Toxicology International (Formerly Indian Journal of Toxicology)

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Toxic Effects Associated With Neonicotinoid Exposure on Non-target Organisms: A Review


Affiliations
1 Department of Biotechnology, IIS (Deemed to be University), Jaipur - 302020, Rajasthan, India
2 Department of Biotechnology, IIS (Deemed to be University), Jaipur - 302020, Rajastha, India
     

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The neonicotinoid class of insecticide is nicotine-like neuro-toxicants used to control the pests of agriculture crops and ornamental plants. They act as selective agonists of acetylcholine receptors in the central nervous system of insect pests and work by disrupting their nerve impulses. Some of the properties of this class of insecticides are a long half-life in soil, low volatility, and higher water solubility, leading to their accumulation in soil, underground water, and water bodies due to surface runoff. This, in turn, results in exposure to many beneficial non-target aquatic and soil fauna such as arthropods, fish, birds, mammals, etc. Although it has a selective mode of action for insects, some in vivo and in vitro investigations have also shown toxicity in non-target invertebrates and vertebrates. Initially, neonicotinoid toxicity was observed in honey bees, which are essential pollinators of crops. Later, studies reported the accumulation of neonicotinoid residues leading to the mortality of aquatic fauna, including salt marsh and freshwater mosquitoes, brine shrimp, fleas, and crayfish. Imidacloprid exposure led to disruption of larval development in the Mayfly larvae. Also, earthworms that play a crucial role in enhancing soil fertility were drastically affected by acetamiprid, clothianidin, imidacloprid, nitenpyram, and thiacloprid. Apart from these, toxicological impacts were also observed in vertebrates such as birds, where imidacloprid, clothianidin, acetamiprid, and thiacloprid caused reproductive, metabolic, and morphological alterations. Similarly, imidacloprid and acetamiprid caused gills, brain and liver dysfunction with embryo mortality. Even after the selective action of neonicotinoids, instances of mammalian toxicity were also reported in many in vivo studies. DNA damage and liver dysfunctions due to imidacloprid in rabbits were observed in various studies. In a recent study, imidacloprid exposure led to DNA damage and oxidative stress in bone marrow-derived mesenchymal cells of buffalo. Also, many instances of neurotoxicity, reproductive toxicity, immunotoxicity, genotoxicity and cytotoxicity in mouse and rat models were observed due to different neonicotinoids. Many in vitro studies using mammalian cell lines have also established potential risks of neonicotinoid exposure. This review, therefore, is a compilation of various toxicity studies of different types of neonicotinoid pesticides in both nontarget invertebrates and vertebrates, including several kinds of toxicities caused in mammals with neonicotinoid exposure.

Keywords

Insecticide, Invertebrates, Pesticide, Toxicity, Vertebrates.
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  • Kimura-Kuroda J, Komuta Y, Kuroda Y, Hayashi M, Kawano H. Nicotine-like effects of the neonicotinoid insecticides acetamiprid and imidacloprid on cerebellar neurons from neonatal rats. PloS One. 2012; 7(2):324- 32. https://doi.org/10.1371/journal.pone.0032432

  • Bass C, Denholm I, Williamson MS, Nauen R. The global status of insect resistance to neonicotinoid insecticides. Pestic Biochem Physiol. 2015. https://doi.org/10.1016/j. pestbp.2015.04.004

  • Prabhaker N, Castle SJ, Naranjo SE, Toscano NC, Morse JG. Compatibility of two systemic neonicotinoids, imi¬dacloprid and thiamethoxam, with various natural enemies of agricultural pests. J Econ Entomol. 2011; 104(3):773-781. https://doi.org/10.1603/EC10362

  • Watts M. Highly hazardous pesticides: neonicotinoids. Pesticide Action network Asia and Pacific (PAN AP) factsheet. 2011.

  • Botias C, David A, Hill EM, Goulson D. Contamination of wild plants near neonicotinoid seed-treated crops, and implications for non-target insects. Sci Total Environ. 2016; 566–567:269–278. http://dx.doi.org/10.1016/j.sci¬totenv.2016.05.065

  • Pisa LW, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Downs CA, Goulson D, Kreutzweiser DP, Krupke C, Liess M, McField M, Morrissey A, Noome DA, Settele J, Simon-Delso N, Stark JD, Van der Sluijs JP, Van Dyck H, Wiemers M. Effects of neonicotinoids and fipronil on non-target invertebrates. Environ Sci Pollut Res Int. 2015; 22:68-102. https://doi.org/10.1007/s11356-014- 3471-x

  • Suchail S, Guez D, Belzunces LP. Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environ Toxicol Chem. 2001; 20(11):2482-2486. https://doi.org/10.1002/ etc.5620201113

  • Lu C, Warchol KM, Callahan RA. Sub-lethal exposure to neonicotinoids impaired honey bees winterization before proceeding to colony collapse disorder. Bull Insectology. 2014; 67(1):125-130.

  • Pettis JS, Engelsdorp DV, Johnson J, Dively G. Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften. 2012; 99(2):153-158. https://doi.org/10.1007/s00114-011- 0881-1

  • Zhang Y, Zeng D, Li L, Hong X, Li-Byarlay H, Luo S. Assessing the toxicological interaction effects of imi-dacloprid, thiamethoxam, and chlorpyrifos on Bombus terrestris based on the combination index. Sci Rep. 2022; 12:6301. https://doi.org/10.1038/s41598-022-09808-3

  • Vastrad AS. Neonicotinoids-current success and future outlook. Pestology. 2003; 27(7):60-63.

  • Bayo FS. Insecticide mode of action in relation to their toxicity to non-target organisms. J Environment Analytic Toxicol. 2012. https://doi.org/10.4172/2161- 0525.S4-002

  • Song MY, Stark JD, Brow JJ. Comparative toxicity of four insecticides, including imidacloprid and tebufe¬nozide, to four aquatic arthropods. Environ Toxicol Chem. 1997; 16(12):2494–2500. https://doi.org/10.1002/ etc.5620161209

  • Barbee GC, Stout MJ. Comparative acute toxicity of neonicotinoid and pyrethroid insecticides to non-target crayfish (Procambarus clarkii) associated with rice-crayfish crop rotations. Pest Manag Sci. 2009; 65(11):1250–1256. https://doi.org/10.1002/ps.1817

  • Moser SE, Obrycki JJ. Non target effects of neonicotinoid seed treatments; mortality of coccinellid larvae related to zoophytophagy. Biol Control. 2009; 51(3):487-492. https://doi.org/10.1016/j.biocontrol.2009.09.001

  • Roessink I, Merga LB, Zweers HJ, Brink PJVD. The neonicotinoid imidacloprid shows high chronic toxic¬ity to Mayfly Nymphs. Environ Toxicol Chem. 2013; 32(5):1096–1100. https://doi.org/10.1002/etc.2201

  • Wang Y, Cang T, Zhao X, Yu R, Chen L, Wu C, Wang Q. Comparative acute toxicity of twenty-four insecti¬cides to earthworm Eisenia fetida. Ecotoxicol Environ Saf. 2012; 79:122–128. https://doi.org/10.1016/j. ecoenv.2011.12.016

  • Mostert MA, Schoeman AS, Vander M. The relative toxicities of insecticide to earthworms of the Pheretima group (Oligochaeta). Pest Manag Sci. 2002; 58(5):446- 450. https://doi.org/10.1002/ps.473

  • Bandeira FO, Alves PRL, Hennig TB, Brancalione J, Nogueira DJ, Matias WG. Chronic effects of clothianidin to non-target soil invertebrates: ecological risk assess¬ment using the Species Sensitivity Distribution (SSD) approach. J Hazard Mater. 2021; 419:126491. https://doi. org/10.1016/j.jhazmat.2021.126491

  • Hallmann CA, Foppen RPB, Turnhout CAMV, Kroon HD, Jongejans E. Declines in insectivorous birds are associated with high neonicotinoid concentra¬tions. Nature. 2014; 511(7509):341-343. https://doi. org/10.1038/nature13531

  • Pandey SP, Mohanty B. The neonicotinoid pesticide imidacloprid and the dithiocarbamate fungicide man¬cozeb disrupt the pituitary–thyroid axis of a wildlife bird. Chemosphere. 2015; 122:227-234. https://doi.org/10.1016/j.chemosphere.2014.11.061

  • Tokumoto J, Danjo M, Kobayashi Y, Kinoshita K, Omotehara T, Tatsumi A, Hashiguchi M, Sekijima T, Kamisoyama H, Yokoyama T, Kitagawa H, Hoshi N. Effects of exposure to clothianidin on the reproductive system of male quails. J Vet Med Sci. 2013; 75(6):755-60. https://doi.org/10.1292/jvms.12-0544

  • Taha BA, Mohammed RH. An investigation of the toxicity of compound insecticide (acetamiprid with thiamethoxam) on the development of Broiler chicken Ross 308. J Educ Sci. 2022; 31(1):123-136. https://doi. org/10.33899/edusj.2022.132403.1206

  • Ozdemir S, Altun S, Arslan H. Imidacloprid expo¬sure cause the histopathological changes, activation of TNF-α, iNOS, 8-OHdG biomarkers, and alteration of caspase 3, iNOS, CYP1A, MT1 gene expression levels in common carp (Cyprinus carpio L.). Toxicol Rep. 2017; 5:125-133. https://doi.org/10.1016/j.toxrep.2017.12.019

  • Ma X, Li H, Xiong J, Mehler WT, You J. Developmental toxicity of a neonicotinoid insecticide, acetamiprid to Zebrafish embryos. J Agric Food Chem. 2019; 67:2429- 2436. https://doi.org/10.1021/acs.jafc.8b05373

  • Stivaktakis PD, Kavvalakis MP, Tzatzarakis MN, Alegakis AK, Panagiotakis MN, Fragkiadaki P, Vakonaki E, Ozcagli E, Hayes WA, Rakitskii VN, Tsatsakis AM. Long-term exposure of rabbits to imidacloprid as quan¬tified in blood induces genotoxic effect. Chemosphere. 2016; 149:108-13. https://doi.org/10.1016/j.chemo¬sphere.2016.01.040

  • Vardavas AI, Ozcagli E, Fragkiadaki P, Stivaktakis PD, Tzatzarakis MN, Alegakisa AK, Vasilaki F, Kaloudis K, Tsiaoussis J, Kouretas D, Tsitsimpikou C, Carvalho F, Tsatsakis AM. The metabolism of imidacloprid by alde¬hyde oxidase contributes to its clastogenic effect in New Zealand rabbits. Mutat Res Gen Tox En. 2018; 829-830:27- 32. https://doi.org/10.1016/j.mrgentox.2018.03.002.

  • Al-Arami AM, AL-Sanabani AS. Histopathological effects of pesticide imidacloprid insecticide on the liver in male rabbits. Ibn al-Haitham J Pure Appl Sci. 2021; 34(4):1-9. https://doi.org/10.30526/34.4.2695

  • Singh H, Lonare MK, Sharma M, Udehiya R, Singla S, Saini SP, Dumka VK. Interactive effect of carbendazim and imidacloprid on buffalo bone marrow-derived mes¬enchymal stem cells: Oxidative stress, cytotoxicity and genotoxicity. Drug Chem Toxicol. 2021; 1-15. https:// doi.org/10.1080/01480545.2021.2007023

  • Han W, Tian Y, Shen X. Human exposure to neonicoti¬noid insecticides and the evaluation of their potential toxicity: An overview. Chemosphere. 2018; 192:59-65. https://doi.org/10.1016/j.chemosphere.2017.10.149

  • Ueyama J, Harada KH, Koizumi A, Sugiura Y, Kondo T, Saito I, Kamijima M. Temporal levels of urinary neonic¬otinoid and dialkylphosphate concentration in Japanese women between 1994 and 2011. Environ Sci Technol. 2015; 49(24):14522-14528. https://doi.org/10.1021/acs. est.5b03062

  • Koureas M, Tsezou A, Tsakalof A, Orfanidou T, Hadjichristodoulou C. Increased levels of oxidative DNA damage in pesticide sprayers in Thessaly Region (Greece). Implications of pesticide exposure. Sci Total Environ. 2014; 496:358-364. https://doi.org/10.1016/j. scitotenv.2014.07.062

  • Hernandez AF, Casado I, Pena G, Gil F, Villanueva E, Pla A. Low level of exposure to pesticides leads to lung dysfunction in occupationally exposed sub¬jects. Inhal Toxicol. 2008; 20(9):839-849. https://doi. org/10.1080/08958370801905524

  • Loser D, Grillberger K, Hinojosa MG, Blum J, Haufe Y, Danker T, Johansson Y, Moller C, Nicke A, Bennekou SH, Gardner I, Bauch C, Walker P, Forsby A, Ecker GF, Kraushaar U, Leist M. Acute effects of the imidacloprid metabolite desnitro-imidacloprid on human nACh receptors relevant for neuronal signaling. Arch Toxicol. 2021; 95(12):3695-3716. https://doi.org/10.1007/ s00204-021-03168-z

  • Lonare MK, Kumar M, More AS, Telang AG. Toxicological investigation of single oral dose adminis¬tration of imidacloprid in male Wistar rats. Toxicol. Int. 2020; 26:8-14. https://doi.org/10.18311/TI/2019/V26I1

  • Nakayama A, Yoshida M, Kagawa N, Nagao T. The neonicotinoids acetamiprid and imidacloprid impair neurogenesis and alter the microglial profile in the hippocampal dentate gyrus of mouse neonates. J Appl Toxicol. 2019; 39(6):877-887. https://doi.org/10.1002/ jat.3776

  • Lonare M, Kumar M, Raut S, Badgujar P, Doltade S, Telang A. Evaluation of imidacloprid-induced neurotoxicity in male rats: A protective effect of cur¬cumin. Neurochem Int. 2014; 78:122-9. https://doi. org/10.1016/j.neuint.2014.09.004

  • Abou-Donia MB, Goldstein B, Bullman S, Tu T, Khan WA, Dechkovskaia AM, Abdel-Rahman AA. Imidacloprid induces neurobehavioral deficits and increases expres¬sion of glial fibrillary acidic protein in the motor cortex and hippocampus in offspring rats following in utero exposure. J Toxicol Environ Health A. 2008; 71(2):119- 130. http://dx.doi.org/10.1080/15287390701613140

  • Lonare M, Kumar M, Raut S, More A, Doltade S, Badgujar P, Telang A. Evaluation of ameliorative effect of curcumin on imidacloprid-induced male repro¬ductive toxicity in Wistar rats. Environ Toxicol. 2016; 31(10):1250-63. https://doi.org/10.1002/tox.22132

  • Kapoor U, Srivastava MK, Srivastava LP. Toxicological impact of technical imidacloprid on ovarian morphol¬ogy, hormones and antioxidant enzymes in female rats. Food Chem Toxicol. 2011; 49(12):3086-3089. https:// doi.org/10.1016/j.fct.2011.09.009

  • Bal R, Naziroglu M, Turk G, Yilmaz O, Kuloglu T, Etem E, Baydas G. Insecticide imidacloprid induces morpho¬logical and DNA damage through oxidative toxicity on the reproductive organs of developing male rats. Cell Biochem Funct. 2012; 30(6):492-499. https://doi. org/10.1002/cbf.2826

  • Hirano T, Yanai S, Omotehara T, Hashimoto R, Umemura Y, Kubota N, Minami K, Nagahara D, Matsuo E, Yoshiko AY, Shinohara R, Furuyashiki T, Mantani Y, Yokoyama T, Kitagawa H, Hoshi N. The combined effect of clothianidin and environmental stress on the behav¬ioral and reproductive function in male mice. J Vet Med Sci. 2015; 77(10):1207–1215. https://doi.org/10.1292/ jvms.15-0188

  • Di Prisco G, Iannaccone M, Ianniello F, Ferrara R, Caprio E, Pennacchio F, Capparelli R. The neonicotinoid insecticide Clothianidin adversely affects immune sig¬naling in a human cell line. Sci Rep. 2017; 7(1):13446. https://doi.org/10.1038/s41598-017-13171-z

  • Sinha S, Thaker AM. Study on the impact of lead acetate pollutant on immunotoxicity produced by thiameth¬oxam pesticide. Indian J Pharmacol. 2014; 46(6):596-600. https://doi.org/10.4103/0253-7613.144910

  • Devan RKS, Prabu PC, Panchapakesan S. Immunotoxicity assessment of sub-chronic oral administration of acet¬amiprid in Wistar rats. Drug Chem Toxicol. 2015; 38(3):328-336. https://doi.org/10.3109/01480545.2014. 966382

  • Gawade L, Dadarkar SS, Husain R, Gatne M. A detailed study of developmental immunotoxicity of imidaclo¬prid in Wistar rats. Food Chem Toxicol. 2013; 51:61–70. https://doi.org/10.1016/j.fct.2012.09.009

  • Badgujar PC, Jain SK, Singh A, Punia JS, Gupta RP, Chandratre GA. Immunotoxic effects of imidacloprid following 28 days of oral exposure in BALB/c mice. Environ Toxicol Pharmacol. 2013; 35(3):408-418. https://doi.org/10.1016/j.etap.2013.01.012

  • Salema LH, Alwan MJ, Yousif AA. Immunotoxic effect of thiamethoxam in immunized mice with Brucella abortus cultural filtrate antigen. Vet World. 2016; 9(12):1407-1412. https://doi.org/10.14202/vet¬world.2016.1407-1412

  • Kataria SK, Chillar AK, Kumar A, Tomar M, Malik V. Cytogenetic and hematological alterations induced by acute oral exposure of imidacloprid in female mice. Drug Chem Toxicol. 2016; 39(1):59-65. https://doi.org/ 10.3109/01480545.2015.1026972

  • Kocaman AY, Rencuzogullari E, Topaktas M. In vitro investigation of the genotoxic and cytotoxic effects of thiacloprid in cultured human peripheral blood lym¬phocytes. Environ Toxicol. 2014; 29(6):631-641. https:// doi.org/10.1002/tox.21790

  • Sekeroglu V, Sekeroglu ZA, Kefelioglu H. Cytogenetic effects of commercial formulations of deltamethrin and/ or thiacloprid on Wistar rat bone marrow cells. Environ Toxicol. 2013; 28(9):524-531. https://doi.org/10.1002/ tox.20746

  • Bagri P, Jain SK. Assessment of acetamiprid-induced genotoxic effects in bone marrow cells of Swiss albino male mice. Drug Chem Toxicol. 2019; 42(4):357-363. https://doi.org/10.1080/01480545.2018.1429461

  • Calderon-Segura ME, Gomez-Arroyo S, Villalobos- Pietrini R, Martınez-Valenzuela C, Carbajal-Lopez Y, Calderon-Ezquerro MDC, Cortes-Eslava J, Garcıa- Martınez R, Flores-Ramırez D, Rodrıguez-Romero MI, Mendez-Perez P, Banuelos-Ruız E. Evaluation of genotoxic and cytotoxic effects in human peripheral blood lymphocytes exposed in vitro to neo¬nicotinoid insecticides news. J Toxicol. 2012; 11. https:// doi.org/10.1155/2012/612647


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  • Toxic Effects Associated With Neonicotinoid Exposure on Non-target Organisms: A Review

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Authors

Leena Khurana
Department of Biotechnology, IIS (Deemed to be University), Jaipur - 302020, Rajasthan, India
Payal Chaturvedi
Department of Biotechnology, IIS (Deemed to be University), Jaipur - 302020, Rajasthan, India
Charu Sharma
Department of Biotechnology, IIS (Deemed to be University), Jaipur - 302020, Rajasthan, India
Pradeep Bhatnagar
Department of Biotechnology, IIS (Deemed to be University), Jaipur - 302020, Rajasthan, India
Nidhi Gupta
Department of Biotechnology, IIS (Deemed to be University), Jaipur - 302020, Rajastha, India

Abstract


The neonicotinoid class of insecticide is nicotine-like neuro-toxicants used to control the pests of agriculture crops and ornamental plants. They act as selective agonists of acetylcholine receptors in the central nervous system of insect pests and work by disrupting their nerve impulses. Some of the properties of this class of insecticides are a long half-life in soil, low volatility, and higher water solubility, leading to their accumulation in soil, underground water, and water bodies due to surface runoff. This, in turn, results in exposure to many beneficial non-target aquatic and soil fauna such as arthropods, fish, birds, mammals, etc. Although it has a selective mode of action for insects, some in vivo and in vitro investigations have also shown toxicity in non-target invertebrates and vertebrates. Initially, neonicotinoid toxicity was observed in honey bees, which are essential pollinators of crops. Later, studies reported the accumulation of neonicotinoid residues leading to the mortality of aquatic fauna, including salt marsh and freshwater mosquitoes, brine shrimp, fleas, and crayfish. Imidacloprid exposure led to disruption of larval development in the Mayfly larvae. Also, earthworms that play a crucial role in enhancing soil fertility were drastically affected by acetamiprid, clothianidin, imidacloprid, nitenpyram, and thiacloprid. Apart from these, toxicological impacts were also observed in vertebrates such as birds, where imidacloprid, clothianidin, acetamiprid, and thiacloprid caused reproductive, metabolic, and morphological alterations. Similarly, imidacloprid and acetamiprid caused gills, brain and liver dysfunction with embryo mortality. Even after the selective action of neonicotinoids, instances of mammalian toxicity were also reported in many in vivo studies. DNA damage and liver dysfunctions due to imidacloprid in rabbits were observed in various studies. In a recent study, imidacloprid exposure led to DNA damage and oxidative stress in bone marrow-derived mesenchymal cells of buffalo. Also, many instances of neurotoxicity, reproductive toxicity, immunotoxicity, genotoxicity and cytotoxicity in mouse and rat models were observed due to different neonicotinoids. Many in vitro studies using mammalian cell lines have also established potential risks of neonicotinoid exposure. This review, therefore, is a compilation of various toxicity studies of different types of neonicotinoid pesticides in both nontarget invertebrates and vertebrates, including several kinds of toxicities caused in mammals with neonicotinoid exposure.

Keywords


Insecticide, Invertebrates, Pesticide, Toxicity, Vertebrates.

References





DOI: https://doi.org/10.18311/ti%2F2023%2Fv30i1%2F30246