the ChE activity of the yabby (C. destructor). Using the concentration addition approach to estimate mixture toxicity, the observed inhibition of ChE activity caused by all binary mixtures of CPF plus MAL, CPF plus METH and MAL plus METH was additive. In ternary mixtures, all combinations of CPF, MAL and METH were either additive or antagonistic depending on the relative ratios of these chemicals in the mixtures. The effect of mixtures of these three insecticides on C. destructor has not previously been assessed, and the data suggest that individual chemical risk assessments are likely to incorrectly estimate the effect of these insecticides on C. destructor in the aquatic environment where combinations of such chemicals occur.

Highlights

  • AChE activity inhibition caused by both binary and tertiary mixtures was dependent on the relative ratios of these chemicals in the mixtures.

  • All combinations of CPF, MAL and METH conformed to less than additive and antagonistic.

  • Data suggests that individual chemical risk assessments are likely to incorrectly estimate the effect of these insecticides.

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References

  • Abdullah A, Kumar A, Chapman J (1994) Inhibition of acetylcholinesterase in the Australian freshwater shrimp (Paratya australiensis) by profenofos. Environ Toxicol Chem 13:1861–1866

    Article  Google Scholar 

  • Aldridge WN, Reiner E (1972) Enzyme inhibitors as substrates. Interact Este Este Organo carbamic Acids Biochem J 115:14–162

    Google Scholar 

  • Altenburger R, Nendza M, Schüürmann G (2003) Mixture toxicity and its modeling by quantitative structure‐activity relationships. Environ Toxicol Chem 22:1900–1915

    Article  CAS  Google Scholar 

  • Backhaus T, Faust M, Scholze M, Gramatica P, Vighi M, Grimme LH (2004) Joint algal toxicity of phenylurea herbicides is equally predictable by concentration addition and independent action. Environ Toxicol Chem 23:258–264

    Article  CAS  Google Scholar 

  • Barata C, Solayan A, Porte C (2004) Role of B-esterases in assessing toxicity of organophosphorus (chlorpyrifos, malathion) and carbamate (carbofuran) pesticides to Daphnia magna. Aquat Toxicol 66:125–139

    Article  CAS  Google Scholar 

  • Belden JB, Gilliom RJ, Lydy MJ (2007) How well can we predict the toxicity of pesticide mixtures to aquatic life? Integr Environ Assess Manag 3:364–372

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Cedergreen N (2014) Quantifying synergy: a systematic review of mixture toxicity studies within environmental toxicology. PLoS ONE 9:e96580

    Article  Google Scholar 

  • Chambers H, Brown B, Chambers JE (1990) Noncatalytic detoxication of six organophosphorus compounds by rat liver homogenates. Pestic Biochem Physiol 36:308–315

    Article  CAS  Google Scholar 

  • Chen C, Wang Y, Zhao X, Wang Q, Qian Y (2014) The combined toxicity assessment of carp (Cyprinus carpio) acetylcholinesterase activity by binary mixtures of chlorpyrifos and four other insecticides. Ecotoxicology 23:221–228

    Article  CAS  Google Scholar 

  • Drost W, Backhaus T, Vassilakaki M, Horst Grimme L (2003) Mixture toxicity of s-triazines to Lemna minor under conditions of simultaneous and sequential exposure. Fresenius Environ Bull 12:601–607

    CAS  Google Scholar 

  • Eaton DL et al. (2008) Review of the toxicology of chlorpyrifos with an emphasis on human exposure and neurodevelopment. Crit Rev Toxicol 38:1–125

    Article  CAS  Google Scholar 

  • Eggen RI, Behra R, Burkhardt-Holm P, Escher BI, Schweigert N (2004) Peer reviewed: challenges in ecotoxicology. Crit Rev Toxicol 38(suppl 2):1–125

    Google Scholar 

  • Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88IN191–9095

    Article  Google Scholar 

  • EPA (2016) Restricted use products (RUP) report. Tech report, U.S. Environment Protection Agency, Washington, D.C.

  • Escartı́n E, Porte C (1996) Acetylcholinesterase Inhibition in the CrayfishProcambarus clarkiiExposed to Fenitrothion. Ecotoxicol Environ Saf 34:160–164

    Article  Google Scholar 

  • Faust M et al. (2001) Predicting the joint algal toxicity of multi-component s-triazine mixtures at low-effect concentrations of individual toxicants. Aquat Toxicol 56:13–32

    Article  CAS  Google Scholar 

  • Faust M, Altenburger R, Backhaus T, Bödeker W, Scholze M, Grimme L (2000) Predictive assessment of the aquatic toxicity of multiple chemical mixtures. J Environ Qual 29:1063–1068

    Article  CAS  Google Scholar 

  • Ferrari A, Venturino A, de D’Angelo AMP (2007) Effects of carbaryl and azinphos methyl on juvenile rainbow trout (Oncorhynchus mykiss) detoxifying enzymes. Pestic Biochem Physiol 88:134–142

    Article  CAS  Google Scholar 

  • Firpo S (2011) Mixture and single-compound toxicity using Daphnia magna. Comparisons with estimates of concentration addition and independent action. Swedish University of Agricultural Sciences, Uppsala

  • Gilliom RJ (2007) Pesticides in US streams and groundwater. Environ Sci Technol 41:3408–3414

    Article  CAS  Google Scholar 

  • Huynh H, Nugegoda D (2012) Effects of chlorpyrifos exposure on growth and food utilization in Australian catfish, Tandanus tandanus. J World Aquac Soc 42:5

    Google Scholar 

  • Jensen CS, Garsdal L, Baatrup E (1997) Acetylcholinesterase inhibition and altered locomotor behavior in the carabid beetle Pterostichus cupreus. A linkage between biomarkers at two levels of biological complexity. Environ Toxicol Chem 16:1727–1732. https://doi.org/10.1002/etc.5620160822

    Article  CAS  Google Scholar 

  • Jokanović M (2001) Biotransformation of organophosphorus compounds. Toxicology 166:139–160

    Article  Google Scholar 

  • Junghans M, Backhaus T, Faust M, Scholze M, Grimme L (2006) Application and validation of aproaches for the predictive hazard assessment of realistic pesticide mixtures. Aquat Toxicol 76:93–110

    Article  CAS  Google Scholar 

  • Key PB, Fulton MH (2006) Correlation between 96-h mortality and 24-h acetylcholinesterase inhibition in three grass shrimp larval life stages. Ecotoxicol Environ Saf 63:389–392

    Article  CAS  Google Scholar 

  • Kirby M, Morris S, Hurst M, Kirby S, Neall P, Tylor T, Fagg A (2000) The use of cholinesterase activity in flounder (Platichthys flesus) muscle tissue as a biomarker of neurotoxic contamination in UK estuaries. Mar Pollut Bull 40:780–791

    Article  CAS  Google Scholar 

  • Kok FN, Hasirci V (2004) Determination of binary pesticide mixtures by an acetylcholinesterase–choline oxidase biosensor. Biosens Bioelectron 19:661–665

    Article  CAS  Google Scholar 

  • Kumar A, Doan H, Barnes M, Chapman JC, Kookana RR (2010) Response and recovery ofacetylcholinesterase activity in freshwater shrimp, Paratya australiensis (Decapoda: Atyidae) exposed toselected anti-cholinesterase insecticides. Ecotoxicol Environ Saf 73:1503–1510

    Article  CAS  Google Scholar 

  • Laetz CA, Baldwin DH, Collier TK, Hebert V, Stark JD, Scholz NL (2009) The synergistic toxicity of pesticide mixtures: implications for risk assessment and the conservation of endangered Pacific salmon. Environ Health Perspect 117:348

    Article  CAS  Google Scholar 

  • Laetz CA, Baldwin DH, Hebert V, Stark JD, Scholz NL (2013) Interactive neurobehavioral toxicity of diazinon, malathion, and ethoprop to juvenile coho salmon. Environ Sci Technol 47:2925–2931

    Article  CAS  Google Scholar 

  • Lewis JA, Gehman EA, Baer CE, Jackson DA (2013) Alterations in gene expression in Caenorhabditis elegans associated with organophosphate pesticide intoxication and recovery. BMC Genom 14:291. https://doi.org/10.1186/1471-2164-14-291

    Article  CAS  Google Scholar 

  • Li H, Jiang H, Gao X, Wang X, Qu W, Lin R, Chen J (2008) Acute toxicity of the pesticide methomyl on the topmouth gudgeon (Pseudorasbora parva): mortality and effects on four biomarkers. Fish Physiol Biochem 34:209–216

    Article  CAS  Google Scholar 

  • Lodge DM, Kershner MW, Aloi JE, Covich AP (1994) Effects of an omnivorous crayfish (Orconectes rusticus) on a freshwater littoral food web. Ecology 75:1265–1281

    Article  Google Scholar 

  • Lydy M, Belden J, Wheelock C, Hammock B, Denton D (2004) Challenges in regulating pesticide mixtures Ecology and Society 9 (6):1.

  • Mileson BE et al. (1998) Common mechanism of toxicity: a case study of organophosphorus pesticides. Toxicol Sci 41:8–20

    CAS  Google Scholar 

  • Momot WT, Gowing H, Jones PD (1978) The dynamics of crayfish and their role in ecosystems Am Mid Natur 99:10–35

    Article  Google Scholar 

  • Monosson E (2005) Chemical mixtures: considering the evolution of toxicology and chemical assessment. Environ Health Perspect 113:383

    Article  CAS  Google Scholar 

  • Moore DR, Teed RS (2013) Risks of carbamate and organophosphate pesticide mixtures to salmon in the Pacific Northwest. Integr Environ Assess Manag 9:70–78

    Article  CAS  Google Scholar 

  • Morifusa E (1974) Organophosphorus pesticides; organic and biological chemistry. CRC pesticide. CRC Press, Cleveland, Ohio

    Google Scholar 

  • Mwila K et al. (2013) The effect of mixtures of organophosphate and carbamate pesticides on acetylcholinesterase and application of chemometrics to identify pesticides in mixtures. Environ Monit Assess 185:2315–2327

    Article  CAS  Google Scholar 

  • NRC (1993) Pesticides in the Diets of Infants and Children. National Academy Press, Washington, DC

    Google Scholar 

  • Olima C, Pablo F, Lim R (1997) Comparative tolerance of three populations of the freshwater shrimp (Paratya australiensis) to the organophosphate pesticide, chlorpyrifos. Bull Environ Contam Toxicol 59:321–328

    Article  CAS  Google Scholar 

  • Pham B, Miranda A, Allinson G, Nugegoda D (2017) Evaluating the non-lethal effects of organophosphorous and carbamate insecticides on the yabby (Cherax destructor) using cholinesterase (AChE, BChE), Glutathione S-Transferase and ATPase as biomarkers. Ecotoxicol Environ Saf 143:283–288

    Article  CAS  Google Scholar 

  • Schäfer RB, Pettigrove V, Rose G, Allinson G, Wightwick A, von der Ohe PC, Shimeta J, Kefford BJ (2011) Effects of pesticides monitored with three sampling methods in 24 sites on macroinvertebrates and microorganisms. Environ Sci Technol 45(4):1665–1672

    Article  Google Scholar 

  • Tahara M, Kubota R, Nakazawa H, Tokunaga H, Nishimura T (2005) Use of cholinesterase activity as an indicator for the effects of combinations of organophosphorus pesticides in water from environmental sources. Water Res 39:5112–5118

    Article  CAS  Google Scholar 

  • Trekels H, Van de Meutter F, Bervoets L, Stoks R (2012) Species-specific responsiveness of four enzymes to endosulfan and predation risk questions their usefulness as general biomarkers. Ecotoxicology 21(268):268–279

    Article  CAS  Google Scholar 

  • Tu HT, Silvestre F, Scippo M-L, Thome J-P, Phuong NT, Kestemont P (2009) Acetylcholinesterase activity as a biomarker of exposure to antibiotics and pesticides in the black tiger shrimp (Penaeus monodon). Ecotoxicol Environ Saf 72:1463–1470

    Article  CAS  Google Scholar 

  • Verro R, Finizio A, Otto S, Vighi M (2008) Predicting pesticide environmental risk in intensive agricultural areas. II: screening level risk assessment of complex mixtures in surface waters. Environ Sci Technol 43:530–537

    Article  Google Scholar 

  • Vighi M et al. (2003) Water quality objectives for mixtures of toxic chemicals: problems and perspectives. Ecotoxicol Environ Saf 54:139–150

    Article  CAS  Google Scholar 

  • Wang Y, Chen C, Zhao X, Wang Q, Qian Y (2015) Assessing joint toxicity of four organophosphate and carbamate insecticides in common carp (Cyprinus carpio) using acetylcholinesterase activity as an endpoint. Pestic Biochem Physiol 122:81–85

    Article  CAS  Google Scholar 

  • WHO (1986) Environmental Health Criteria 63:I; Organophosphorous Insecticides, a General Introduction International Programme on Chemical Safety. World Health Organization, Geneva

    Google Scholar 

  • Xuereb B, Chaumot A, Mons R, Garric J, Geffard O (2009) Acetylcholinesterase activity in Gammarus fossarum (Crustacea Amphipoda): intrinsic variability, reference levels, and a reliable tool for field surveys. Aquat Toxicol 93:225–233

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the 165 scholarship of Vietnam for sponsorship of the PhD scholarship given to BP (no. 5902 QD/BTCTW). BP gratefully acknowledges the support of staff and students in the Ecotoxicology Research Lab, School of Science, RMIT University.

Funding

This work was funded by the College of Science, Engineering and Health, and School of Science, RMIT University.

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Correspondence to Ben Pham.

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This article does contain studies with animals performed by the authors, however juvenile yabbies (juvenile crayfish) do not currently require an approval from an animal ethics committee in Australia.

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Pham, B., Miranda, A., Allinson, G. et al. Assessing interactive mixture toxicity of carbamate and organophosphorus insecticides in the yabby (Cherax destructor). Ecotoxicology 27, 1217–1224 (2018). https://doi.org/10.1007/s10646-018-1973-x

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