THIAMETHOXAM-INDUCED NEUROTOXICITY AND GUT DAMAGE IN HONEYBEES (APIS MELLIFERA) MOLECULAR AND BEHAVIORAL EVIDENCE OF A SILENT THREAT
Main Article Content
Keywords
Life longevity gene, Cholinergic toxicity, Neonicotinoid, Foraging behavior, Pollinators.
Abstract
Neonicotinoid insecticides are widely used in agriculture for controlling insect pests. Sub-lethal doses of neonicotinoids can damage gut tissues and cause neurophysiological disorders in honey bees. They disrupt the normal function of the Acetylcholinesterase (AChE) enzyme which plays a vital role in nerve impulse transmission and honey bee foraging behavior. This study investigated the potentially toxic impact of thiamethoxam exposure on honey bee, (Apis mellifera) gut as well as Acetylcholinesterase (AChE) and Major Royal Jelly Protein (MRJP1) gene expression. Adult honey bees were subjected to thiamethoxam exposure in the laboratory at different concentrations of 0.0097%, 0.0048%, and 0.0024% via feeding bioassay for 3 days. After the thiamethoxam exposure consumption rate, survival rate, and mortality rate of honey bees were assessed. Highest survival was observed at the lowest concentration (0.0024%) followed by a progressive decrease in survival with increasing concentration. Treated group of bees showed abnormal behavioral changes like flight incapacity, ataxia, and proboscis extension. Histological analysis of gut tissue showed epithelial disorientation and vacuolization. Ct values obtained from Real-Time PCR results showed 47.8- and 58-fold upregulation of the AChE2 and MRJP1 genes respectively, indicating pesticide-induced cholinergic toxicity and stress response in bees. This study demonstrated the detrimental effects of thiamethoxam which reduces honey bees’ survival by inducing neurotoxicity and stress, posing a significant threat to ecosystem stability.
References
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25. O'Shea-Wheller, T. A., Rinkevich, F. D., Danka, R. G., Simone-Finstrom, M., Tokarz, P. G., and Healy, K. B. 2022. A derived honey bee stock confers resistance to Varroa destructor and associated viral transmission. Scientific Reports, 12: 4852 – 4871
26. Paoli, M. and Giurfa, M. 2024. Pesticides and pollinator brain: How do neonicotinoids affect the central nervous system of bees. The European Journal of Neuroscience, 60 (8):5927 – 5948.
27. Pervez, M. and Manzoor, F. 2020. A study on lethal doses of various pesticides on Honeybees (Apis mellifera L.) – a laboratory trial. Physiological Entomology, 46 (1): 34 – 44.
28. Roat, T. C., Santos-Pinto, J. R. A. D., Miotelo, L., De Souza, C. L., Palma, M. S., and Malaspina, O. 2020. Using a toxicoproteomic approach to investigate the effects of thiamethoxam on the brain of Apis mellifera. Chemosphere, 258: 127362 – 12775.
29. Tsvetkov, N., Samson-Robert, O., Sood, K., Patel, H. S., Malena, D. A., Gajiwala, P. H., and Zayed, A. 2017. Chronic exposure to neonicotinoids reduces honey bee health near corn crops. Science, 356 (6345): 1395 - 1397.
30. Sandstrom, M. W., Nowell, L. H., Mahler, B. J. and Van Metre, P. C. 2022. New-generation pesticides are prevalent in California’s Central Coast streams. Science of the Total Environment, 56 (18): 12151 – 12162.
31. Suchail, S., Debrauwer, L. and Belzunces, L. P. 2004. Metabolism of imidacloprid in Apis mellifera. Pest Management Science: formerly Pesticide Science, 60 (3): 291 – 296.
32. Tavares, D. A., Roat, T. C., Carvalho, S. M., Silva-Zacarin, E. C. M. and Malaspina, O. 2015. In vitro effects of thiamethoxam on larvae of Africanized honey bee Apis mellifera (Hymenoptera: Apidae). Chemosphere, 135: 370 – 378.
33. Tavares, D.A., Dussaubat, C., Kretzschmar, A., et al. (2017) Exposure of larvae to thiamethoxam affects the survival and physiology of the honeybee at post-embryonic stages. Environmental Pollution, 229: 386 – 393.
34. Tison, L., Hahn, M. L., Holtz, S., Robner, A., Greggers, U., Bischoff, G. and Menzel, R. 2016. Honeybees’ behavior is impaired by chronic exposure to the neonicotinoid thiacloprid in the field. Environmental Science and Technology, 50 (13): 7218 – 7227.
35. Tome, H. V., Schmehl, D. R., Wedde, A. E., Godoy, R. S., Ravaiano, S. V., Guedes, R. N. and Ellis, J. D. 2020. Frequently encountered pesticides can cause multiple disorders in developing worker honey bees. Environmental Pollution, 256: 113420 – 113431.
36. Van der Sluijs, J. P., Simon-Delso, N., Goulson, D., Maxim, L., Bonmatin, J. M., and Belzunces, L. P. 2013. Neonicotinoids, bee disorders and the sustainability of pollinator services. Current Opinion in Environmental Sustainability, 5(3-4): 293 - 305.
37. Wagner, D. L., Grames, E. M., Forister, M. L., Berenbaum, M. R. and Stopak, D. 2021. Insect decline in the Anthropocene: Death by a thousand cuts. Proceedings of the National Academy of Sciences of the United States of America. Annual Review of Entomology 118 (2): 1 – 11.
38. Wang, K., Chen, H., Lin, Z., Niu, Q., Wang, Z., Gao, F., and Ji, T. 2020. Carbendazim exposure during the larval stage suppresses major royal jelly protein expression in nurse bees (Apis mellifera). Chemosphere, 266: 129011 – 129025.
39. Wang, Y., Zhang, W., Shi, T., Xu, S., Lu, B., Qin, H. and Yu, L. 2020. Synergistic toxicity and physiological impact of thiamethoxam alone or in binary mixtures with three commonly used insecticides on honeybees. Apidologie, 51: 395 – 405.
40. Warner, S., Pokhrel, L. R., Akula, S. M., Ubah, C. S., Richards, S. L., Jensen, H. and Kearney, G. D. 2024. A scoping review on the effects of Varroa mite (Varroa destructor) on global honey bee decline. Science of the Total Environment, 906: 167492 – 167503.
41. Williamson, S. M. and Wright, G. A. 2013. Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. Journal of Experimental Biology, 216 (10): 1799 –1807.
42. Williamson, S. M., Willis, S. J. and Wright, G. A. 2014. Exposure to neonicotinoids influences the motor function of adult worker honeybees. Ecotoxicology, 23: 1409 –1418.
43. Yang, Y., Ma, S., Yan, Z., Liu, F., Diao, Q., and Dai, P. 2019. Effects of three common pesticides on survival, food consumption, and midgut bacterial communities of adult workers Apis cerana and Apis mellifera. Environmental Pollution, 249: 860 –867.
2. Almasri, H., Liberti, J., Brunet, J., Engel, P., and Belzunces, L. P. 2022. Mild chronic exposure to pesticides alters physiological markers of honey bee health without perturbing the core gut microbiota. Scientific Reports, 12(1). 4281 – 4296.
3. Abbott, W. S. 1925. A method of computing the effectiveness of an insecticide. Journal of Economic Entomology, 18: 265 – 267.
4. Bruckner, S., Straub, L., Villamar-Bouza, L., Beneduci, Z. J., Neumann, P., and Williams, G. R. 2024. Life stage-dependent effects of neonicotinoid exposure on honey bee hypopharyngeal gland development. Ecotoxicology and Environmental Safety, 288: 117337 – 117342.
5. Calmorin, L. 1997. Statistics in Education and the Sciences, 1st ed. pp. 172 – 183.
6. Choudhary, A., Mohindru, B., Karedla, A. K., Singh, J. and Chhuneja, P. K. 2022. Sub-lethal effects of thiamethoxam on Apis mellifera Linnaeus. Toxin Reviews, 41 (3): 1044 – 1057.
7. Christen, V., Mittner, F. and Fent, K. 2016. Molecular effects of neonicotinoids in honey bees (Apis mellifera). Environmental Science and Technology, 50 (7): 4071 – 4081.
8. Chakrabarti, P., Carlson, E. A., Lucas, H. M., Melathopoulos, A. P., and Sagili, R. R. 2020. Field rates of SivantoTM (flupyradifurone) and Transform® (sulfoxaflor) increase oxidative stress and induce apoptosis in honey bees (Apis mellifera L.). PLoS ONE, 15 (5): 233 - 249.
9. Di Prisco, G., Cavaliere, V., Annoscia, D., Varricchio, P., Caprio, E., Nazzi, F. and Pennacchio, F. 2013. Neonicotinoid clothianidin adversely affects insect immunity and promotes the replication of a viral pathogen in honey bees. Proceedings of the National Academy of Sciences, 110 (46): 18466 - 18471.
10. Goulson, D. 2013. An overview of the environmental risks posed by neonicotinoid insecticides. Journal of Applied Ecology, 50 (4): 977 – 987.
11. Hacker, G. 2000. The morphology of apoptosis. Cell and Tissue Research, 301: 5 – 17.
12. Henry, M., Beguin, M., Requier, F., Rollin, O., Odoux, J. F., Aupinel, P. and Decourtye, A. 2012. A common pesticide decreases foraging success and survival in honey bees. Science, 336 (6079): 348 – 350.
13. Hopwood, J., Code, A., Vaughan, M., Biddinger, D., Shepherd, M., Black, S. H. and Mazzacano, C. 2016. How neonicotinoids can kill bees. The Xerces Society for Invertebrate Conservations, 90126 (3): 1 – 44.
14. Iwasa, T., Motoyama, N., Ambrose, J.T. and Roe, R. M. 2004. Mechanism
15. For the differential toxicity of neonicotinoid insecticides in honeybee, A. mellifera. Crop Protection., 23: 371 – 378.
16. Kesnerova, L., Emery, O., Troilo, M., Liberti, J., Erkosar, B. and Engel, P. 2020. Gut microbiota structure differs between honeybees in winter and summer. The ISME journal, 14 (3): 801 – 814.
17. Kessler, S. C., Tiedeken, E. J., Simcock, K. L., Derveau, S., Mitchell, J., Softley, S. and Wright, G. A. 2015. Bees prefer foods containing neonicotinoid pesticides. Nature, 521 (7550): 74 – 76.
18. Khalifa, S. A. M., Elshafiey, E. H., Shetaia, A. A., El-Wahed, A. A. A., Algethami, F. A., Musharraf, S. G., AlAjmi, M. F., Zhao, C., Masry, S. H. D., Abdel-Daim, M. M., Halabi, M. F., Kai, G., Al Naggar, Y., Bishr, M., Diab, M. A. M. and El-Seedi, H. R. 2021. Overview of bee pollination and its economic value for crop production. Insects, 12 (688): 1 – 23.
19. Laurino, D., Porporato, M., Patetta, A. and Manino, A. 2011. Toxicity of neonicotinoid insecticides to honey bees: laboratory tests. Bulletin of Insectology, 64 (1): 107 – 113.
20. Li, Z., Yu, T., Chen, Y., Heerman, M., He, J., Huang, J. and Su, S. 2019. Brain transcriptome of honey bees (Apis mellifera) exhibiting impaired olfactory learning induced by a sublethal dose of imidacloprid. Pesticide Biochemistry and Physiology, 156: 36 – 43.
21. Lu, C., Hung, Y. T. and Cheng, Q. 2020. A review of sub-lethal neonicotinoid insecticides exposure and effects on pollinators. Current Pollution Reports, 6: 137 – 151.
22. Martelli, F., Zhongyuan, Z., Wang, J., Wong, C., Karagas, N. E., Roessner, U., Rupasinghe, T., Venkatachalam, K., Perry, T., Bellen, H. J. and Batterham, P. 2020. Low doses of the neonicotinoid insecticide imidacloprid induce ROS triggering neurological and metabolic impairments in Drosophila. Proceedings of the National Academy of Sciences, 117 (41): 25840 – 25850.
23. Martinello, M., Manzinello, C., Borin, A. et al. 2020. A survey from 2015 to 2019 to investigate the occurrence of pesticide residues in dead honeybees and other matrices related to honeybee mortality incidents in Italy. Diversity, 12 (15): 2 – 16.
24. Oliveira, R. A., Roat, T. C., Carvalho, S. M. and Malaspina, O. 2013. Side‐effects of thiamethoxam on the brain and midgut of the Africanized honeybee Apis mellifera (Hymenoptera: Apidae). Environmental Toxicology, 29 (10): 1122 – 1133.
25. O'Shea-Wheller, T. A., Rinkevich, F. D., Danka, R. G., Simone-Finstrom, M., Tokarz, P. G., and Healy, K. B. 2022. A derived honey bee stock confers resistance to Varroa destructor and associated viral transmission. Scientific Reports, 12: 4852 – 4871
26. Paoli, M. and Giurfa, M. 2024. Pesticides and pollinator brain: How do neonicotinoids affect the central nervous system of bees. The European Journal of Neuroscience, 60 (8):5927 – 5948.
27. Pervez, M. and Manzoor, F. 2020. A study on lethal doses of various pesticides on Honeybees (Apis mellifera L.) – a laboratory trial. Physiological Entomology, 46 (1): 34 – 44.
28. Roat, T. C., Santos-Pinto, J. R. A. D., Miotelo, L., De Souza, C. L., Palma, M. S., and Malaspina, O. 2020. Using a toxicoproteomic approach to investigate the effects of thiamethoxam on the brain of Apis mellifera. Chemosphere, 258: 127362 – 12775.
29. Tsvetkov, N., Samson-Robert, O., Sood, K., Patel, H. S., Malena, D. A., Gajiwala, P. H., and Zayed, A. 2017. Chronic exposure to neonicotinoids reduces honey bee health near corn crops. Science, 356 (6345): 1395 - 1397.
30. Sandstrom, M. W., Nowell, L. H., Mahler, B. J. and Van Metre, P. C. 2022. New-generation pesticides are prevalent in California’s Central Coast streams. Science of the Total Environment, 56 (18): 12151 – 12162.
31. Suchail, S., Debrauwer, L. and Belzunces, L. P. 2004. Metabolism of imidacloprid in Apis mellifera. Pest Management Science: formerly Pesticide Science, 60 (3): 291 – 296.
32. Tavares, D. A., Roat, T. C., Carvalho, S. M., Silva-Zacarin, E. C. M. and Malaspina, O. 2015. In vitro effects of thiamethoxam on larvae of Africanized honey bee Apis mellifera (Hymenoptera: Apidae). Chemosphere, 135: 370 – 378.
33. Tavares, D.A., Dussaubat, C., Kretzschmar, A., et al. (2017) Exposure of larvae to thiamethoxam affects the survival and physiology of the honeybee at post-embryonic stages. Environmental Pollution, 229: 386 – 393.
34. Tison, L., Hahn, M. L., Holtz, S., Robner, A., Greggers, U., Bischoff, G. and Menzel, R. 2016. Honeybees’ behavior is impaired by chronic exposure to the neonicotinoid thiacloprid in the field. Environmental Science and Technology, 50 (13): 7218 – 7227.
35. Tome, H. V., Schmehl, D. R., Wedde, A. E., Godoy, R. S., Ravaiano, S. V., Guedes, R. N. and Ellis, J. D. 2020. Frequently encountered pesticides can cause multiple disorders in developing worker honey bees. Environmental Pollution, 256: 113420 – 113431.
36. Van der Sluijs, J. P., Simon-Delso, N., Goulson, D., Maxim, L., Bonmatin, J. M., and Belzunces, L. P. 2013. Neonicotinoids, bee disorders and the sustainability of pollinator services. Current Opinion in Environmental Sustainability, 5(3-4): 293 - 305.
37. Wagner, D. L., Grames, E. M., Forister, M. L., Berenbaum, M. R. and Stopak, D. 2021. Insect decline in the Anthropocene: Death by a thousand cuts. Proceedings of the National Academy of Sciences of the United States of America. Annual Review of Entomology 118 (2): 1 – 11.
38. Wang, K., Chen, H., Lin, Z., Niu, Q., Wang, Z., Gao, F., and Ji, T. 2020. Carbendazim exposure during the larval stage suppresses major royal jelly protein expression in nurse bees (Apis mellifera). Chemosphere, 266: 129011 – 129025.
39. Wang, Y., Zhang, W., Shi, T., Xu, S., Lu, B., Qin, H. and Yu, L. 2020. Synergistic toxicity and physiological impact of thiamethoxam alone or in binary mixtures with three commonly used insecticides on honeybees. Apidologie, 51: 395 – 405.
40. Warner, S., Pokhrel, L. R., Akula, S. M., Ubah, C. S., Richards, S. L., Jensen, H. and Kearney, G. D. 2024. A scoping review on the effects of Varroa mite (Varroa destructor) on global honey bee decline. Science of the Total Environment, 906: 167492 – 167503.
41. Williamson, S. M. and Wright, G. A. 2013. Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. Journal of Experimental Biology, 216 (10): 1799 –1807.
42. Williamson, S. M., Willis, S. J. and Wright, G. A. 2014. Exposure to neonicotinoids influences the motor function of adult worker honeybees. Ecotoxicology, 23: 1409 –1418.
43. Yang, Y., Ma, S., Yan, Z., Liu, F., Diao, Q., and Dai, P. 2019. Effects of three common pesticides on survival, food consumption, and midgut bacterial communities of adult workers Apis cerana and Apis mellifera. Environmental Pollution, 249: 860 –867.
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Apr 22, 2024
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Tahira Minal, Mahnoor Pervez, Zerish Kiran Jamil, Nimra Aslam, Rabia Latif, Fawad Khan, Nimra Akhtar, Sadia Amir, & Farman ali. (2024). THIAMETHOXAM-INDUCED NEUROTOXICITY AND GUT DAMAGE IN HONEYBEES (APIS MELLIFERA) MOLECULAR AND BEHAVIORAL EVIDENCE OF A SILENT THREAT. Journal of Population Therapeutics and Clinical Pharmacology, 31(4), 2339-2353. https://doi.org/10.53555/4dwqjb84
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Author Biographies
Tahira Minal
Department of Zoology Lahore College for Women University, Lahore, Pakistan.
Mahnoor Pervez
Department of Zoology Lahore College for Women University, Lahore Pakistan.
Zerish Kiran Jamil
Department of Zoology Lahore College for Women University, Lahore Pakistan
Nimra Aslam
Department of Zoology Lahore College for Women University, Lahore Pakistan.
Rabia Latif
Department of Zoology Lahore College for Women University, Lahore Pakistan.
Fawad Khan
Medical Entomologist, Health Department Khyber Pakhtunkhwa, Pakistan.
Nimra Akhtar
Department of Zoology Lahore College for Women University, Lahore Pakistan.
Sadia Amir
Department of Zoology Lahore College for Women University, Lahore Pakistan.
Farman ali
Entomology department Abdul Wali Khan University Mardan Khyber Pakhtunkhwa
How to Cite
Tahira Minal, Mahnoor Pervez, Zerish Kiran Jamil, Nimra Aslam, Rabia Latif, Fawad Khan, Nimra Akhtar, Sadia Amir, & Farman ali. (2024). THIAMETHOXAM-INDUCED NEUROTOXICITY AND GUT DAMAGE IN HONEYBEES (APIS MELLIFERA) MOLECULAR AND BEHAVIORAL EVIDENCE OF A SILENT THREAT. Journal of Population Therapeutics and Clinical Pharmacology, 31(4), 2339-2353. https://doi.org/10.53555/4dwqjb84