Toxicity and effects on anuran tadpole metamorphosis of the anthranilic diamide insecticides chlorantraniliprole and cyantraniliprole

References

• Barry, J. D., H. E. Portillo, I. Billy Annan, R. A. Cameron, D. G. Clagg, R. F. Dietrich, L. J. Watson, R. M. Leighty, D. L. Ryan, J. A. McMillan, et al. 2014. Movement of cyantraniliprole in plants after foliar applications and its impact on the control of sucking and chewing insects. Pest. Manag. Sci. 71:395–403. doi:10.1002/ps.3816.
   PubMed Web of Science ®Google Scholar
• Bentley, K. S., L. J. Fletcher, and M. D.Woodward. 2010. “Chlorantraniliprole: An insecticide of the anthranilic diamide class.” Hayes’ Handbook. Pest. Toxicol, edited by Krieger Robert, 2231–2242. 3rd ed. Academic Press
   Google Scholar
• Brodeur, J. C., M. J. Damonte, D. E. Rojas, D. Cristos, C. Vargas, M. B. Poliserpi, and A. E. Andriulo. 2022. Concentration of current-use pesticides in frogs from the Pampa región and correlation of mixture toxicity index with biological effects. Environ. Res. 204:112354. doi:10.1016/j.envres.2021.112354.
   PubMed Web of Science ®Google Scholar
• Brodeur, J. C., and S. V. D. Fonseca Peña. 2023. Effects of the neonicotinoid insecticides thiamethoxam and imidacloprid on metamorphosis of the toad Rhinella arenarum at environmentally-relevant concentrations. J. Toxicol. Environ. Health Part A 86:435–45. doi:10.1080/15287394.2023.2213259.
   Web of Science ®Google Scholar
• Brodeur, J. C., A. Sassone, G. N. Hermida, and N. Codugnello. 2013. Environmentally-relevant concentrations of atrazine induce non-monotonic acceleration of developmental rate and increased size at metamorphosis in Rhinella arenarum tadpoles. Ecotoxicol. Environ. Saf. 92:10–17. doi:10.1016/j.ecoenv.2013.01.019.
   PubMed Web of Science ®Google Scholar
• Brodeur J. C., R. P. Suarez, G. S. Natale, A. E. Ronco, and M. Elena Zaccagnini. 2011. “Reduced body condition and enzymatic alterations in frogs inhabiting intensive crop production areas.” Ecotoxicology and Environmental Safety 74 (5): 1370–1380. doi:10.1016/j.ecoenv.2011.04.024.
   PubMed Web of Science ®Google Scholar
• Brodeur, J. C., G. Svartz, C. S. Perez-Coll, D. J. G. Marino, and J. Herkovits. 2009. Comparative susceptibility to atrazine of three developmental stages of Rhinella arenarum and influence on metamorphosis: Non-monotonous acceleration of the time to climax and delayed tail resorption. Aquat. Toxicol. 91:161–70. doi:10.1016/j.aquatox.2008.07.003.
   PubMed Web of Science ®Google Scholar
• Brodeur, J. C., and J. Vera Candioti. 2017. Impacts of agriculture and pesticides on amphibian terrestrial life stages: Potential biomonitor/bioindicator species for the pampa region of Argentina. In Ecotoxicology and genotoxicology - non-traditional terrestrial models. M. L. Larramendy ed., pp. 163–94, Royal Society of Chemistry: London. ISBN: 9781.782628118. doi:10.1039/9781788010573-00163.782628118.
   Google Scholar
• Brodeur, J. C., K. B. Woodburn, and G. M. Glecka. 2005. Potentiation of the vitellogenic response to 17α‐ethinylestradiol by cortisol in the fathead minnow Pimephales promelas. Environ. Toxicol. Chem. 24:1125–32. doi:10.1897/04-309R.1.
   PubMed Web of Science ®Google Scholar
• Brown, D. B., and L. Cai. 2007. Amphibian metamorphosis. Dev. Biol. 306:20–33. doi:10.1016/j.ydbio.2007.03.021.
   PubMed Web of Science ®Google Scholar
• CDPR. 2019. Surface water for pesticides in agricultural areas in the central coast and Southern California. California Dep. Pest. Reg. 6:1–25.
   Google Scholar
• Cheron, M., and F. Brischou. 2020. Aminomethylphosphonic acid alters amphibian embryonic development at environmental concentrations. Environ. Res. 190:109944. doi:10.1016/j.envres.2020.109944.
   PubMedGoogle Scholar
• Cordova, D., E. A. Benner, M. D. Sacher, J. J. Rauh, J. S. Sopa, G. P. Lahm, T. P. Selby, T. M. Stevenson, L. Flexner, S. Gutteridge, et al. 2006. Anthranilic diamides: A new class of insecticides with a novel mode of action, ryanodine receptor activation. Pest. Biochem. Physiol 84:196–214. doi:10.1016/j.pestbp.2005.07.005.
   Web of Science ®Google Scholar
• Denver, R. J. 2021. Stress hormones mediate developmental plasticity in vertebrates with complex life cycles. Neurobiol. Stress 14:100301. doi:10.1016/j.ynstr.2021.100301.
   PubMed Web of Science ®Google Scholar
• Elfikrie, N., Y. B. Ho, S. Z. Zaidon, H. Juahir, and E. S. S. Tan. 2020. Occurrence of pesticides in surface water, pesticides removal efficiency in drinking water treatment plant and potential health risk to consumers in Tengi River Basin, Malaysia. Sci. Total Environ. 712:136540. doi:10.1016/j.scitotenv.2020.136540.
   PubMed Web of Science ®Google Scholar
• European Food Safety Authority (EFSA). 2013. Conclusion on the peer review of the pesticide risk assessment of the active substance chlorantraniliprole. Efsa. J 11: 3143. doi:10.2903/j.efsa.2013.3143.
   Google Scholar
• European Food Safety Authority (EFSA). 2014. Conclusion on the peer review of the pesticide risk assessment of the active substance cyantraniliprole. Efsa. J 12: 3814. doi:10.2903/j.efsa.2014.3814.
   Google Scholar
• Fonseca Peña, S. V. D., G. S. Natale, and J. C. Brodeur. 2022. Toxicity of the neonicotinoid insecticides thiamethoxam and imidacloprid to tadpoles of three species of South American amphibians and effects of thiamethoxam on the metamorphosis of Rhinella arenarum. J. Toxicol. Environ. Health Part A 85:1019–39. doi:10.1080/15287394.2022.2147113.
   PubMed Web of Science ®Google Scholar
• Gosner, K. 1960. “A simplified table for staging anuran embryos and larvae with notes on identification.” Herpetologica 16:183–190.
   Google Scholar
• Greenwood, S. N., R. G. Belz, and B. P. Weiser. 2022. A conserved mechanism for hormesis in molecular systems. Dose-Response 20:1–11. doi:10.1177/15593258221109335.
   Web of Science ®Google Scholar
• Hadiatullah, H., Y. Zhang, A. Samurkas, Y. Xie, R. Sundarraj, H. Zuilhof, J. Qiao, and Z. Yuchi. 2022. Recent progress in the structural study of ion channels as insecticide targets. Insect Sci. 29:1–30. doi:10.1111/1744-7917.13032.
   Web of Science ®Google Scholar
• Hannig, G. T., M. Ziegler, and P. G. Marcon. 2009. Feeding cessation effects of chlorantraniliprole, a new anthranilic diamide insecticide, in comparison with several insecticides in distinct chemical classes and mode-of-action groups. Pest Manag. Sci. 65:969–74. doi:10.1002/ps.1781.
   PubMed Web of Science ®Google Scholar
• Hassan, H. F., H. S. Mohammed, and N. M. Meligi. 2021. Potential impact of marjoram on coragen- induced physiological and histological alterations in male albino rats. Egyptian. J Zool 75:25–38. doi:10.21608/ejz.2020.49316.1044.
   Google Scholar
• Hill, C. E., J. P. Myers, and L. N. Vandenberg. 2018. Nonmonotonic dose–response curves occur in dose ranges that are relevant to regulatory decision-making. Dose-Response 16:1–4. doi:10.1177/1559325818798282.
   Web of Science ®Google Scholar
• IUCN. 2022. The IUCN red list of threatened species. Version 2021-3. https://www.iucnredlist.org.
   Google Scholar
• Jayasiri, M. M. J. G. C. N., S. Yadav, N. D. K. Dayawansa, C. R. Propper, V. Kumar, and G. R. Singleton. 2022. Spatio-temporal analysis of water quality for pesticides and other agricultural pollutants in Deduru Oya River basin of Sri Lanka. J. Clean. Product 330:129897. doi:10.1016/j.jclepro.2021.129897.
   Web of Science ®Google Scholar
• Jenkins, J. A., K. R. Hartop, G. Bukhari, D. E. Howton, K. L. Smalling, S. V. Mize, M. L. Hladik, D. Johnson, R. O. Draugelis-Dale, and B. L. Brown. 2021. Juvenile African clawed frogs (Xenopus laevis) express growth, metamorphosis, mortality, gene expression and metabolic changes when exposed to thiamethoxam and clothianidin. Int J Mol Sci 22:13291. doi:10.3390/ijms222413291.
   PubMed Web of Science ®Google Scholar
• Kimura, M., A. Shoda, M. Murata, Y. Hara, S. Yonoichi, Y. Ishida, Y. Mantani, T. Yokoyama, T. Hirano, Y. Ikenaka, et al. 2023. Neurotoxicity and behavioral disorders induced in mice by acute exposure to the diamide insecticide chlorantraniliprole. J. Vet. Med. Sci. 85 (4):497–506. doi:10.1292/jvms.23-0041.
   PubMedGoogle Scholar
• Kleinau, G., C. L. Worth, A. Kreuchwig, H. Biebermann, P. Marcinkowski, P. Scheerer, and G. Krause. 2017. Structural–functional features of the thyrotropin receptor: A class a G-protein-coupled receptor at work. Front. Endocrinol 8:86. doi:10.3389/fendo.2017.00086.
   PubMed Web of Science ®Google Scholar
• Kolupaeva, V. N., A. A. Kokoreva, A. A. Belik, and P. A. Pletenev. 2019. Study of the behavior of the new insecticide cyantraniliprole in large lysimeters of the Moscow State University. Open Agric. 4:599–607. doi:10.1515/opag-2019-0057.
   Web of Science ®Google Scholar
• Lagarde, F., C. Beausoleil, S. M. Belcher, L. P. Belzunces, C. Emond, M. Guerbet, and C. Rousselle. 2015. Non-monotonic dose-response relationships and endocrine disruptors: A qualitative method of assessment. Environ. Health 14 (1):13. doi:10.1186/1476-069X-14-13.
   PubMedGoogle Scholar
• Lahm, G. P., T. P. Selby, J. H. Freudenberger, T. M. Stevenson, B. J. Myers, G. Seburyamo, B. K. Smith, L. Flexner, C. E. Clark, and D. Cordova. 2005. Insecticidal anthranilic diamides: A new class of potent ryanodine receptor activators. Bioorg. Med. Chem. Lett. 15 (22):4898–906. doi:10.1016/j.bmcl.2005.08.034.
   PubMed Web of Science ®Google Scholar
• Lalonde, B., and C. Garron. 2020. Temporal and spatial analysis of surface water pesticide occurrences in the maritime region of Canada. Arch. Environ. Contam. Toxicol. 79 (1):12–22. doi:10.1007/s00244-020-00742-x.
   PubMed Web of Science ®Google Scholar
• Larson, J. L., C. T. Redmond, and D. A. Potter. 2012. Comparative impact of an anthranilic diamide and other insecticidal chemistries on beneficial invertebrates and ecosystem services in turfgrass. Pest Manag. Sci. 68:740–48. doi:10.1002/ps.2321.
   PubMed Web of Science ®Google Scholar
• McClelland, S. J., and S. K. Woodley. 2022. Developmental exposure to trace concentrations of chlorpyrifos results in nonmonotonic changes in brain shape and behavior in amphibians. Environ. Sci. Technol. 56 (13):9379–86. doi:10.1021/acs.est.2c01039.
   PubMedGoogle Scholar
• Mondal, A. K., K. Goswami, S. Ghosh, S. Pal, A. K. Mukherjee, P. Samanta, D. Kole, and A. R. Ghosh. 2019. RETRACTED ARTICLE: Toxicity analysis of Ferterra (Chlorantraniliprole 0.4% GR) on Tilapia (Oreochromis niloticus (Linn.): Histological and ultrastructural observations. Proc. Zool. Soc 73:324–324. doi:10.1007/s12595-019-00290-w.
   Google Scholar
• Nagaraju, B., and V. V. Rathnamma. 2013. Acute toxicity of chlorantraniliprole to freshwater fish Channa punctatus (Bloch). Adv. Zool. Bot 1:78–82. doi:10.13189/azb.2013.010402.
   Google Scholar
• Oberemok, V. V., K. V. Laikova, Y. I. Gninenko, A. S. Zaitsev, P. M. Nyadar, and T. A. Adeyemi. 2015. A short history of insecticides. J. Plant. Protect. Res 55 (3):221–26. doi:10.1515/jppr-2015-0033.
   Google Scholar
• OECD. 1992. Fish Acute Toxicity Test. OECD Organisation for Co-operation and Economic Development. Test Guideline 203.
   Google Scholar
• Okada, R., K. Yamamoto, A. Koda, Y. Ito, H. Hayashi, S. Tanaka, Y. Hanaoka, and S. Kikuyama. 2004. Development of radioimmunoassay for bullfrog thyroid-stimulating hormone (TSH): Effects of hypothalamic releasing hormones on the reléase of TSH from the pituitary in vitro. Gen. Comp. Endocrinol 135:42–50. doi:10.1016/j.ygcen.2003.09.001.
   PubMed Web of Science ®Google Scholar
• Pandey, N., D. Rana, G. Chandrakar, G. Basana Gowda, N. B. Patil, G. G. P. Pandi, M. Annamalai, S. S. Pokhare, P. C. Rath, and T. Adak. 2020. Role of climate change variables (standing water and rainfall) on dissipation of chlorantraniliprole from a simulated rice ecosystem. Ecotoxicol. Environ. Saf. 205:111324. doi:10.1016/j.ecoenv.2020.111324.
   PubMed Web of Science ®Google Scholar
• Rathnamma, V. V., and B. Nagaraju. 2013. Median lethal concentrations (LC50) of chlorantraniliprole and its effects on behavioral changes in freshwater fish Labeo rohita. Int. J. Public. Health 2:137–42. doi:10.11591/ijphs.v2i4.4208.
   Google Scholar
• Rathnamma, V. V., and B. Nagaraju. 2014a. Acute toxicity and histopathological changes in freshwater fish Cirrhinus mrigala exposed to chlorantraniliprole. J.Zool. Stud 1:23–30.
   Google Scholar
• Rathnamma, V. V., and B. Nagaraju. 2014b. Oxidative stress induced by chlorantraniliprole in various tissues of freshwater fish Ctenopharyngodon idella. J. Med. Sci. Public Health 221:27.
   Google Scholar
• Redman, Z. C., C. Anastasio, and R. S. Tjeerdema. 2020. Quantum yield for the aqueous photochemical degradation of chlorantraniliprole and simulation of its environmental fate in a model California rice field. Environ. Toxicol. Chem. 39 (10):1929–35. doi:10.1002/etc.4827.
   PubMed Web of Science ®Google Scholar
• Rezende-Teixeira, P., R. G. Dusi, P. C. Jimenez, L. S. Espindola, and L. V. Costa-Lotufo. 2022. What can we learn from commercial insecticides? Efficacy, toxicity, environmental impacts, and future developments. Environ. Pollut. 300:118983. doi:10.1016/j.envpol.2022.118983.
   PubMed Web of Science ®Google Scholar
• Roelants, K., D. J. Gower, M. Wilkinson, S. P. Loader, S. D. Biju, K. Guillaume, L. Moriau, and F. Bossuyt. 2007. Global patterns of diversification in the history of modern amphibians. Proc. Natl. Acad. Sci. U.S.A. 104:887–92. doi:10.1073/pnas.0608378104.
   PubMed Web of Science ®Google Scholar
• Samurkas, A., L. Yao, H. Hadiatullah, R. Ma, Y. Xie, R. Sudarraj, H. Zuilhof, and Z. Yuchi. 2022. Ryanodine receptor as insecticide target. Curr. Pharm. Des. 28:26–35. doi:10.2174/1381612827666210902150224.
   PubMed Web of Science ®Google Scholar
• Santos, M. F., A. P. Krüger, L. M. Turchen, G. C. Cutler, E. E. Oliveiral, and R. N. C. Guedes. 2018. Non-targeted insecticidal stress in a pest species: Insecticides, sexual fitness and hormesis in the Neotropical brown stink bug Euschistus heros. Ann. Appl. Biol. 172:375–83. doi:10.1111/aab.12428.
   Web of Science ®Google Scholar
• Sattelle, D. B., D. Cordova, and T. R. Cheek. 2008. Insect ryanodine receptors: Molecular targets for novel pest control chemicals. Invert. Neurosci. 8 (3):107–19. doi:10.1007/s10158-008-0076-4.
   PubMedGoogle Scholar
• Schmidt-Jeffris, R. A., and B. A. Nault. 2016. Anthranilic diamide insecticides delivered via multiple approaches to control vegetable pests: A case study in snap bean. J. Econ. Entomol. 109 (6):2479–88. doi:10.1093/jee/tow219.
   PubMed Web of Science ®Google Scholar
• Schneider, C. A., W. S. Rasband, and K. W. Eliceiri. 2012. NIH image to Image J: 25 years of image analysis. Nat. Meth 9-7:671–75. doi:10.1038/nmeth.2089.
   Web of Science ®Google Scholar
• Selby, T. P., G. P. Lahm, and T. M. Stevenson. 2016. A retrospective look at anthranilic diamide insecticides: Discovery and lead optimization to chlorantraniliprole and cyantraniliprole. Pest Manag. Sci. 73:658–65. doi:10.1002/ps.4308.
   PubMed Web of Science ®Google Scholar
• Selby, T. P., G. P. Lahm, T. M. Stevenson, K. A. Hughes, D. Cordova, I. Billy Annan, J. D. Barry, E. A. Benner, M. J. Currie, and T. F. Pahutski. 2013. Discovery of cyantraniliprole, a potent and selective anthranilic diamide ryanodine receptor activator with cross-spectrum insecticidal activity. Bioorg. Med. Chem. Lett. 23 (23):6341–45. doi:10.1016/j.bmcl.2013.09.076.
   PubMed Web of Science ®Google Scholar
• Shi, Y.-B. 2000. Amphibian metamorphosis: From morphology to molecular biology, p. 288. New York: John Wiley & Sons.
   Google Scholar
• Shuman-Goodier, M. E., G. R. Singleton, A. M. Forsman, S. Hines, N. Christodoulides, K. D. Daniels, and C. R. Propper. 2021. Development assays using invasive cane toads, Rhinella marina, reveal safety concerns of a common formulation of the rice herbicide, butachlor. Environ. Pollut. 272:115955. doi:10.1016/j.envpol.2020.115955.
   PubMed Web of Science ®Google Scholar
• Song, C., J. Zhang, G. Hu, S. Meng, L. Fan, Y. Zheng, J. Chen, and X. Zhang. 2019. Risk assessment of chlorantraniliprole pesticide use in rice-crab coculture systems in the basin of the lower reaches of the Yangtze River in China. Chemosphere 230:440–48. doi:10.1016/j.chemosphere.2019.05.097.
   PubMed Web of Science ®Google Scholar
• Stinson, S. A., S. Hasenbein, R. E. Connon, X. Deng, J. S. Alejo, S. P. Lawler, and E. B. Holland. 2022. Agricultural surface water, imidacloprid, and chlorantraniliprole result in altered gene expression and receptor activation in Pimephales promelas. Sci. Total Environ. 806:150920. doi:10.1016/j.scitotenv.2021.150920.
   PubMed Web of Science ®Google Scholar
• Stuart, S. N., J. S. Chanson, N. A. Cox, B. E. Young, A. S. L. Rodrigues, D. L. Fischman, and R. W. Waller. 2004. Status and trends of amphibian declines and extinctions worldwide. Scienci. Express 306:1783–86. doi:10.1126/science.1103538.
   PubMed Web of Science ®Google Scholar
• Sun, Z., and H. Xu. 2019. Ryanodine receptors for drugs and insecticides: An overview. Mini. Rev. Med. Chem 19:22–33. doi:10.2174/1389557518666180330112908.
   PubMed Web of Science ®Google Scholar
• Tata, J. R. 2006. Amphibian metamorphosis as a model for the developmental actions of thyroid hormone. Mol. Cell. Endocrinol. 246 (1–2):10–20. doi:10.1016/j.mce.2005.11.024.
   PubMed Web of Science ®Google Scholar
• Thambirajah, A. A., E. M. Koide, J. J. Imbery, and C. C. Helbing. 2019. Contaminant and environmental influences on thyroid hormone action in amphibian metamorphosis. Front. Endocrinol 10:276. doi:10.3389/fendo.2019.00276.
   PubMed Web of Science ®Google Scholar
• Tiwari, S., and L. L. Stelinski. 2013. Effects of cyantraniliprole, a novel anthranilic diamide insecticide, against Asian citrus psyllid under laboratory and field conditions. Pest Manag. Sci. 69:1066–72. doi:10.1002/ps.3468.
   PubMed Web of Science ®Google Scholar
• Tuelher, E. S., E. H. da Silvia, H. L. Freitas, F. A. Namorato, J. Serra, R. N. C. Guedes, and E. E. Oliveira. 2017. Chlorantraniliprole-mediated toxicity and changes in sexual fitness of the Neotropical brown stink bug Euschistus heros. J. Pest. Sci 90:397–405. doi:10.1007/s10340-016-0777-0.
   Web of Science ®Google Scholar
• United Nations. 2019. Globally harmonized system of classification and labelling of chemicals. Eight Revised. doi:10.18356/f8fbb7cb-en
   Google Scholar
• USEPA. 2012. Ecological effects test OCSPP 850.2000: Background and special considerations- tests with terrestrial wildlife. Washington: Office of Chemical Safety and Pollution Prevention (7101). EPA 712-C-026.
   Google Scholar
• Utami, R. R., G. W. Geerling, I. R. S. Salami, S. Notodarmojo, and M. J. Ragas. 2020. Environmental prioritization of pesticide in the upper Citarum River Basin, Indonesia, using predicted and measured concentrations. Sci. Total Environ. 738:140130. doi:10.1016/j.scitotenv.2020.140130.
   PubMed Web of Science ®Google Scholar
• Vela, N., G. Pérez-Lucas, M. J. Navarro, I. Garrido, J. Fenoll, and S. Navarro. 2017. Evaluation of the leaching potential of anthranilamide insecticides through the soil. Bull. Environ. Contam. Toxicol 99 (4):465–69. doi:10.1007/s00128-017-2155-x.
   PubMed Web of Science ®Google Scholar
• Wei, L., W.-W. Shao, G.-H. Ding, X.-L. Fan, M.-L. Yu, and Z.-H. Lin. 2014. Acute and joint toxicity of three agrochemicals to Chinese tiger frog (Hoplobatrachus chinensis) tadpoles. Zool. Res 35:272–79.
   Google Scholar
• Wei, L., W.-W. Shao, and Z.-H. Lin. 2021. Effects of four individual pesticides and their pairwise combinations on the survival and growth of the tadpoles of two anuran species. Pakistan J. Zool 54:1–10. doi:10.17582/journal.pjz/20181124041148.
   Web of Science ®Google Scholar
• Xu, C., Y. Fan, X. Zhang, W. Kong, W. Miao, and Q. X. Li. 2020. DNA damage in liver cells of the tilapia fish Oreochromis mossambicus larva induced by the insecticide cyantraniliprole at sublethal doses during chronic exposure. Chemosphere 238:124586. doi:10.1016/j.chemosphere.2019.124586.
   PubMed Web of Science ®Google Scholar
• Zhang, C., X. Hu, H. Zhao, M. Wu, H. He, C. Zhang, T. Tang, L. Ping, and Z. Li. 2013. Residues of cyantraniliprole and its metabolite J9Z38 in rice field ecosystem. Chemosphere 93 (1):190–95. doi:10.1016/j.chemosphere.2013.05.033.
   PubMed Web of Science ®Google Scholar
• Zhang, Z., P. Sun, J. Zhao, H. Zhang, X. Wang, L. Li, L. Xiong, N. Yang, Y. Li, Z. Yuchi, et al. 2022. Design, synthesis and biological activity of diamide compounds based on 3-substituent of the pyrazole ring. Pest. Manage. Sci 78:2022–33. doi:10.1002/ps.6826.
   PubMed Web of Science ®Google Scholar