Neurotoxic Effects of Imidacloprid on Pethia conchonius (Rosy Barb), a Common Freshwater Fish of India

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Authors

  • Genetics and Molecular Biology Laboratory, Department of Zoology, University of North Bengal, P.O. NBU., Darjeeling - 734013, West Bengal ,IN
  • Genetics and Molecular Biology Laboratory, Department of Zoology, University of North Bengal, P.O. NBU., Darjeeling - 734013, West Bengal ,IN
  • Genetics and Molecular Biology Laboratory, Department of Zoology, University of North Bengal, P.O. NBU., Darjeeling - 734013, West Bengal ,IN
  • Genetics and Molecular Biology Laboratory, Department of Zoology, University of North Bengal, P.O. NBU., Darjeeling - 734013, West Bengal ,IN
  • Genetics and Molecular Biology Laboratory, Department of Zoology, University of North Bengal, P.O. NBU., Darjeeling - 734013, West Bengal ,IN

DOI:

https://doi.org/10.18311/ti/2024/v31i1/35473

Keywords:

Acetylcholinesterase, Histology, Imidacloprid, Neurotoxicity, Optic Tectum, Pethia conchonius

Abstract

Insecticides are essential to control arthropod pests in agriculture. However, due to their stability and extended half-lives, they contaminate freshwater aquatic systems like lakes, ponds, and rivers by surface run-offs and leaching. Neonicotinoids are a globally used agricultural pesticides that act as an agonist to the nicotinic acetylcholine receptor (nAChRs) and are known to have harmful effects on non-target organisms like fish. This study aimed to determine the neurotoxic, behavioural, and histopathological effect of three sub-lethal concentrations (SLC I, SLC II, and SLC III) of Imidacloprid (IMI), a neonicotinoid, on the freshwater fish Pethia conchonius. Fish were exposed to IMI for 96 hr, during which their behaviour was recorded, and the brain tissues were collected at 24 hr intervals. Compared to the control group, the IMI-exposed fish showed changes in behaviour, such as jerky, erratic swimming, disequilibrium, and mucus secretion. A significant decrease in Acetylcholinesterase (AChE) activity and histopathological damage were recorded in the brain tissues. The severity of damage and decline in activity was both concentration and time-dependent. The AChE inhibition was observed for SLC III after 96 hr (33.70±2.52) compared to control at 96 hr (84.63±4.25). The optic tectum showed detachment in its layers along with necrosis, and vacuolation. The results indicate that IMI is highly neurotoxic which not only inhibits AChE activity but also causes neural damage in the brain leading to a wide range of behavioural alterations.

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Published

2024-02-28

How to Cite

Dutta, D., Ray, A., Bhattacharya, E., Ghosh, B., & Bahadur, M. (2024). Neurotoxic Effects of Imidacloprid on <i>Pethia conchonius</i> (Rosy Barb), a Common Freshwater Fish of India. Toxicology International, 31(1), 43–54. https://doi.org/10.18311/ti/2024/v31i1/35473
Received 2023-10-28
Accepted 2023-11-30
Published 2024-02-28

 

References

GOI. 2022. Statistical Database. Directorate of Plant Protection, Quarantine and Storage, GOI. Available from: http://ppqs.gov.in/statistical-database.

Khatun H, Jamal A. Uses of chemical pesticides in agricultural fields in West Bengal and their effects on nontarget species- A review study. Int J Innov Res Sci Tech. 2021; 8(6):64–9.

Nayak P, Solanki H. Pesticides, and Indian agriculture- A review. Int J Res Granthaalayah. 2021; 9(5):250-63. https:// doi.org/10.29121/granthaalayah.v9.i5.2021.3930 DOI: https://doi.org/10.29121/granthaalayah.v9.i5.2021.3930

Banerjee I, Tripathi SK, Roy AS, Sengupta P. Pesticide use pattern among farmers in a rural district of West Bengal, India. J Nat Sci Bio Med. 2014; 5(2):313. https://doi.org/10.4103/0976- 9668.136173 PMid:25097405 PMCid: PMC4121905 DOI: https://doi.org/10.4103/0976-9668.136173

Raj A, Kumar A, Dames JF. Tapping the role of microbial biosurfactants in pesticide remediation: An eco-friendly approach for environmental sustainability. Front Microbiol. 2021; 12:791723. https://doi.org/10.3389/fmicb.2021.791723 PMid:35003022 PMCid: PMC8733403 DOI: https://doi.org/10.3389/fmicb.2021.791723

Gibbons D, Morrissey C, Mineau P. A review of the direct and indirect effects of neonicotinoids and fipronil on vertebrate wildlife. Environ Sci Pollut Res. 2015; 22: 103-18. https://doi. org/10.1007/s11356-014-3180-5 PMid:24938819 PMCid: PMC4284370 DOI: https://doi.org/10.1007/s11356-014-3180-5

Mörtl M, Vehovszky Á, Klátyik S, Takács E, Győri J, Székács A. Neonicotinoids: Spreading, translocation and aquatic toxicity. Int J Environ Res Public Health. 2020; 17(6): 2006. https://doi.org/10.3390/ijerph17062006 PMid:32197435 PMCid: PMC7143627 DOI: https://doi.org/10.3390/ijerph17062006

Rajput VD, Harish, Singh RK, Verma KK, Sharma L, Quiroz- Figueroa FR, Meena M, Gour VS, Minkina T, Sushkova S, Mandzhieva S. Recent developments in enzymatic antioxidant defence mechanism in plants with special reference to abiotic stress. Biol. 2021; 10(4): 267. https://doi.org/10.3390/ biology10040267 PMid:33810535 PMCid: PMC8066271 DOI: https://doi.org/10.3390/biology10040267

Rana A, Sharma N, Arya V. Heavy uses of pesticides in India: A quantitative analysis. The Indian Ecol Soc. 2022; 49(3): 994-1004. https://doi.org/10.55362/IJE/2022/3627 DOI: https://doi.org/10.55362/IJE/2022/3627

Elbert A, Haas M, Springer B, Thielert W, Nauen R. Applied aspects of neonicotinoid uses in crop protection. Pest Manag Sci. 2008; 64(11): 1099-105. https://doi.org/10.1002/ ps.1616 PMid:18561166 DOI: https://doi.org/10.1002/ps.1616

Hladik ML, Main AR, Goulson D. Environmental risks, and challenges associated with neonicotinoid insecticides. Environ Sci Tech. 2018; 52:3329-35. https://doi.org/10.1021/ acs.est.7b06388 PMid:29481746 DOI: https://doi.org/10.1021/acs.est.7b06388

Özdemir S, Altun S, Arslan H. Imidacloprid exposure causes 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. 2018; 5:125-33. https://doi.org/10.1016/j.toxrep.2017.12.019 PMid:29321977 PMCid: PMC5751999 DOI: https://doi.org/10.1016/j.toxrep.2017.12.019

Kumar A, Tomar M, Kataria SK. Effect of sub-lethal doses of imidacloprid on histological and biochemical parameters in female albino mice. ISOR J Environ Sci Toxicol Food Technol. 2014; 8:9-15. https://doi.org/10.9790/2402- 08140915 DOI: https://doi.org/10.9790/2402-08140915

Amenyogbe E, Huang JS, Chen G, Wang Z. An overview of the pesticides’ impacts on fishes and humans. Int J Aquat Bio. 2021; 9(1): 55-65. http://dx.doi.org/10.22034/ijab. v9i1.972

Merga LB, Van den Brink PJ. Ecological effects of imidacloprid on a tropical freshwater ecosystem and subsequent recovery dynamics. Sci Total Environ. 2021; 784:147167. https://doi.org/10.1016/j. scitotenv.2021.147167 PMid:34088063 DOI: https://doi.org/10.1016/j.scitotenv.2021.147167

Schäfer RB, van den Brink PJ, Liess M. Impacts of pesticides on freshwater ecosystems. Ecological Impacts of Toxic Chemicals. 2011; 2011:111-37. https://doi.org/10.2174/978 160805121211101010111 DOI: https://doi.org/10.2174/978160805121211101010111

Mahboob S, Al-Ghanim KA, Sultana S, Al-Balawi HA, Sultana T, Al-Misned F, Ahmed Z. A study on the acute toxicity of triazophos, profenofos, carbofuran and carbaryl pesticides on Cirrhinus mrigala. Pak J Zool. 2015; 47(2).

Inyang IR, Korogbegha TF. Haematological and biochemical responses of Heterobranchus bidorsalis to imidacloprid. Ann Eco Environ Sci. 2018; 2(2): 41-6. https://doi.org/10.22259/2637-5338.0202006 DOI: https://doi.org/10.22259/2637-5338.0202006

Dutta D, Ray A, Ghosh B, Bahadur M. Assessment of imidacloprid induced genotoxicity in Pethia conchonius (Rosy barb), a common freshwater fish of India. Drug Chem Toxicol. 2023; 1-4. https://doi.org/10.1080/01480545.2023.2222931 PMid:37326304 DOI: https://doi.org/10.1080/01480545.2023.2222931

Qadir S, Iqbal F. Effect of sublethal concentration of imidacloprid on the histology of heart, liver and kidney in Labeo rohitr. Pak J Pharm Sci. 2016; 29(6).

Salunke A, P Pandya, P Parikh. Behavioural alterations and neurotoxicity of Imidacloprid on freshwater Teleost Oreochromis mossambicus. Int Res J Sci Eng. 2020; 9:23-30.

Rahman AN, Abdel-Mageed MA, Assayed ME, Gharib HS, Nasr MA, Elshopakey GE, Moniem HA, Shahin SE, ELHusseiny E, Ahmed SA. Imidacloprid induced growth, haematological, neuro-behavior, antioxidant, economic, genetic, and histopathological alterations in Clarias gariepinus: Alleviative role of dietary Hyphaene thebaica. Aquaculture. 2023; 564:739058. https://doi.org/10.1016/j. aquaculture.2022.739058 DOI: https://doi.org/10.1016/j.aquaculture.2022.739058

Günal AÇ, Erkmen B, Paçal E, Arslan P, Yildirim Z, Erkoç F. Sub-lethal effects of imidacloprid on Nile Tilapia (Oreochromis niloticus). Water Air Soil Pollut. 2020; 231:1- 10. https://doi.org/10.1007/s11270-019-4366-8 DOI: https://doi.org/10.1007/s11270-019-4366-8

Lionetto MG, Caricato R, Giordano ME, Pascariello MF, Marinosci L, Schettino T. Integrated use of biomarkers (acetylcholinesterase and antioxidant enzymes activities) in Mytilus galloprovincialis and Mullus barbatus in an Italian coastal marine area. Mar Pollut Bull. 2003; 46(3): 324-30. https://doi.org/10.1016/S0025-326X(02)00403-4 PMid:12604066 DOI: https://doi.org/10.1016/S0025-326X(02)00403-4

Singh S, Bhattacharjee S, Pal J. Acute toxicity of chlorpyrifos to zebrafish, Danio rerio (Cyprinidae). J Anim Sci. 2017; 11:45-9.

Guerra LJ, do Amaral AM, de Quadros VA, da Luz Fiuza T, Rosemberg DB, Prestes OD, Zanella R, Clasen B, Loro VL. Biochemical and behavioural responses in zebrafish exposed to imidacloprid oxidative damage and antioxidant responses. Arch Environ Contam Toxicol. 2021; 81(2): 255-64. https:// doi.org/10.1007/s00244-021-00865-9 PMid:34137922 DOI: https://doi.org/10.1007/s00244-021-00865-9

Alvim TT, dos Reis Martinez CB. Genotoxic and oxidative damage in the freshwater teleost Prochilodus lineatus exposed to the insecticide’s lambda-cyhalothrin and imidacloprid alone and in combination. Mut Res. 2019; 842:85-93. https://doi.org/10.1016/j.mrgentox.2018.11.011 PMid:31255229 DOI: https://doi.org/10.1016/j.mrgentox.2018.11.011

Singh S, Bhutia D, Sarkar S, Rai BK, Pal J, Bhattacharjee S, Bahadur M. Analyses of pesticide residues in water, sediment, and fish tissue from river Deomoni flowing through the tea gardens of Terai Region of West Bengal, India. Int J Fis Aquat Stud. 2015; 3(2): 17-23.

Das A. Comparative study of pollution status of two main rivers: Karola and Tista of Jalpaiguri, West Bengal. Int J Curr Pharm Res. 2017; 9(7): 76-81.

Mondal R, Mukherjee A, Biswas S, Kole RK. GC-MS/MS determination and ecological risk assessment of pesticides in aquatic system: A case study in Hooghly River basin in West Bengal, India. Chemosphere. 2018; 206:217-30. https://doi. org/10.1016/j.chemosphere.2018.04.168 PMid:29751247 DOI: https://doi.org/10.1016/j.chemosphere.2018.04.168

Shah ZU, Parveen S. Distribution, and risk assessment of pesticide residues in sediment samples from river Ganga, India. Plos One. 2023; 18(2):e0279993. https://doi.org/10.1371/ journal.pone.0279993 PMid:36730256 PMCid: PMC9894440 DOI: https://doi.org/10.1371/journal.pone.0279993

Organisation for Economic Co-operation and Development, OECD: 2019. Test No. 203: fish, acute toxicity test. France: OECD Publishing; 2019

Islam MA, Hossen MS, Sumon KA, Rahman MM. Acute toxicity of imidacloprid on the developmental stages of common carp Cyprinus carpio. Toxicol Environ Health Sci. 2019; 11:244-51. https://doi.org/10.1007/s13530-019- 0410-8 DOI: https://doi.org/10.1007/s13530-019-0410-8

Rice EW, Baird RB, Eaton AD, Clesceri LS. Standard methods for the examination of water and wastewater Washington: American Public Health Association; 2012.

Bernet D, Schmidt H, Meier W, Burkhardt‐Holm P, Wahli T. Histopathology in fish: Proposal for a protocol to assess aquatic pollution. J Fis Dis. 1999; 22(1): 25-34. https://doi. org/10.1046/j.1365-2761.1999.00134.x DOI: https://doi.org/10.1046/j.1365-2761.1999.00134.x

Ellman GL, Courtney KD, Andres Jr V, Featherstone RM. A new and rapid colourimetric determination of acetylcholinesterase activity. Biochem Pharmacol. 1961; 7(2): 88-95. https://doi.org/10.1016/0006-2952(61)90145-9 PMid:13726518 DOI: https://doi.org/10.1016/0006-2952(61)90145-9

Lushchak VI, Matviishyn TM, Husak VV, Storey JM, Storey KB. Pesticide toxicity: A mechanistic approach. EXCLI J. 2018; 17:1101. http://dx.doi.org/10.17179/ excli2018-1710

Crosby EB, Bailey JM, Oliveri AN, Levin ED. Neurobehavioral impairments caused by developmental imidacloprid exposure in zebrafish. Neurotoxicol Teratol. 2015; 49:81-90. https://doi.org/10.1016/j.ntt.2015.04.006 PMid:25944383 PMCid: PMC4458463 DOI: https://doi.org/10.1016/j.ntt.2015.04.006

Ullah R, Zuberi A, Ullah S, Ullah I, Dawar FU. Cypermethrin induced behavioural and biochemical changes in mahseer, Tor putitora. J Toxicol Sci. 2014; 39(6): 829-36. https://doi. org/10.2131/jts.39.829 PMid:25374374 DOI: https://doi.org/10.2131/jts.39.829

Zhang JF, Liu H, Sun YY, Wang XR, Wu JC, Xue YQ. Responses of the antioxidant defenses of the Goldfish Carassius auratus, exposed to 2, 4-dichlorophenol. Environ Toxicol Pharm. 2005; 19(1):185-90. https://doi.org/10.1016/j.etap.2004.07.001 PMid:21783475 DOI: https://doi.org/10.1016/j.etap.2004.07.001

Yang C, Lim W, Song G. Mediation of oxidative stress toxicity induced by pyrethroid pesticides in fish. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology. 2020; 234:108758. https://doi.org/10.1016/j.etap.2004.07.001 PMid:21783475 DOI: https://doi.org/10.1016/j.cbpc.2020.108758

Cong Y, Han X, Wang Y, Chen Z, Lu Y, Liu T, Wu Z, Jin Y, Luo Y, Zhang X. Drug toxicity evaluation based on organ-on-a-chip technology: A review. Micromachines. 2020; 11(4):381. https://doi.org/10.3390/mi11040381 PMid:32260191 PMCid: PMC7230535 DOI: https://doi.org/10.3390/mi11040381

Mishra A, Devi Y. Histopathological alterations in the brain (optic tectum) of the freshwater teleost Channa punctatus in response to acute and sub-chronic exposure to the pesticide Chlorpyrifos. Acta histochem. 2014; 116(1): 176-81. https:// doi.org/10.1016/j.acthis.2013.07.001 PMid:23948667 DOI: https://doi.org/10.1016/j.acthis.2013.07.001

Nataraj B, Hemalatha D, Rangasamy B, Maharajan K, Ramesh M. Hepatic oxidative stress, genotoxicity and histopathological alteration in freshwater fish Labeo rohita exposed to organophosphorus pesticide profenofos. Biocatal Agric Biotechnol. 2017; 12: 185-90. https://doi. org/10.1016/j.bcab.2017.09.006 DOI: https://doi.org/10.1016/j.bcab.2017.09.006

Srivastava P, Singh A, Pandey AK. Pesticides toxicity in fishes: Biochemical, physiological, and genotoxic aspects. Biochem Cell Arch. 2016; 16(2):199-218.

Desai B, Parikh P. Behavioural responses to acute exposure of Imidacloprid and Curzate on Labeo rohita (Hamilton, 1822). Int J Sci Res. 2014; 2(1):1-2.

Halappa R, David M. Behavioral responses of the freshwater fish, Cyprinus carpio (Linnaeus) following sublethal exposure to chlorpyrifos. Turk J Fis Aquat Sci. 2009; 9(2). https://doi.org/10.4194/trjfas.2009.0218 DOI: https://doi.org/10.4194/trjfas.2009.0218

Li S, Li AJ, Zhao J, Santillo MF, Xia M. Acetylcholinesterase inhibition assays for high-throughput screening. In High- Throughput Screening Assays in Toxicology. 2022; 47-58. https://doi.org/10.1007/978-1-0716-2213-1_6 PMid:35294755 PMCid: PMC9440486 DOI: https://doi.org/10.1007/978-1-0716-2213-1_6

Glusczak L, dos Santos Miron D, Crestani M, da Fonseca MB, de Araújo Pedron F, Duarte MF, Vieira VL. Effect of glyphosate herbicide on acetylcholinesterase activity and metabolic and hematological parameters in piava (Leporinus obtusidens). Ecotoxicol Environ Saf. 2006;65(2):237- 41. https://doi.org/10.1016/j.ecoenv.2005.07.017 PMid:16174533 DOI: https://doi.org/10.1016/j.ecoenv.2005.07.017

Topal A, Alak G, Ozkaraca M, Yeltekin AC, Comaklı S, Acıl G, Kokturk M, Atamanalp M. Neurotoxic responses in brain tissues of rainbow trout exposed to imidacloprid pesticide: Assessment of 8-hydroxy-2-deoxyguanosine activity, oxidative stress and acetylcholinesterase activity. Chemosphere. 2017; 175:186-91. https://doi.org/10.1016/j. chemosphere.2017.02.047 PMid:28219821 DOI: https://doi.org/10.1016/j.chemosphere.2017.02.047

Veeraiah K, Reddy IS, Krishna C, Sindhuri C. Acute toxicity of imidacloprid to freshwater fish Labeo rohita and the consequential biochemical changes. Paripex Indian J Res. 2018; 7(12): 35–40.

Vieira CE, Costa PG, Lunardelli B, de Oliveira LF, da Costa Cabrera L, Risso WE, Primel EG, Meletti PC, Fillmann G, dos Reis Martinez CB. Multiple biomarker responses in Prochilodus lineatus subjected to shortterm in situ exposure to streams from agricultural areas in Southern Brazil. Sci Total Environ. 2016; 542:44- 56. https://doi.org/10.1016/j.scitotenv.2015.10.071 PMid:26519566 DOI: https://doi.org/10.1016/j.scitotenv.2015.10.071

Lakshmaiah G. Brain histopathology of the fish Cyprinus carpio exposed to lethal concentrations of an organophosphate insecticide phorate. Int J Adv Res Dev. 2017; 2(5):668-72. https://doi.org/10.7439/ijasr. v2i4.3233 DOI: https://doi.org/10.7439/ijasr.v2i4.3233