Effect of chlorpyrifos and carbofuran on morphology, behavior and acetylcholinesterase activity of earthworm (Eisenia fetida)


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Authors

  • JYOTI YADAV Technical Officer and corresponding author, Regional Plant Quarantine Station, Directorate of Plant Protection, Quarantine & Storage, Ministry of Agriculture and Farmers Welfare, New Delhi
  • DHARAMBIR SINGH Associate Professor, Department of Zoology, CCS Haryana Agricultural University, Hisar
  • SHEFALI SHEFALI Ph D Scholar, Department of Zoology, CCS Haryana Agricultural University, Hisar

https://doi.org/10.56093/ijas.v90i10.107887

Keywords:

Acetylcholinesterase, Biomarker, Carbofuran, Chlorpyrifos, Eisenia fetida, Toxicity

Abstract

Organophosphates (OP) and carbamates when applied in agricultural fields are the potential environmental polluters and toxicants for soil flora and fauna. Upon exposure to such chemical pesticides, morphology, behaviour and acetylcholinesterase (AChE) activity of earthworms (Eisenia fetida) is altered. The present study dealt with the comparative analysis of toxic effects induced by chlorpyrifos (OP) and carbofuran (carbamate) exposure on morphology, behavior and AChE activity using standard filter paper contact toxicity method. The LC50 of chlorpyrifos and carbofuran for 24 hr was 0.25% and 5.13%, respectively, marking chlorpyrifos as more toxic pesticide than carbofuran. The treated worms exhibited abnormal morphological symptoms such as excessive mucus secretion, depigmentation, deformity, loss of metameric segments and damaged clitellum. Variation in behaviour such as reduced activity, sluggish movements and flattened posture marked the stress induced due to pesticide toxicity even at lower doses. Restlessness along with jerky movements was observed on exposure to higher concentrations of chlorpyrifos, whereas lower concentrations resulted in avoidance behavior toward pesticide coated glass vials. Thereafter, worms were exposed to different concentrations of chlorpyrifos (0.13%, 0.25% and 0.38%) and carbofuran (2.57%, 5.13% and 7.70%) for 24h and 48h to assess sub-acute and acute toxicity effects of these pesticides on AChE. The enzyme activity after 48h was 94.14%, 60.21% and 40.44% for the worms exposed to 0.125%, 0.25% and 0.375% chlorpyrifos, respectively. The enzyme activity after 48h was 98.17%, 93.92% and 79.25% for the worms exposed to 2.57%, 5.13% and 7.70% carbofuran, respectively. Time and dose dependent significant (p<0.05) decrease in the levels of AChE in pre-clitellar region of earthworms was observed as compared to control when worms were exposed to chlorpyrifos and carbofuran. Alteration in behavioural response of the earthworms may be attributed to the decline in AChE activity of pre-clitellar region. However, chlorpyrifos was more potent inhibitor of AChE activity in Eisenia fetida as compared to that of carbofuran. Such alterations indicate the potential health risk of these pesticides’ exposure at high concentrations to E. fetida.

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References

Abbott W S. 1925. A method of computing the effectiveness of an insecticide. Journal of Economic Entomology 18: 265-267. DOI: https://doi.org/10.1093/jee/18.2.265a

Ali A S and Naaz I. 2013. Earthworm biomarkers: the new tools of environmental impact assessment. Bioscience Biotechnology Research Communications 6: 163-169.

Bagul P K, More B C and Patole S S. 2016. Sub lethal effects of cypermethrin and oxyfluorfen on stress enzyme activities of earthworm species, Eisenia fetida Savigny 1826. International Journal of Innovative Technology and Exploring Engineering 5(12): 21178- 21182.

Bigbee J W, Sharma K V, Chan E L P and Bogler O. 2000. Evidence for the direct role of acetylcholinesterase in neurite outgrowth in primary dorsal root ganglion neurons. Brain Research 861(2): 354–362. DOI: https://doi.org/10.1016/S0006-8993(00)02046-1

Bigbee J W and Sharma K V. 2004. The adhesive role of acetylcholinesterase (AChE): detection of AChE binding proteins in developing rat spinal cord. Neurochemical Research 29(11): 2043–2050. DOI: https://doi.org/10.1007/s11064-004-6877-x

Calisi A, Lionetto M G and Schettino T. 2009. Pollutant- induced alterations of granulocyte morphology in the earthworm Eisenia foetida. Ecotoxicology and Environmental Safety 72: 1369-1377. DOI: https://doi.org/10.1016/j.ecoenv.2009.03.010

Calisi A, Lionetto M G and Schettino T. 2011. Biomarker response in the earthworm Lumbricus terrestris exposed to chemical pollutants. Science of Total Environment 409: 4456–4464. DOI: https://doi.org/10.1016/j.scitotenv.2011.06.058

Caselli F, Gastaldi L, Gambi N and Fabbri E. 2006. In vitro characterization of cholinesterases in the earthworm Eisenia andrei. Comparative Biochemistry and Physiology C Toxicology and Pharmacology 143: 416-421. DOI: https://doi.org/10.1016/j.cbpc.2006.04.003

Chakravorty R D and Kaviraj A. 2010. Studies on relative toxicities of six insecticides on epigeic earthworm, Perionyx exacavatus. Bulletin of Environmental Contamination and Toxicology 85: 83-86. DOI: https://doi.org/10.1007/s00128-010-0038-5

Chen J, Saleem M, Wang C, Liang W and Zhang Q. 2018. Individual and combined effects of herbicide tribenuron-methyl and fungicide tebuconazole on soil earthworm Eisenia fetida, Scientific Reports 8: 2967. DOI: https://doi.org/10.1038/s41598-018-21288-y

Ellis S R, Hodson M E and Wege P. 2010. The soil-dwelling earthworm Allolobophora chlorotica modifies its burrowing behavior in response to carbendazim applications. Ecotoxicology and Environmental Safety 73: 1424–1428. DOI: https://doi.org/10.1016/j.ecoenv.2010.05.010

Ellman G L, Courtney K D, Andres V V and Featherstone R M. 1961. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Phamocology 7: 88–95. DOI: https://doi.org/10.1016/0006-2952(61)90145-9

Ferreira R C B, Papinib S, Andrea M M D. 2015. Bioavailability and influence of 14C-carbofuran on Eisenia andrei avoidance, growth and reproduction in treated natural tropical soils. Journal of Environmental Science and Health Part B 50(4): 266-274. DOI: https://doi.org/10.1080/03601234.2015.999599

Finney D J. 1971. Probit Analysis, 3rd ed. Cambridge University Press, Cambridge, 333 pp.

Gambi N, Pasteris A and Fabbri E. 2007. Acetylcholinesterase activity in the earthworm Eisenia andrei at different conditions of carbaryl exposure. Comparative Biochemistry and Physiology Part C Toxicology and Pharmacology 145: 678–685. DOI: https://doi.org/10.1016/j.cbpc.2007.03.002

Gastaldi L, Ranzato E, Capri F, Hankard P, Pires G, Canesi L. et al. 2007. Application of a biomarker battery for the evaluation of the sublethal effects of pollutants in the earthworm Eisenia andrei. Comparative Biochemistry and Physiology C Toxicology and Pharmacology 146: 398–405. DOI: https://doi.org/10.1016/j.cbpc.2007.04.014

Grisaru D M, Pick and Perry C. et al. 2006. Hydrolytic and nonenzymatic functions of acetylcholinesterase comodulate hemopoietic stress responses. Journal of Immunology 176(1): 27–35. DOI: https://doi.org/10.4049/jimmunol.176.1.27

Hernandez S J, Notaria J, Capoweiz Y, Rault M. 2017. Soil enzyme dynamics in chlorpyrifos treated soils under the influence of earthworms. Science of Total Environment 612: 1407-1416. DOI: https://doi.org/10.1016/j.scitotenv.2017.09.043

Ibtissem B, Abdelly C and Sfar S. 2012. Antioxidant and antibacterial properties of Mesembryanthemum crystallinum and Carpobrotus edulis extracts. Advances in Chemical and Engineering Sciences 2: 359-365. DOI: https://doi.org/10.4236/aces.2012.23042

Jovana M, Tanja M and Mirjana S. 2014. Effects of three pesticides on the earth-worm Eisenia fetida (Savigny, 1826) under laboratory conditions: assessment of mortality, biomass & growth inhibition. European Journal of Soil Biology 62: 127-131. DOI: https://doi.org/10.1016/j.ejsobi.2014.03.003

Lazonby J and Waddington D. 2015. The Essential Chemical Industry – Online, University of York, York, UK.

Lionetto M G, Calisi A and Schettino T. 2012. Earthworm biomarkers as tools for soil pollution assessment. Croatia: INTECH Open Access Publisher.

Lionetto M G, Roberto C, Antonio C, Maria E G and Trifone S. 2013. Acetylcholinesterase as a biomarker in environmental and occupational medicine: New Insights and Future Perspectives. Biomedical Research International 13: 1-8. DOI: https://doi.org/10.1155/2013/321213

Mekahlia M N, Tine S, Menasria T, Amieur H and Salhi H. 2015. In vitro biomarker responses of earthworm Lumbricus terrestris exposed to herbicide sekator and phosphate fertilizer. Water Air Soil Pollution 227(1): 1-15. DOI: https://doi.org/10.1007/s11270-015-2712-z

Meshorer E and Soreq H. 2006. Virtues and woes of AChE alternative splicing in stress-related neuropathologies. Trends in Neuroscience 29(4): 216–224. DOI: https://doi.org/10.1016/j.tins.2006.02.005

Mudiam M K R, Ch R and Saxena P N. 2013. Gas chromatography-mass spectrometry based metabolomic approach for optimization and toxicity evaluation of earthworm sub-lethal responses to carbofuran. PLoS ONE, 8(12): e81077. doi:10.1371/journal. pone.0081077. DOI: https://doi.org/10.1371/journal.pone.0081077

Nunes D H, Pasini A, Benito N P and Brown G G. 2007. Minhocascomoindicadoras da qualidadeambiental. Um estudo de casonaregiao de Jaguapita, PR, Brasil. (In) G. G. Brownand C. Fragoso (Eds). Minhocasna América Latina: biodiversidade e ecologia, pp 467-480. Embrapa Soja. Londrina.

Nusair S D, Zarour Y S A and Altarifi A A. 2017. Effects of dibenzo-p-dioxins/dibenzofurans on acetylcholinesterase activity and histopathology of the body wall of earthworm Eisenia andrei: a potential biomarker for ecotoxicity monitoring. Water Air Soil Pollution 228-266. DOI: https://doi.org/10.1007/s11270-017-3448-8

OECD. 2000. Earthworm reproduction test (Eisenia fetida/andrei). (In) Organization for Economic Cooperation and Development (Ed.) OECD Guideline for testing chemicals. Proposal for a new guideline.

Otieno P O, Lalah J O, Virani M Jondiko, I O and Schramm K W. 2010. Carbofuran and its toxic metabolites provide forensic evidence for furadan exposure in Vulture (Gyps africanus) in Kenya. Bulletin of Environmental Contamination and Toxicology 84: 536–544. DOI: https://doi.org/10.1007/s00128-010-9956-5

Ramsey H, Schneider A and Stoskopf M K. 2011. A comparison of multiple esterases as biomarkers of organophosphate exposure and effect in two earthworm species. Bulletin of Environmental Contamination and Toxicology 86(4): 373–378. DOI: https://doi.org/10.1007/s00128-011-0236-9

Rao J V, Pavan Y S and Madhavendra S S. 2003. Toxic effects of chlorpyrifos on morphology and acetylcholinesterase activity in the earthworm, Eisenia fetida. Ecotoxicology and Environmental Safety 54: 296–301. DOI: https://doi.org/10.1016/S0147-6513(02)00013-1

Rault M, Mazzia C and Capowiez Y. 2007. Tissue distribution and characterization of cholinesterase activity in six earthworm species. Comparative Biochemistry and Physiology Part B, 147: 340–346. DOI: https://doi.org/10.1016/j.cbpb.2007.01.022

Reddy N C and Rao J V. 2008. Biological response of earthworm, Eisenia fetida (Savigny) to an organophosphorous pesticide, profenofos. Ecotoxicology and Environmental Safety 71: 574-582. DOI: https://doi.org/10.1016/j.ecoenv.2008.01.003

Rombke J, Jansch S and Garcia M. 2007. Earthworms as bioindicators (in particular for the influence of land use). (In) G.G. Brown and C. Fragoso (Eds). Minhocasna America Latina: biodiversidade e ecologia, pp 455-466. Embrapa Soja. Londrina.

Sandeep, Singh D, Yadav J and Urmila. 2017. Assessment of nutrient status of vermicompost of leaf litter using Eisenia fetida. Journal of Entomology and Zoological Studies 5(2): 1135-1137.

Santos M J G, Ferreira V, Soares A M V M and Loureiro S. 2011. Evaluation of the combined effects of dimethoate and spirodiclofen on plants and earthworms in a designed microcosm. Applied Soil Ecology 48: 294–300. DOI: https://doi.org/10.1016/j.apsoil.2011.04.009

Schaefer M. 2003. Behavioural endpoints in earthworm ecotoxicology. Journal of Soils Sediments 3: 79–84. DOI: https://doi.org/10.1007/BF02991072

Singh S, Tiwari R K and Pandey R S. 2019. Acute toxicity evaluation of triazophos, deltamethrin and their combination on earthworm, Eudrilus eugeniae and its impact on AChE activity. Chemistry and Ecology. DOI: 10.1080/02757540.2019.1600679 DOI: https://doi.org/10.1080/02757540.2019.1600679

Soreq H and Seidman S. 2001. Acetylcholinesterase—new roles for an old actor. Nature Review Neuroscience 2(4): 294– 302. DOI: https://doi.org/10.1038/35067589

Stepic S, Hackenberger B K, Velki M, Hackenberger D K and Loncaric Z. 2013. Potentiation effect of metolachlor on toxicity of organochlorine and organophosphate insecticides in earthworm Eisenia andrei. Bulletin of Environmental Contamination and Toxicology 91: 55–61. DOI: https://doi.org/10.1007/s00128-013-1000-0

Sternfeld M, Ming G L, Song H J et al. 1998. Acetylcholinesterase enhances neurite growth and synapse development through alternative contributions of its hydrolytic capacity, core protein, and variable C termini. Journal of Neuroscience 18(4): 1240–1249. DOI: https://doi.org/10.1523/JNEUROSCI.18-04-01240.1998

Tiwari R K, Singh S, Pandey R S and Sharma B. 2016. Enzymes of earthworm as indicators of pesticide pollution in soil. Advances in Enzyme Research 4: 113-124. DOI: https://doi.org/10.4236/aer.2016.44011

Tiwari R K, Singh S, Pandey R S. 2019. Assessment of acute toxicity and biochemical responses to chlorpyrifos, cypermethrin and their combination exposed earthworm, Eudrilus eugeniae. Toxicology Reports 6: 288–297. DOI: https://doi.org/10.1016/j.toxrep.2019.03.007

Uwizeyimanaa H, Wanga M, Chena W and Khana K. 2017. The eco-toxic effects of pesticide and heavy metal mixtures towards earthworms in soil. Environmental Toxicology and Pharmacology 55: 20–29. DOI: https://doi.org/10.1016/j.etap.2017.08.001

Vandana S and Keshav S. 2015. Toxic effect of herbicide 2, 4-D on the earthworm Eutyphoeus waltoni Michaelsen. Environmental Process 2: 251–260. DOI: https://doi.org/10.1007/s40710-015-0057-7

Velki M and Hackenberger B K. 2013a. Inhibition and recovery of molecular biomarkers of earthworm Eisenia andrei after exposure to organophosphate dimethoate. Soil Biology and Biochemistry 57: 100–8. DOI: https://doi.org/10.1016/j.soilbio.2012.09.018

Velki M and Hackenberger B K. 2013b. Biomarker responses in earthworm Eisenia andrei exposed to pirimiphos-methyl and deltamethrin using different toxicity tests. Chemosphere 90(3): 1216–1226. DOI: https://doi.org/10.1016/j.chemosphere.2012.09.051

Wang J H et al. 2012. Biochemical responses of earthworm (Eisenia foetida) to the pesticides chlorpyrifos and fenvalerate. Toxicology Mechanisms and Methods 22(3): 236–241. DOI: https://doi.org/10.3109/15376516.2011.640718

Wang K, Qi S, Xiyan M, Chai T, Yang Y, Wang D, Li D, Che W and Wang C. 2015. Evaluation of the toxicity, AChE Activity and DNA damage caused by Imidacloprid on earthworms, Eisenia fetida. Bulletin of Environmental Contamination and Toxicology 95: 475–480. DOI: https://doi.org/10.1007/s00128-015-1629-y

Yadav J, Gupta R K and Kumar D. 2017a. Changes in C: N of different substrates during vermicomposting. Ecology Environment and Conservation 23(1): 368-372.

Yadav J, Singh D, Yadav J and Kumar D. 2017b. Organophosphates and carbamates as inhibitors of acetylcholinesterase in Eisenia fetida. Pollution Research 36(2): 277- 281.

Yasmin S and Souza D D. 2010. Effects of pesticides on the growth and reproduction of earthworm: a review. Applied Environment and Soil Science: 1-9. DOI: https://doi.org/10.1155/2010/678360

Yuguda A U, Abubakar Z A, Jibo A U, Abdul Hameed A and Nayaya A J. 2015. Assessment of toxicity of some agricultural pesticides on earthworm (Lumbricus terrestris). American Eurasian Journal of Sustainable Agriculture 9(4): 49-59.

Zhang W, Chen L, Liu K, Chen L, Lin K, Guo J, Liu L, Cui C and Yan Z. 2014. Lead accumulations and toxic effects in earthworms (Eisenia fetida) in the presence of decabromodiphenyl ether. Environmental Science and Pollution Research 21: 3484–3490. DOI: https://doi.org/10.1007/s11356-013-2344-z

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2020-12-03

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2020-12-04

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YADAV, J., SINGH, D., & SHEFALI, S. (2020). Effect of chlorpyrifos and carbofuran on morphology, behavior and acetylcholinesterase activity of earthworm (Eisenia fetida). The Indian Journal of Agricultural Sciences, 90(10), 1871-1876. https://doi.org/10.56093/ijas.v90i10.107887
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