Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Toxicity testing of pesticides in zebrafish—a systematic review on chemicals and associated toxicological endpoints

  • 81 Accesses

Abstract

The use of zebrafish (Danio rerio) has arisen as a promising biological platform for toxicity testing of pesticides such as herbicides, insecticides, and fungicides. Therefore, it is relevant to assess the use of zebrafish in models of exposure to investigate the diversity of pesticide-associated toxicity endpoints which have been reported. Thus, this review aimed to assess the recent literature on the use of zebrafish in pesticide toxicity studies to capture data on the types of pesticide used, classes of pesticides, and zebrafish life stages associated with toxicity endpoints and phenotypic observations. A total of 352 articles published between September 2012 and May 2019 were curated. The results show an increased trend in the use of zebrafish for testing the toxicity of pesticides, with a great diversity of pesticides (203) and chemical classes (58) with different applications (41) being used. Furthermore, experimental outcomes could be clustered in 13 toxicity endpoints, mainly developmental toxicity, oxidative stress, and neurotoxicity. Organophosphorus, pyrethroid, azole, and triazine were the most studied classes of pesticides and associated with various toxicity endpoints. Studies frequently opted for early life stages (embryos and larvae). Although there is an evident lack of standardization of nomenclatures and phenotypic alterations, the information gathered here highlights associations between (classes of) pesticides and endpoints, which can be used to relate mechanisms of action specific to certain classes of chemicals.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Abbreviations

AChE:

Acetylcholinesterase

AOP:

Adverse outcome pathway

CAT:

Catalase

DACT:

Diaminochlorotriazine

DDT:

Dichlorodiphenyltrichloroethane

DE:

Deethylatrazine

DIP:

Deisopropylatrazine

EDCs:

Endocrine-disrupting chemicals

EU:

European Union

FET:

Fish Embryo Toxicity Assay

GPx:

Glutathione peroxidase

GST:

Glutathione S-transferase

HC:

High-content

HPA:

Hypothalamic-pituitary-adrenocortical

HPG:

Hypothalamic-pituitary-gonadal

HPT:

Hypothalamic-pituitary-thyroid

HT:

High-throughput

LC50 :

Lethal concentration at which 50% of the population if killed in a given period of time

MS-222:

Tricaine methanesulfonate

NTs:

Neurotransmitters

OECD:

Organisation for Economic Co-operation and Development

OPFRs:

Organophosphate flame retardants

PD:

Parkinson’s disease

POPs:

Persistent organic pollutants

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

ToxCast™:

EPA’s Toxicity Forecaster

US EPA:

United States Environmental Protection Agency

References

  1. Abedi ZH, McKinley WP (1967) Bioassay of captan by zebrafish larvae [20]. Nature 216:1321–1322

  2. Adeyemi JA, da Cunha M-JA, Barbosa F (2015) Teratogenicity, genotoxicity and oxidative stress in zebrafish embryos (Danio rerio) co-exposed to arsenic and atrazine. Comp Biochem Physiol Part C Toxicol Pharmacol 172–173:7–12. https://doi.org/10.1016/j.cbpc.2015.04.001

  3. Almeida DV, Vaz B, Azevedo Figueiredo M et al (2014) Fluorescent transgenic zebrafish as a biosensor for growth-related effects of methyl parathion. Aquat Toxicol 152:147–151. https://doi.org/10.1016/J.AQUATOX.2014.04.001

  4. Altenhofen S, Nabinger DD, Wiprich MT et al (2017) Tebuconazole alters morphological, behavioral and neurochemical parameters in larvae and adult zebrafish (Danio rerio). Chemosphere 180:483–490. https://doi.org/10.1016/j.chemosphere.2017.04.029

  5. Ankley GT, Johnson RD (2004) Small fish models for identifying and assessing the effects of endocrine-disrupting chemicals. ILAR J 45:469–483. https://doi.org/10.1093/ilar.45.4.469

  6. Ankley GT, Gray LE (2013) Cross-species conservation of endocrine pathways: A critical analysis of tier 1 fish and rat screening assays with 12 model chemicals. Environ Toxicol Chem 32:1084–1087. https://doi.org/10.1002/etc.2151

  7. Aragon A, Legradi J, Ballesteros-Gómez A et al (2017) Determination of monoamine neurotransmitters in zebrafish (Danio rerio) by gas chromatography coupled to mass spectrometry with a two-step derivatization. Anal Bioanal Chem 409:2931–2939. https://doi.org/10.1007/s00216-017-0239-4

  8. Armiliato N, Ammar D, Nezzi L et al (2014) Changes in ultrastructure and expression of steroidogenic factor-1 in ovaries of zebrafish Danio rerio exposed to glyphosate. J Toxicol Environ Health A 77:405–414. https://doi.org/10.1080/15287394.2014.880393

  9. Bailey J, Oliveri A, Levin ED (2013) Zebrafish model systems for developmental neurobehavioral toxicology. Birth Defects Res Part C Embryo Today Rev 99:14–23. https://doi.org/10.1002/bdrc.21027

  10. Baumann L, Knörr S, Keiter S et al (2015) Prochloraz causes irreversible masculinization of zebrafish (Danio rerio). Environ Sci Pollut Res Int 22:16417–16422. https://doi.org/10.1007/s11356-014-3486-3

  11. Benford DJ, Hanley AB, Bottrill K et al (2000) Biomarkers as predictive tools in toxicity testing. Altern Lab Anim 28:119–131. https://doi.org/10.1177/026119290002800104

  12. Bhattacharya S, Zhang Q, Carmichael PL et al (2011) Toxicity testing in the 21st century: defining new risk assessment approaches based on perturbation of intracellular toxicity pathways. PLoS One 6:e20887. https://doi.org/10.1371/journal.pone.0020887

  13. Blahová J, Plhalová L, Hostovský M et al (2013) Oxidative stress responses in zebrafish Danio rerio after subchronic exposure to atrazine. Food Chem Toxicol 61:82–85. https://doi.org/10.1016/j.fct.2013.02.041

  14. Blakley B, Brousseau P, Fournier M, Voccia I (1999) Immunotoxicity of pesticides: a review. Toxicol Ind Health 15:119–132. https://doi.org/10.1177/074823379901500110

  15. Boekelheide K, Campion SN (2010) Toxicity testing in the 21st century: using the new toxicity testing paradigm to create a taxonomy of adverse effects. Toxicol Sci 114:20–24. https://doi.org/10.1093/toxsci/kfp307

  16. Bortolotto JW, Cognato GP, Christoff RR et al (2014) Long-term exposure to paraquat alters behavioral parameters and dopamine levels in adult zebrafish (Danio rerio). Zebrafish 11:142–153. https://doi.org/10.1089/zeb.2013.0923

  17. Brander SM, Gabler MK, Fowler NL et al (2016) Pyrethroid pesticides as endocrine disruptors: molecular mechanisms in vertebrates with a focus on fishes. Environ Sci Technol 50:8977–8992. https://doi.org/10.1021/acs.est.6b02253

  18. Brandhorst BP, Corley-Smith GE (2004) Production of haploid and diploid androgenetic zebrafish. In: Germ Cell Protocols. Humana Press, New Jersey, pp 255–270

  19. Bui-Nguyen TM, Baer CE, Lewis JA et al (2015) Dichlorvos exposure results in large scale disruption of energy metabolism in the liver of the zebrafish, Danio rerio. BMC Genomics 16:853. https://doi.org/10.1186/s12864-015-1941-2

  20. Cao C, Wang Q, Jiao F, Zhu G (2016a) Impact of co-exposure with butachlor and triadimefon on thyroid endocrine system in larval zebrafish. Exp Toxicol Pathol 68:463–469. https://doi.org/10.1016/j.etp.2016.07.004

  21. Cao F, Liu X, Wang C et al (2016b) Acute and short-term developmental toxicity of cyhalofop-butyl to zebrafish (Danio rerio). Environ Sci Pollut Res 23:10080–10089. https://doi.org/10.1007/s11356-016-6236-x

  22. Cao F, Zhu L, Li H et al (2016c) Reproductive toxicity of azoxystrobin to adult zebrafish (Danio rerio). Environ Pollut 219:1109–1121. https://doi.org/10.1016/j.envpol.2016.09.015

  23. Capela R, Garric J, Castro LFC, Santos MM (2020) Embryo bioassays with aquatic animals for toxicity testing and hazard assessment of emerging pollutants: A review. Sci Total Environ 705:135740. https://doi.org/10.1016/j.scitotenv.2019.135740

  24. Carson R, Darling L, Darling L (1962) Silent Spring, 1st edn. Houghton Miffin Company.

  25. Castello PR, Drechsel DA, Patel M (2007) Mitochondria are a major source of paraquat-induced reactive oxygen species production in the brain. J Biol Chem 282:14186–14193. https://doi.org/10.1074/jbc.M700827200

  26. Champagne DL, Hoefnagels CCM, de Kloet RE, Richardson MK (2010) Translating rodent behavioral repertoire to zebrafish (Danio rerio): relevance for stress research. Behav Brain Res 214:332–342. https://doi.org/10.1016/J.BBR.2010.06.001

  27. Chang J, Liu S, Zhou S et al (2013) Effects of butachlor on reproduction and hormone levels in adult zebrafish (Danio rerio). Exp Toxicol Pathol 65:205–209. https://doi.org/10.1016/j.etp.2011.08.007

  28. Chen Y, Wang X, Li Y et al (2015) Persistent organic pollutants in matched breast milk and infant faeces samples. Chemosphere 118:309–314. https://doi.org/10.1016/J.CHEMOSPHERE.2014.09.076

  29. Chrustek A, Hołyńska-Iwan I, Dziembowska I et al (2018) Current research on the safety of pyrethroids used as insecticides. Medicina (B Aires) 54:61. https://doi.org/10.3390/medicina54040061

  30. Corsini E, Sokooti M, Galli CL et al (2013) Pesticide induced immunotoxicity in humans: a comprehensive review of the existing evidence. Toxicology 307:123–135. https://doi.org/10.1016/J.TOX.2012.10.009

  31. Costa LG, Galli CL, Murphy SD (eds) (1987) Toxicology of pesticides. Springer, Berlin Heidelberg

  32. Costa LG, Giordano G, Guizzetti M, Vitalone A (2008) Neurotoxicity of pesticides: A brief review. Front Biosci 13:1240–1249

  33. Cowie AM, Sarty KI, Mercer A et al (2017a) Molecular networks related to the immune system and mitochondria are targets for the pesticide dieldrin in the zebrafish (Danio rerio) central nervous system. J Proteome 157:71–82. https://doi.org/10.1016/j.jprot.2017.02.003

  34. Cowie AM, Sarty KI, Mercer A et al (2017b) The pesticide dieldrin disrupts proteins related to oxidative respiration and mitochondrial stress in the central nervous system. Data Br 11:628–633. https://doi.org/10.1016/j.dib.2017.03.008

  35. Crosby EB, Bailey JM, Oliveri AN, Levin ED (2015) Neurobehavioral impairments caused by developmental imidacloprid exposure in zebrafish. Neurotoxicol Teratol 49:81–90

  36. Dach K, Yaghoobi B, Schmuck MR et al (2019) Teratological and behavioral screening of the National Toxicology Program 91-Compound Library in zebrafish (Danio rerio). Toxicol Sci 167:77–91. https://doi.org/10.1093/toxsci/kfy266

  37. Dang Y, Giesy JP, Wang J, Liu C (2015) Dose-dependent compensation responses of the hypothalamic-pituitary-gonadal-liver axis of zebrafish exposed to the fungicide prochloraz. Aquat Toxicol 160:69–75. https://doi.org/10.1016/j.aquatox.2015.01.003

  38. de Brito RL, de Oliveira R, Abe FR et al (2017) Ecotoxicological assessment of glyphosate-based herbicides: effects on different organisms. Environ Toxicol Chem 36:1755–1763. https://doi.org/10.1002/etc.3580

  39. de Esch C, Slieker R, Wolterbeek A et al (2012) Zebrafish as potential model for developmental neurotoxicity testing: a mini review. Neurotoxicol Teratol 34:545–553. https://doi.org/10.1016/J.NTT.2012.08.006

  40. Domingo JL, Bocio A (2007) Levels of PCDD/PCDFs and PCBs in edible marine species and human intake: a literature review. Environ Int 33:397–405. https://doi.org/10.1016/j.envint.2006.12.004

  41. Domingues I, Oliveira R, Soares AMVM, Amorim MJB (2016) Effects of ivermectin on Danio rerio: a multiple endpoint approach: behaviour, weight and subcellular markers. Ecotoxicology 25:491–499. https://doi.org/10.1007/s10646-015-1607-5

  42. Eddins D, Cerutti D, Williams P et al (2010) Zebrafish provide a sensitive model of persisting neurobehavioral effects of developmental chlorpyrifos exposure: comparison with nicotine and pilocarpine effects and relationship to dopamine deficits. Neurotoxicol Teratol 32:99–108. https://doi.org/10.1016/J.NTT.2009.02.005

  43. Eddleston M, Buckley NA, Eyer P, Dawson AH (2008) Management of acute organophosphorus pesticide poisoning. Lancet (London, England) 371:597–607. https://doi.org/10.1016/S0140-6736(07)61202-1

  44. Egbuta C, Lo J, Ghosh D (2014) Mechanism of inhibition of estrogen biosynthesis by azole fungicides. Endocrinology 155:4622–4628. https://doi.org/10.1210/en.2014-1561

  45. FAO (2019) News Article: 2050: A third more mouths to feed. http://www.fao.org/news/story/en/item/35571/icode/. Accessed 9 Jul 2019

  46. Faqi AS, Hoberman A, Lewis E, Stump D (2013) Developmental and Reproductive Toxicology. In: A Comprehensive Guide to Toxicology in Preclinical Drug Development. Elsevier Inc., pp 335–364

  47. Fitzmaurice AG, Rhodes SL, Lulla A et al (2013) Aldehyde dehydrogenase inhibition as a pathogenic mechanism in Parkinson disease. Proc Natl Acad Sci 110:636–641. https://doi.org/10.1073/pnas.1220399110

  48. Gaind N (2016) US grants for zebrafish studies on the rise. Nature. https://doi.org/10.1038/nature.2016.20391

  49. Garry VF, Kelly JT, Sprafka JM et al (1994) Survey of health and use characterization of pesticide appliers in Minnesota. Arch Environ Heal An Int J 49:337–343. https://doi.org/10.1080/00039896.1994.9954984

  50. Glickman AH, Lech JJ (1982) Differential toxicity of trans-permethrin in rainbow trout and mice: II. Role of target organ sensitivity. Toxicol Appl Pharmacol 66:162–171. https://doi.org/10.1016/0041-008X(82)90281-2

  51. Goulart TLS, Boyle RT, Souza MM (2015) Cytotoxicity of the association of pesticides Roundup Transorb® and Furadan 350 SC® on the zebrafish cell line, ZF-L. Toxicol in Vitro 29:1377–1384. https://doi.org/10.1016/j.tiv.2015.06.007

  52. Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957

  53. Groh KJ, Carvalho RN, Chipman JK et al (2015) Development and application of the adverse outcome pathway framework for understanding and predicting chronic toxicity: II. A focus on growth impairment in fish. Chemosphere 120:778–792

  54. Gunnarsson L, Jauhiainen A, Kristiansson E et al (2008) Evolutionary conservation of human drug targets in organisms used for environmental risk assessments. Environ Sci Technol 42:5807–5813. https://doi.org/10.1021/es8005173

  55. Haverinen J, Vornanen M (2016) Deltamethrin is toxic to the fish (crucian carp, Carassius carassius) heart. Pestic Biochem Physiol 129:36–42. https://doi.org/10.1016/J.PESTBP.2015.10.014

  56. Hayasaka D, Korenaga T, Suzuki K et al (2012) Cumulative ecological impacts of two successive annual treatments of imidacloprid and fipronil on aquatic communities of paddy mesocosms. Ecotoxicol Environ Saf 80:355–362. https://doi.org/10.1016/J.ECOENV.2012.04.004

  57. He X, Gao J, Dong T et al (2016) Developmental neurotoxicity of methamidophos in the embryo-larval stages of zebrafish. Int J Environ Res Public Health 14:23. https://doi.org/10.3390/ijerph14010023

  58. Hill AJ, Teraoka H, Heideman W, Peterson RE (2005) Zebrafish as a model vertebrate for investigating chemical toxicity. Toxicol Sci 86:6–19. https://doi.org/10.1093/toxsci/kfi110

  59. Hoppin JA, Umbach DM, Kullman GJ, et al (2007) Pesticides and other agricultural factors associated with self-reported farmer’s lung among farm residents in the Agricultural Health Study. https://doi.org/10.1136/oem.2006.028480

  60. Howe K, Clark MD, Torroja CF et al (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498–503. https://doi.org/10.1038/nature12111

  61. Jia L, Zhang D, Huang H et al (2018a) Triazophos-induced toxicity in zebrafish: miRNA-217 inhibits nup43. Toxicol Res (Camb) 7:913–922. https://doi.org/10.1039/C8TX00065D

  62. Jia M, Wang Y, Teng M et al (2018b) Toxicity and metabolomics study of isocarbophos in adult zebrafish (Danio rerio). Ecotoxicol Environ Saf 163:1–6. https://doi.org/10.1016/J.ECOENV.2018.07.027

  63. Jia W, Mao L, Zhang L et al (2018c) Effects of two strobilurins (azoxystrobin and picoxystrobin) on embryonic development and enzyme activities in juveniles and adult fish livers of zebrafish (Danio rerio). Chemosphere 207:573–580. https://doi.org/10.1016/j.chemosphere.2018.05.138

  64. Jia Z-Q, Liu D, Sheng C-W et al (2018d) Acute toxicity, bioconcentration, elimination and antioxidant effects of fluralaner in zebrafish, Danio rerio. Environ Pollut 232:183–190. https://doi.org/10.1016/j.envpol.2017.09.032

  65. Jiang J, Wu S, Liu X et al (2015a) Effect of acetochlor on transcription of genes associated with oxidative stress, apoptosis, immunotoxicity and endocrine disruption in the early life stage of zebrafish. Environ Toxicol Pharmacol 40:516–523. https://doi.org/10.1016/j.etap.2015.08.005

  66. Jiang J, Wu S, Wang Y et al (2015b) Carbendazim has the potential to induce oxidative stress, apoptosis, immunotoxicity and endocrine disruption during zebrafish larvae development. Toxicol in Vitro 29:1473–1481. https://doi.org/10.1016/j.tiv.2015.06.003

  67. Jin Y, Pan X, Cao L et al (2013) Embryonic exposure to cis-bifenthrin enantioselectively induces the transcription of genes related to oxidative stress, apoptosis and immunotoxicity in zebrafish (Danio rerio). Fish Shellfish Immunol 34:717–723. https://doi.org/10.1016/j.fsi.2012.11.046

  68. Jin Y, Liu Z, Peng T, Fu Z (2015) The toxicity of chlorpyrifos on the early life stage of zebrafish: a survey on the endpoints at development, locomotor behavior, oxidative stress and immunotoxicity. Fish Shellfish Immunol 43:405–414. https://doi.org/10.1016/j.fsi.2015.01.010

  69. Jr JC, Loos JJ (1967) Changed feeding rate of Erachydanio rerio (Hamilton-Buchanan) resulting from exposure to sublethal concentrations of zinc, potassium dichromate, and alkyl benzene sulfonate detergent. Proc Pennsylvania Acad Sci 40:47–52

  70. Juntarawijit C, Juntarawijit Y (2018) Association between diabetes and pesticides: a case-control study among Thai farmers. Environ Health Prev Med 23:3. https://doi.org/10.1186/s12199-018-0692-5

  71. Kais B, Ottermanns R, Scheller F, Braunbeck T (2018) Modification and quantification of in vivo EROD live-imaging with zebrafish (Danio rerio) embryos to detect both induction and inhibition of CYP1A. Sci Total Environ 615:330–347. https://doi.org/10.1016/j.scitotenv.2017.09.257

  72. Kavlock R, Chandler K, Houck K et al (2012) Update on EPA’s ToxCast program: providing high throughput decision support tools for chemical risk management. Chem Res Toxicol 25:1287–1302. https://doi.org/10.1021/tx3000939

  73. Keifer MC, Firestone J (2007) Neurotoxicity of pesticides. J Agromedicine 12:17–25. https://doi.org/10.1300/J096v12n01_03

  74. Klüver N, Vogs C, Altenburger R et al (2016) Development of a general baseline toxicity QSAR model for the fish embryo acute toxicity test. Chemosphere 164:164–173. https://doi.org/10.1016/j.chemosphere.2016.08.079

  75. Krewski D, Westphal M, Al-Zoughool M et al (2011) New directions in toxicity testing. Annu Rev Public Health 32:161–178. https://doi.org/10.1146/annurev-publhealth-031210-101153

  76. Kumar J, Lind PM, Salihovic S et al (2014) Influence of persistent organic pollutants on the complement system in a population-based human sample. Environ Int 71:94–100. https://doi.org/10.1016/J.ENVINT.2014.06.009

  77. Kung TS, Richardson JR, Cooper KR, White LA (2015) Developmental deltamethrin exposure causes persistent changes in dopaminergic gene expression, neurochemistry, and locomotor activity in zebrafish. Toxicol Sci 146:235–243. https://doi.org/10.1093/toxsci/kfv087

  78. Lee D-H, Porta M, Jacobs DR, Vandenberg LN (2014) Chlorinated persistent organic pollutants, obesity, and type 2 diabetes. Endocr Rev 35:557–601. https://doi.org/10.1210/er.2013-1084

  79. Lee YS, Lewis JA, Ippolito DL et al (2016) Repeated exposure to neurotoxic levels of chlorpyrifos alters hippocampal expression of neurotrophins and neuropeptides. Toxicology 340:53–62. https://doi.org/10.1016/J.TOX.2016.01.001

  80. Levin E, Cerutti D (2009) Behavioral Neuroscience of Zebrafish. In: Methods of Behavior Analysis in Neuroscience, 2nd edn. CRC Press/Taylor & Francis, pp 293–310

  81. Li B, Lin J, Pang X et al (2018a) Binary mixtures of alcohol ethoxylates, nonylphenol ethoxylates and pesticides exhibit comparative bioactivity against three pests and toxicological risks to aquatic organisms. Chemosphere 204:44–50. https://doi.org/10.1016/j.chemosphere.2018.04.034

  82. Li H, Cao F, Zhao F et al (2018b) Developmental toxicity, oxidative stress and immunotoxicity induced by three strobilurins (pyraclostrobin, trifloxystrobin and picoxystrobin) in zebrafish embryos. Chemosphere 207:781–790. https://doi.org/10.1016/j.chemosphere.2018.05.146

  83. Li M, Wu Q, Wang Q et al (2018c) Effect of titanium dioxide nanoparticles on the bioavailability and neurotoxicity of cypermethrin in zebrafish larvae. Aquat Toxicol 199:212–219. https://doi.org/10.1016/j.aquatox.2018.03.022

  84. Li B, Liu Y, Zhang P et al (2019a) Selection of organosilicone surfactants for tank-mixed pesticides considering the balance between synergistic effects on pests and environmental risks. Chemosphere 217:591–598. https://doi.org/10.1016/j.chemosphere.2018.11.061

  85. Li M, Liu X, Feng X (2019b) Cardiovascular toxicity and anxiety-like behavior induced by deltamethrin in zebrafish (Danio rerio) larvae. Chemosphere 219:155–164. https://doi.org/10.1016/j.chemosphere.2018.12.011

  86. Li R, Wang H, Mi C et al (2019c) The adverse effect of TCIPP and TCEP on neurodevelopment of zebrafish embryos/larvae. Chemosphere 220:811–817. https://doi.org/10.1016/j.chemosphere.2018.12.198

  87. Li S, Sun Q, Wu Q et al (2019d) Endocrine disrupting effects of tebuconazole on different life stages of zebrafish (Danio rerio). Environ Pollut 249:1049–1059. https://doi.org/10.1016/j.envpol.2019.03.067

  88. Li S, Wu Q, Sun Q et al (2019e) Parental exposure to tebuconazole causes thyroid endocrine disruption in zebrafish and developmental toxicity in offspring. Aquat Toxicol 211:116–123. https://doi.org/10.1016/j.aquatox.2019.04.002

  89. Liang X, Yu L, Gui W, Zhu G (2015) Exposure to difenoconazole causes changes of thyroid hormone and gene expression levels in zebrafish larvae. Environ Toxicol Pharmacol 40:983–987. https://doi.org/10.1016/j.etap.2015.10.005

  90. Liguori I, Russo G, Curcio F et al (2018) Oxidative stress, aging, and diseases. Clin Interv Aging 13:757–772. https://doi.org/10.2147/CIA.S158513

  91. Lim J, Park SH, Jee SH, Park H (2015) Body concentrations of persistent organic pollutants and prostate cancer: a meta-analysis. Environ Sci Pollut Res 22:11275–11284. https://doi.org/10.1007/s11356-015-4315-z

  92. Liu Z, Wang Y, Zhu Z et al (2016a) Atrazine and its main metabolites alter the locomotor activity of larval zebrafish (Danio rerio). Chemosphere 148:163–170. https://doi.org/10.1016/j.chemosphere.2016.01.007

  93. Liu N, Dong F, Xu J et al (2016b) Chiral bioaccumulation behavior of tebuconazole in the zebrafish (Danio rerio). Ecotoxicol Environ Saf 126:78–84. https://doi.org/10.1016/j.ecoenv.2015.12.007

  94. Liu H, Chu T, Chen L et al (2017a) In vivo cardiovascular toxicity induced by acetochlor in zebrafish larvae. Chemosphere 181:600–608. https://doi.org/10.1016/j.chemosphere.2017.04.090

  95. Liu H, Chu T, Chen L et al (2017b) The cardiovascular toxicity of triadimefon in early life stage of zebrafish and potential implications to human health. Environ Pollut 231:1093–1103. https://doi.org/10.1016/j.envpol.2017.05.072

  96. Liu Z, Fu Z, Jin Y (2017c) Immunotoxic effects of atrazine and its main metabolites at environmental relevant concentrations on larval zebrafish ( Danio rerio ). Chemosphere 166:212–220. https://doi.org/10.1016/j.chemosphere.2016.09.100

  97. Lopes FM, Varela Junior AS, Corcini CD et al (2014) Effect of glyphosate on the sperm quality of zebrafish Danio rerio. Aquat Toxicol 155:322–326. https://doi.org/10.1016/j.aquatox.2014.07.006

  98. Lor Y, Revak A, Weigand J et al (2015) Juvenile exposure to vinclozolin shifts sex ratios and impairs reproductive capacity of zebrafish. Reprod Toxicol 58:111–118. https://doi.org/10.1016/j.reprotox.2015.09.003

  99. Lucki I (1998) The spectrum of behaviors influenced by serotonin. Biol Psychiatry 44:151–162

  100. Lulla A, Barnhill L, Bitan G et al (2016) Neurotoxicity of the Parkinson disease-associated pesticide Ziram is Synuclein-dependent in zebrafish embryos. Environ Health Perspect 124:1766–1775. https://doi.org/10.1289/EHP141

  101. Lungu-Mitea S, Oskarsson A, Lundqvist J (2018) Development of an oxidative stress in vitro assay in zebrafish (Danio rerio) cell lines. Sci Rep 8:12380. https://doi.org/10.1038/s41598-018-30880-1

  102. Lushchak VI, Matviishyn TM, Husak VV et al (2018) Pesticide toxicity: a mechanistic approach. EXCLI J 17:1101–1136. https://doi.org/10.17179/excli2018-1710

  103. Ma X, Li H, Xiong J et al (2019) Developmental toxicity of a neonicotinoid insecticide, acetamiprid to zebrafish embryos. J Agric Food Chem 67:2429–2436. https://doi.org/10.1021/acs.jafc.8b05373

  104. Manjunatha B, Philip GH (2016) Reproductive toxicity of chlorpyrifos tested in zebrafish (Danio rerio). Toxicol Ind Health 32:1808–1816. https://doi.org/10.1177/0748233715589445

  105. Mathias JR, Saxena MT, Mumm JS (2012) Advances in zebrafish chemical screening technologies. Future Med Chem 4(14):1811–1822. https://doi.org/10.4155/fmc.12.115

  106. McKinlay R, Plant JA, Bell JNB, Voulvoulis N (2008) Endocrine disrupting pesticides: implications for risk assessment. Environ Int 34:168–183. https://doi.org/10.1016/J.ENVINT.2007.07.013

  107. Mesnage R, Antoniou MN (2018) Ignoring adjuvant toxicity falsifies the safety profile of commercial pesticides. Front Public Health 5. https://doi.org/10.3389/fpubh.2017.00361

  108. Mikeš O, Čupr P, Kohút L et al (2012) Fifteen years of monitoring of POPs in the breast milk, Czech Republic, 1994–2009: trends and factors. Environ Sci Pollut Res 19:1936–1943. https://doi.org/10.1007/s11356-012-0798-z

  109. Mirkin IR, Anderson HA, Hanrahan L et al (1990) Changes in T-lymphocyte distribution associated with ingestion of aldicarb-contaminated drinking water: a follow-up study. Environ Res 51:35–50. https://doi.org/10.1016/S0013-9351(05)80181-1

  110. Mnif W, Hassine AIH, Bouaziz A et al (2011) Effect of endocrine disruptor pesticides: a review. Int J Environ Res Public Health 8:2265–2303. https://doi.org/10.3390/ijerph8062265

  111. Mostafalou S, Abdollahi M (2017) Pesticides: an update of human exposure and toxicity. Arch Toxicol 91:549–599. https://doi.org/10.1007/s00204-016-1849-x

  112. Mu X, Pang S, Sun X et al (2013) Evaluation of acute and developmental effects of difenoconazole via multiple stage zebrafish assays. Environ Pollut 175:147–157. https://doi.org/10.1016/j.envpol.2012.12.029

  113. Mu X, Chai T, Wang K et al (2016) The developmental effect of difenoconazole on zebrafish embryos: a mechanism research. Environ Pollut 212:18–26. https://doi.org/10.1016/j.envpol.2016.01.035

  114. Mukhopadhyay D, Priya P, Chattopadhyay A (2015) Sodium fluoride affects zebrafish behaviour and alters mRNA expressions of biomarker genes in the brain: role of Nrf2/Keap1. Environ Toxicol Pharmacol 40:352–359. https://doi.org/10.1016/j.etap.2015.07.003

  115. Nunes ME, Müller TE, Braga MM et al (2017) Chronic treatment with Paraquat induces brain injury, changes in antioxidant defenses system, and modulates behavioral functions in zebrafish. Mol Neurobiol 54:3925–3934. https://doi.org/10.1007/s12035-016-9919-x

  116. OECD (2013) Test No. 236: fish embryo acute toxicity (FET) test. OECD

  117. Oliveira R, Grisolia CK, Monteiro MS et al (2016) Multilevel assessment of ivermectin effects using different zebrafish life stages. Comp Biochem Physiol Part C Toxicol Pharmacol 187:50–61. https://doi.org/10.1016/j.cbpc.2016.04.004

  118. Padilla S, Corum D, Padnos B et al (2012) Zebrafish developmental screening of the ToxCast™ phase I chemical library. Reprod Toxicol 33:174–187. https://doi.org/10.1016/J.REPROTOX.2011.10.018

  119. Pamanji R, Bethu MS, Yashwanth B et al (2015a) Developmental toxic effects of monocrotophos, an organophosphorous pesticide, on zebrafish (Danio rerio) embryos. Environ Sci Pollut Res 22:7744–7753. https://doi.org/10.1007/s11356-015-4120-8

  120. Pamanji R, Yashwanth B, Bethu MS et al (2015b) Toxicity effects of profenofos on embryonic and larval development of zebrafish (Danio rerio). Environ Toxicol Pharmacol 39:887–897. https://doi.org/10.1016/j.etap.2015.02.020

  121. Pamanji R, Yashwanth B, Venkateswara Rao J (2016) Profenofos induced biochemical alterations and in silico modelling of hatching enzyme, ZHE1 in zebrafish (Danio rerio) embryos. Environ Toxicol Pharmacol 45:123–131. https://doi.org/10.1016/J.ETAP.2016.05.027

  122. Panetto OS, Gomes HF, Fraga Gomes DS et al (2019) The effects of Roundup® in embryo development and energy metabolism of the zebrafish (Danio rerio). Comp Biochem Physiol Part C Toxicol Pharmacol 222:74–81. https://doi.org/10.1016/j.cbpc.2019.04.007

  123. Pereira AG, Jaramillo ML, Remor AP et al (2018) Low-concentration exposure to glyphosate-based herbicide modulates the complexes of the mitochondrial respiratory chain and induces mitochondrial hyperpolarization in the Danio rerio brain. Chemosphere 209:353–362. https://doi.org/10.1016/j.chemosphere.2018.06.075

  124. Pérez J, Domingues I, Monteiro M et al (2013) Synergistic effects caused by atrazine and terbuthylazine on chlorpyrifos toxicity to early-life stages of the zebrafish Danio rerio. Environ Sci Pollut Res Int 20:4671–4680. https://doi.org/10.1007/s11356-012-1443-6

  125. Perez-Rodriguez V, Souders CL, Tischuk C, Martyniuk CJ (2019) Tebuconazole reduces basal oxidative respiration and promotes anxiolytic responses and hypoactivity in early-staged zebrafish (Danio rerio). Comp Biochem Physiol Part C Toxicol Pharmacol 217:87–97. https://doi.org/10.1016/j.cbpc.2018.11.017

  126. Popp J, Pető K, Nagy J (2013) Pesticide productivity and food security. A review. Agron Sustain Dev 33:243–255. https://doi.org/10.1007/s13593-012-0105-x

  127. Qian L, Qi S, Cao F et al (2019a) Effects of penthiopyrad on the development and behaviour of zebrafish in early-life stages. Chemosphere 214:184–194. https://doi.org/10.1016/j.chemosphere.2018.09.117

  128. Qian L, Zhang J, Chen X et al (2019b) Toxic effects of boscalid in adult zebrafish (Danio rerio) on carbohydrate and lipid metabolism. Environ Pollut 247:775–782. https://doi.org/10.1016/j.envpol.2019.01.054

  129. Qian Y, Ji C, Yue S, Zhao M (2019c) Exposure of low-dose fipronil enantioselectively induced anxiety-like behavior associated with DNA methylation changes in embryonic and larval zebrafish. Environ Pollut 249:362–371. https://doi.org/10.1016/j.envpol.2019.03.038

  130. Qiu L, Jia K, Huang L et al (2019) Hepatotoxicity of tricyclazole in zebrafish (Danio rerio). Chemosphere 232:171–179. https://doi.org/10.1016/j.chemosphere.2019.05.159

  131. Raftery TD, Volz DC (2015) Abamectin induces rapid and reversible hypoactivity within early zebrafish embryos. Neurotoxicol Teratol 49:10–18. https://doi.org/10.1016/j.ntt.2015.02.006

  132. Raftery TD, Isales GM, Yozzo KL, Volz DC (2014) High-content screening assay for identification of chemicals impacting spontaneous activity in zebrafish embryos. Environ Sci Technol 48:804–810. https://doi.org/10.1021/es404322p

  133. Sanchez-Bayo F, Goka K (2006) Ecological effects of the insecticide imidacloprid and a pollutant from antidandruff shampoo in experimental rice fields. Environ Toxicol Chem 25:1677–1687

  134. Sánchez-Bayo F, Goulson D, Pennacchio F et al (2016) Are bee diseases linked to pesticides? — a brief review. Environ Int 89–90:7–11. https://doi.org/10.1016/J.ENVINT.2016.01.009

  135. Schmidel AJ, Assmann KL, Werlang CC et al (2014) Subchronic atrazine exposure changes defensive behaviour profile and disrupts brain acetylcholinesterase activity of zebrafish. Neurotoxicol Teratol 44:62–69. https://doi.org/10.1016/j.ntt.2014.05.006

  136. Schoeters G, Hoogenboom R (2006) Contamination of free-range chicken eggs with dioxins and dioxin-like polychlorinated biphenyls. Mol Nutr Food Res 50:908–914. https://doi.org/10.1002/mnfr.200500201

  137. Scholz S, Fischer S, Gündel U et al (2008) The zebrafish embryo model in environmental risk assessment—applications beyond acute toxicity testing. Environ Sci Pollut Res 15:394–404. https://doi.org/10.1007/s11356-008-0018-z

  138. Shahid M, Takamiya M, Stegmaier J et al (2016) Zebrafish biosensor for toxicant induced muscle hyperactivity. Sci Rep 6:23768. https://doi.org/10.1038/srep23768

  139. Soares MP, Jesus F, Almeida AR et al (2017) Endemic shrimp Macrobrachium pantanalense as a test species to assess potential contamination by pesticides in Pantanal (Brazil). Chemosphere 168:1082–1092. https://doi.org/10.1016/j.chemosphere.2016.10.100

  140. Sobanska M, Scholz S, Nyman A-M et al (2018) Applicability of the fish embryo acute toxicity (FET) test (OECD 236) in the regulatory context of Registration, Evaluation, Authorisation, and Restriction of Chemicals (REACH). Environ Toxicol Chem 37:657–670. https://doi.org/10.1002/etc.4055

  141. Spitsbergen JM, Kent ML (2003) The state of the art of the zebrafish model for toxicology and toxicologic pathology research—advantages and current limitations. Toxicol Pathol 31:62–87. https://doi.org/10.1080/01926230390174959

  142. Stanton MF (1965) Diethylnitrosamine-induced hepatic degeneration and neoplasia in the aquarium fish, Brachydanio rerio. JNCI J Natl Cancer Inst 34:117–130. https://doi.org/10.1093/jnci/34.1.117

  143. Stanton MF (1966) Hepatic neoplasms of aquarium fish exposed to Cycas cercinalis. Fed Proc 26:661

  144. Strähle U, Scholz S, Geisler R et al (2012) Zebrafish embryos as an alternative to animal experiments--a commentary on the definition of the onset of protected life stages in animal welfare regulations. Reprod Toxicol 33:128–132. https://doi.org/10.1016/j.reprotox.2011.06.121

  145. Sulukan E, Köktürk M, Ceylan H et al (2017) An approach to clarify the effect mechanism of glyphosate on body malformations during embryonic development of zebrafish ( Daino rerio ). Chemosphere 180:77–85. https://doi.org/10.1016/j.chemosphere.2017.04.018

  146. Sun L, Xu W, Peng T et al (2016) Developmental exposure of zebrafish larvae to organophosphate flame retardants causes neurotoxicity. Neurotoxicol Teratol 55:16–22. https://doi.org/10.1016/j.ntt.2016.03.003

  147. Teng M, Qi S, Zhu W et al (2018a) Effects of the bioconcentration and parental transfer of environmentally relevant concentrations of difenoconazole on endocrine disruption in zebrafish (Danio rerio). Environ Pollut 233:208–217. https://doi.org/10.1016/j.envpol.2017.10.063

  148. Teng M, Zhu W, Wang D et al (2018b) Acute exposure of zebrafish embryo (Danio rerio) to flutolanil reveals its developmental mechanism of toxicity via disrupting the thyroid system and metabolism. Environ Pollut 242:1157–1165. https://doi.org/10.1016/j.envpol.2018.07.092

  149. Teng M, Zhu W, Wang D et al (2018c) Metabolomics and transcriptomics reveal the toxicity of difenoconazole to the early life stages of zebrafish ( Danio rerio ). Aquat Toxicol 194:112–120. https://doi.org/10.1016/j.aquatox.2017.11.009

  150. Törnkvist A, Glynn A, Aune M et al (2011) PCDD/F, PCB, PBDE, HBCD and chlorinated pesticides in a Swedish market basket from 2005 – levels and dietary intake estimations. Chemosphere 83:193–199. https://doi.org/10.1016/J.CHEMOSPHERE.2010.12.042

  151. Tu W, Niu L, Liu W, Xu C (2013) Embryonic exposure to butachlor in zebrafish (Danio rerio): endocrine disruption, developmental toxicity and immunotoxicity. Ecotoxicol Environ Saf 89:189–195. https://doi.org/10.1016/j.ecoenv.2012.11.031

  152. Tu W, Xu C, Jin Y et al (2016a) Permethrin is a potential thyroid-disrupting chemical: in vivo and in silico envidence. Aquat Toxicol 175:39–46. https://doi.org/10.1016/j.aquatox.2016.03.006

  153. Tu W, Xu C, Lu B et al (2016b) Acute exposure to synthetic pyrethroids causes bioconcentration and disruption of the hypothalamus–pituitary–thyroid axis in zebrafish embryos. Sci Total Environ 542:876–885. https://doi.org/10.1016/j.scitotenv.2015.10.131

  154. Tufi S, Leonards P, Lamoree M et al (2016) Changes in neurotransmitter profiles during early zebrafish (Danio rerio) development and after pesticide exposure. Environ Sci Technol 50:3222–3230. https://doi.org/10.1021/acs.est.5b05665

  155. Uren Webster TM, Laing LV, Florance H, Santos EM (2014) Effects of Glyphosate and its Formulation, Roundup, on Reproduction in Zebrafish (Danio rerio). Environmental Science & Technology 48:1271–1279. https://doi.org/10.1021/es404258h

  156. US EPA (1972) DDT Ban Takes Effect. https://archive.epa.gov/epa/aboutepa/ddt-ban-takes-effect.html. Accessed 8 Feb 2020

  157. US EPA (1999) Guidance for identifying pesticide chemicals and other substances that have a common mechanism of toxicity. https://www.epa.gov/sites/production/files/2015-07/documents/guide-2-identify-pest-chem_0.pdf. Accessed 8 Feb 2020

  158. US EPA (2017) About Pesticide Registration. https://www.epa.gov/pesticide-registration/about-pesticide-registration. Accessed 23 Apr 2018

  159. US EPA  (2016) Pesticides Industry Sales and Usage 2008–2012 Market Estimates. https://www.epa.gov/sites/production/files/2015-10/documents/market_estimates2007.pdf. Accessed 23 Apr 2018

  160. Velasques RR, Sandrini JZ, da Rosa CE (2016) Roundup ® in zebrafish: effects on oxidative status and gene expression. Zebrafish 13:432–441. https://doi.org/10.1089/zeb.2016.1259

  161. Wang Y, Lv L, Yu Y et al (2017a) Single and joint toxic effects of five selected pesticides on the early life stages of zebrafish (Danio rerio). Chemosphere 170:61–67. https://doi.org/10.1016/j.chemosphere.2016.12.025

  162. Wang Y, Yang G, Dai D et al (2017b) Individual and mixture effects of five agricultural pesticides on zebrafish (Danio rerio) larvae. Environ Sci Pollut Res 24:4528–4536. https://doi.org/10.1007/s11356-016-8205-9

  163. Wang Y, Liu W, Yang J et al (2017c) Parkinson’s disease-like motor and non-motor symptoms in rotenone-treated zebrafish. Neurotoxicology 58:103–109. https://doi.org/10.1016/j.neuro.2016.11.006

  164. Wang Y, Teng M, Wang D et al (2017d) Enantioselective bioaccumulation following exposure of adult zebrafish ( Danio rerio ) to epoxiconazole and its effects on metabolomic profile as well as genes expression. Environ Pollut 229:264–271. https://doi.org/10.1016/j.envpol.2017.05.087

  165. Wang H, Zhou L, Liao X et al (2019a) Toxic effects of oxine-copper on development and behavior in the embryo-larval stages of zebrafish. Aquat Toxicol 210:242–250. https://doi.org/10.1016/j.aquatox.2019.02.020

  166. Wang X, Shen M, Zhou J, Jin Y (2019b) Chlorpyrifos disturbs hepatic metabolism associated with oxidative stress and gut microbiota dysbiosis in adult zebrafish. Comp Biochem Physiol Part C Toxicol Pharmacol 216:19–28. https://doi.org/10.1016/j.cbpc.2018.11.010

  167. Watson FL, Schmidt H, Turman ZK et al (2014) Organophosphate pesticides induce morphological abnormalities and decrease locomotor activity and heart rate in Danio rerio and Xenopus laevis. Environ Toxicol Chem 33:1337–1345. https://doi.org/10.1002/etc.2559

  168. Weber R, Gaus C, Tysklind M et al (2008) Dioxin- and POP-contaminated sites—contemporary and future relevance and challenges. Environ Sci Pollut Res 15:363–393. https://doi.org/10.1007/s11356-008-0024-1

  169. Weiner ML, Kotkoskie LA (2000) Excipient toxicity and safety. M. Dekker 

  170. Wirbisky SE, Weber GJ, Sepúlveda MS et al (2015) Developmental origins of neurotransmitter and transcriptome alterations in adult female zebrafish exposed to atrazine during embryogenesis. Toxicology 333:156–167. https://doi.org/10.1016/j.tox.2015.04.016

  171. Wu S, Ji G, Liu J et al (2016a) TBBPA induces developmental toxicity, oxidative stress, and apoptosis in embryos and zebrafish larvae (Danio rerio). Environ Toxicol 31:1241–1249. https://doi.org/10.1002/tox.22131

  172. Wu W, Hai Y, Chen L et al (2016b) Deguelin-induced blockade of PI3K/protein kinase B/MAP kinase signaling in zebrafish and breast cancer cell lines is mediated by down-regulation of fibroblast growth factor receptor 4 activity. Pharmacol Res Perspect 4:e00212. https://doi.org/10.1002/prp2.212

  173. Yan S, Wang J, Zhu L et al (2015) Toxic effects of nitenpyram on antioxidant enzyme system and DNA in zebrafish (Danio rerio) livers. Ecotoxicol Environ Saf 122:54–60. https://doi.org/10.1016/j.ecoenv.2015.06.030

  174. Yan L, Gong C, Zhang X et al (2016a) Perturbation of metabonome of embryo/larvae zebrafish after exposure to fipronil. Environ Toxicol Pharmacol 48:39–45. https://doi.org/10.1016/j.etap.2016.10.002

  175. Yan SH, Wang JH, Zhu LS et al (2016b) Thiamethoxam induces oxidative stress and antioxidant response in zebrafish (Danio Rerio) livers. Environ Toxicol 31:2006–2015. https://doi.org/10.1002/tox.22201

  176. Yan SH, Wang JH, Zhu LS et al (2016c) Thiamethoxam induces oxidative stress and antioxidant response in zebrafish ( D anio R erio ) livers. Environ Toxicol 31:2006–2015. https://doi.org/10.1002/tox.22201

  177. Yang Y, Ma H, Zhou J et al (2014) Joint toxicity of permethrin and cypermethrin at sublethal concentrations to the embryo-larval zebrafish. Chemosphere 96:146–154. https://doi.org/10.1016/j.chemosphere.2013.10.014

  178. Yang M, Hu J, Li S et al (2016a) Thyroid endocrine disruption of acetochlor on zebrafish ( Danio rerio ) larvae. J Appl Toxicol 36:844–852. https://doi.org/10.1002/jat.3230

  179. Yang Y, Liu W, Mu X et al (2016b) Biological response of zebrafish embryos after short-term exposure to thifluzamide. Sci Rep 6:38485. https://doi.org/10.1038/srep38485

  180. Yang Y, Qi S, Chen J et al (2016c) Toxic effects of bromothalonil and flutolanil on multiple developmental stages in zebrafish. Bull Environ Contam Toxicol 97:91–97. https://doi.org/10.1007/s00128-016-1833-4

  181. Yang Y, Qi S, Wang D et al (2016d) Toxic effects of thifluzamide on zebrafish (Danio rerio). J Hazard Mater 307:127–136. https://doi.org/10.1016/j.jhazmat.2015.12.055

  182. Yang Y, Ye X, He B, Liu J (2016e) Cadmium potentiates toxicity of cypermethrin in zebrafish. Environ Toxicol Chem 35:435–445. https://doi.org/10.1002/etc.3200

  183. Yang M, Ren B, Qiao L et al (2018a) Behavior responses of zebrafish (Danio rerio) to aquatic environmental stresses in the characteristic of circadian rhythms. Chemosphere 210:129–138. https://doi.org/10.1016/j.chemosphere.2018.07.018

  184. Yang X, Li S, Wang Z et al (2018b) Constraining the teratogenicity of pesticide pollution by a synthetic nanoreceptor. Chem - An Asian J 13:41–45. https://doi.org/10.1002/asia.201701527

  185. Yang Y, Dong F, Liu X et al (2018c) Thifluzamide affects lipid metabolism in zebrafish (Danio reio). Sci Total Environ 633:1227–1236. https://doi.org/10.1016/j.scitotenv.2018.03.302

  186. Yashwanth B, Pamanji R, Rao JV (2016) Toxicomorphomics and toxicokinetics of quinalphos on embryonic development of zebrafish ( Danio rerio ) and its binding affinity towards hatching enzyme, ZHE1. Aquat Toxicol 180:155–163. https://doi.org/10.1016/j.aquatox.2016.09.018

  187. Yu K, Li G, Feng W et al (2015) Chlorpyrifos is estrogenic and alters embryonic hatching, cell proliferation and apoptosis in zebrafish. Chem Biol Interact 239:26–33. https://doi.org/10.1016/j.cbi.2015.06.010

  188. Zhang X, Gao L, Yang K et al (2013) Monocrotophos pesticide modulates the expression of sexual differentiation genes and causes phenotypic feminization in zebrafish (Danio rerio). Comp Biochem Physiol Part C Toxicol Pharmacol 157:33–40. https://doi.org/10.1016/J.CBPC.2012.09.004

  189. Zhang C, Wang J, Zhang S et al (2017a) Acute and subchronic toxicity of pyraclostrobin in zebrafish (Danio rerio). Chemosphere 188:510–516. https://doi.org/10.1016/j.chemosphere.2017.09.025

  190. Zhang J, Liu L, Ren L et al (2017b) The single and joint toxicity effects of chlorpyrifos and beta-cypermethrin in zebrafish (Danio rerio) early life stages. J Hazard Mater 334:121–131. https://doi.org/10.1016/j.jhazmat.2017.03.055

  191. Zhang Q, Zhang Y, Du J, Zhao M (2017c) Environmentally relevant levels of λ-cyhalothrin, fenvalerate, and permethrin cause developmental toxicity and disrupt endocrine system in zebrafish (Danio rerio) embryo. Chemosphere 185:1173–1180. https://doi.org/10.1016/j.chemosphere.2017.07.091

  192. Zhang S, Xu J, Kuang X et al (2017d) Biological impacts of glyphosate on morphology, embryo biomechanics and larval behavior in zebrafish ( Danio rerio ). Chemosphere 181:270–280. https://doi.org/10.1016/j.chemosphere.2017.04.094

  193. Zhang T, Yang M, Pan H et al (2017e) Does time difference of the acetylcholinesterase (AChE) inhibition in different tissues exist? A case study of zebra fish ( Danio rerio ) exposed to cadmium chloride and deltamethrin. Chemosphere 168:908–916. https://doi.org/10.1016/j.chemosphere.2016.10.119

  194. Zhang Y, Han L, He Q et al (2017f) A rapid assessment for predicting drug-induced hepatotoxicity using zebrafish. J Pharmacol Toxicol Methods 84:102–110. https://doi.org/10.1016/j.vascn.2016.12.002

  195. Zhang J, Qian L, Teng M et al (2019a) The lipid metabolism alteration of three spirocyclic tetramic acids on zebrafish (Danio rerio) embryos. Environ Pollut 248:715–725. https://doi.org/10.1016/j.envpol.2019.02.035

  196. Zhang R, Pan Z, Wang X et al (2019b) Short-term propamocarb exposure induces hepatic metabolism disorder associated with gut microbiota dysbiosis in adult male zebrafish. Acta Biochim Biophys Sin Shanghai 51:88–96. https://doi.org/10.1093/abbs/gmy153

  197. Zhou Y, Wang F, Wan J et al (2017) Ecotoxicological bioassays of sediment leachates in a river bed flanked by decommissioned pesticide plants in Nantong City, East China. Environ Sci Pollut Res Int 24:8541–8550. https://doi.org/10.1007/s11356-016-8307-4

  198. Zhuang S, Zhang Z, Zhang W et al (2015) Enantioselective developmental toxicity and immunotoxicity of pyraclofos toward zebrafish (Danio rerio). Aquat Toxicol 159:119–126. https://doi.org/10.1016/j.aquatox.2014.12.006

  199. Zoupa M, Machera K (2017) Zebrafish as an alternative vertebrate model for investigating developmental toxicity—the triadimefon example. Int J Mol Sci 18:817. https://doi.org/10.3390/ijms18040817

Download references

Acknowledgments

We thank to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil, for supporting this research with grants and scholarships, and to Ms. Marta Silva Muniz for contributing with revision of the English manuscript.

Funding

Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil, grant number 461182-9.

Author information

I.F.S.G., T.M.S., L.R.V., F.C.M., A.P.N., and D.F.F. designed and conducted the literature review and wrote the manuscript. All authors approved the submitted version.

Correspondence to Terezinha Maria Souza or Davi Felipe Farias.

Ethics declarations

Conflict of interestThe authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Highlights

- The zebrafish is being increasingly used for testing the toxicity of pesticides.

- Thirteen pesticide-associated toxicity endpoints in zebrafish were documented.

- Developmental toxicity was the endpoint most reported across studies.

- Studies greatly opted for early zebrafish life stages (embryos and larvae).

- There is an evident lack of standardization of nomenclatures in zebrafish testing.

Responsible editor: Philippe Garrigues

Electronic supplementary material

ESM 1

(DOCX 4.00 mb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gonçalves, Í.F.S., Souza, T.M., Vieira, L.R. et al. Toxicity testing of pesticides in zebrafish—a systematic review on chemicals and associated toxicological endpoints. Environ Sci Pollut Res (2020). https://doi.org/10.1007/s11356-020-07902-5

Download citation

Keywords

  • Danio rerio
  • Fungicide
  • Herbicide
  • Insecticide
  • Organophosphorus
  • Pesticide toxicity
  • Toxicity endpoints
  • Zebrafish embryos