Evidence of diet supplementation with vitamin C protecting honeybees from Imidacloprid induced peroxidative damage: a study with Apis cerana indica
DOI:
https://doi.org/10.13102/sociobiology.v69i3.7763Keywords:
neonicotinoids, ascorbic acid, antioxidant enzymes, peritrophic membrane, honey beesAbstract
Neonicotinoids are one of the major stresses contributing to the decline in the population of honeybees. Worker bees are prone to various stress factors during foraging and are susceptible to Imidacloprid due to the reduction in the number of genes encoding for the major enzyme families responsible for the detoxification of toxins. The present study worked on the hypothesis that the dietary supplementation of Ascorbic acid (VIT C) could reduce the peroxidative damage in the worker bees of Apis cerana indica exposed to sub-lethal concentration of imidacloprid (IMD). Furthermore, we also evaluated the role and efficacy of VIT C supplementation on the cytoarchitecture of midgut tissues on exposure to IMD. Colonies of honeybees were maintained by providing sugar syrup to the control group and sugar syrup supplemented with 0.2% VIT C for the experimental group for six months. Worker bees from both groups were randomly collected and exposed to 0.001 mg/mL IMD. To study the peroxidative damage, the activities of various enzymes were analyzed. The activities of antioxidant enzymes including Catalase, Superoxide Dismutase, Glutathione S Transferase, and Glutathione Peroxidase in the hemolymph and midgut tissues of worker bees were significantly decreased due to exposure to IMD as a single agent. However, their activities showed a significant elevation under diet supplementation with VIT C. Histological examination revealed midgut tissue damage and the rupture of peritrophic membrane among the workers exposed to IMD as compared with the control group. The damage to the midgut was alleviated and the peritrophic membrane was found to be intact in the worker bees supplemented with VIT C. Our results indicated that the dietary supplementation of VIT C has the potential to maintain the redox status and thereby can offer protective potential against the peroxidative damages induced by the sub-lethal concentration of IMD.
Downloads
References
Andi, M.A. & Ahmadi, A. (2014). Influence of vitamin C in sugar syrup on brood area, colony population, body weight and protein in honeybees. International Journal of Biosciences, 4: 32-36. doi:10.12692/ijb/4.6.32-36.
Balieira, K.V.B., Mazzo, M., Bizerra, P.F.V., Guimarães, A.R.D.J.S., Nicodemo, D. & Mingatto, F.E. (2018). Imidacloprid- induced oxidative stress in honey bees and the antioxidant action of caffeine. Apidologie, 49: 562-572. doi: 10.1007/s13592-018-0583-1.
Bendich, A., (1990). Antioxidant Micronutrients and Immune Responses, Micronutrients and Immune Functions. New York Academy of Sciences, New York. p. 175.
Bielenin, I. & Ibek, Z. (1980). Influence of sodium fluoride on the midgut epithelium of the honey bee, Apis mellifera L. (Apidae, Hymenoptera). Zeszyty Naukowe Akademii Rolniczej w Krakowie. Zootechnika, 20159: 49-69.
Bindhumol, V., Chitra, K.C. & Mathur, P.P., (2003). Bisphenol A induces reactive oxygen species generation in the liver of male rats. Toxicology, 188: 117-124. doi: 10.1016/S0300-483X(03)00056-8
Blacquiere, T., Smagghe, G., Van Gestel, C.A. & Mommaerts, V. (2012). Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology, 21: 973-992. doi: 10.1007/s10646-012-0863-x.
Bryden, J., Gill, R.J., Mitton, R.A., Raine, N.E. & Jansen, V.A. (2013). Chronic sublethal stress causes bee colony failure. Ecology Letters, 16: 1463-1469. doi:10.1111/ele.12188
Carreck, N.L., Andree, M., Brent, C.S., Cox-Foster, D., Dade, H.A., Ellis, J.D. & Van Englesdorp, D. (2013). Standard methods for Apis mellifera anatomy and dissection. Journal of Apicultural Research, 52: 1-40. doi: 10.3896/IBRA.1.52.4.03.
Casida J.E. & Durkin K.A. (2013). Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annual Review of Entomology. 58: 99-117, doi: 10.1146/annurev-ento-120811-153645
Chance, B., Sies, H. & Boveris, A. (1979). Hydroperoxide metabolism in mammalian organs. Physiological Reviews, 59: 527-605. doi: 10.1152/physrev.1979.59.3.527
Corona, M., & Robinson, G.E. (2006). Genes of the antioxidant system of the honeybee: annotation and phylogeny. Insect Molecular Biology, 15: 687-701.doi: 10.1111/j.1365-2583. 2006.00695.x.
Crailsheim, K. (1988). Transport of leucine in the alimentary canal of the honeybee (Apis mellifera L.) and its dependence on season. Journal of Insect Physiology, 34: 1093-1100. doi: 10.1016/0022-1910(88)90210-7.
David, M & Richard, J.S. (1983). In: Methods of enzymatic analysis. Bergmeyer, J and Grab M. (Eds), Verlag Chemie Wenhein Deer Field, Beach Floride, Pp 358.
Decourtye, A., Armengaud, C., Renou, M., Devillers, J., Cluzeau, S., Gauthier, M. & Pham-Delègue, M.H. (2004). Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.). Pesticide Biochemistry and Physiology, 78: 83-92. doi: 10.1016/j.pestbp.2003.10.001.
Deisseroth, A. & Dounce, A.L. (1970). Catalase: Physical and chemical properties, mechanism of catalysis, and physiological role. Physiological Reviews, 50: 319-375. doi: 10.1152/physrev. 1970.50.3.319.
Di Prisco, G., Cavaliere, V., Annoscia, D., Varricchio, P., Caprio, E., Nazzi, F. & Pennacchio, F. (2013). Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proceedings of the National Academy of Sciences, 110: 18466-18471. doi: 10.1073/pnas.1314923110.
Egaas, E., Sandvik, M., Fjeld, E., Kallqvist, T., Goksoyr, A. & Svensen, A. (1999). Some effects of the fungicide propiconazole on cytochrome P450 and glutathione S-transferase in brown trout (Salmotrutta). Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology, 122: 337-344. doi: 10.1016/S0742-8413(98)10133-0.
El-Gendy, K.S., Aly, N.M., Mahmoud, F.H., Kenawy, A. & El-Sebae, A.K.H. (2010). The role of vitamin C as antioxidant in protection of oxidative stress induced by imidacloprid. Food and Chemical Toxicology, 48: 215-221. doi:10.1016/j.fct.2009.10.003.
Enayati, A.A., Ranson, H. & Hemingway, J. (2005). Insect glutathione transferases and insecticide resistance. Insect Molecular Biology, 14: 3-8. doi: 10.1111/j.1365-2583.2004. 00529.x.
Esther, E., Smit, S., Beukes, M., Apostolides, Z., Pirk, C.W., & Nicolson, S.W. (2015). Detoxification mechanisms of honey bees (Apis mellifera) resulting in tolerance of dietary nicotine. Scientific Reports, 5: 1-11. doi: 10.1038/srep11779.
Farjan, M., Dmitryjuk, M., Lipinski, Z., Biernat-Lopienska, E. & Żołtowska, K. (2012). Supplementation of the honeybee diet with vitamin C: The effect on the antioxidative system of Apis Mellifera carnica brood at different stages. Journal of Apicultural Research, 51: 263-270. doi: 10.3896/IBRA. 1.51.3.07.
Godfray, H.C.J., Blacquiere, T., Field, L. M., Hails, R.S., Petrokofsky, G., Potts, S.G. & McLean, A.R. (2014). A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proceedings of the Royal Society B: Biological Sciences, 281: 20140558. doi: 10.1098/rspb.2014.0558.
Goth, L., Rass, P. & Pay, A. (2004). Catalase enzyme mutations and their association with diseases. Molecular Diagnosis, 8: 141-149. doi:10.1007/BF03260057.
Habig, W.H. Pabst, M.J. & Jokoby, W.B. (1974). Glutathione transferase: A first enzymatic step in mercapturic acid III formation. Journal of Biological Chemistry, 249: 7130-7139. doi: 10.1016/S0021-9258(19)42083-8.
Han, P., Niu, C.Y., Biondi, A., Desneux, N., (2012). Does transgenic Cry1Ac + CpTI cotton pollen affect hypopharyngeal gland development and midgut proteolytic enzyme activity in the honey bee Apis mellifera L. (Hymenoptera, Apidae) Ecotoxicology, 21: 2214-2221. doi: 10.1007/s10646-012-0976-2.
Henry, M., Beguin, M., Requier, F., Rollin, O., Odoux, J.F., Aupinel, P. & Decourtye, A. (2012). A common pesticide decreases foraging success and survival in honey bees. Science, 336: 348-350. doi: 10.1126/science.1215039.
Higes, M., Meana, A., Bartolome, C., Botías, C. & Martín Hernandez, R. (2013). Nosema ceranae (Microsporidia), a controversial 21st century honeybee pathogen. Environmental Microbiology Reports, 5: 17-29. doi: 10.1111/1758-2229.12024.
Hinton, B.T., Palladino, M.A., Rudolph, D. & Labus, J.C. (1995). The epididymis as protector of maturing spermatozoa. Reproduction, Fertility and Development, 7: 731-745.
Ho, Y.S., Xiong, Y., Ma, W., Spector, A. & Ho, D.S. (2004). Mice lacking catalase develop normally but show differential sensitivity to oxidant tissue injury. Journal of Biological Chemistry, 279: 32804-32812. doi: 10.1074/jbc.M404800200.
Hodgson, E., Smart, R.C. (2001). Introduction to Biochemical Toxicology, in: Wiley-Inter Science (3 Eds.), Hoboken, pp. 309-323.
Jakoby, W.B. (1985). Glutathione transferases: An Overview. Methods in Enzymology, 113: 495-499. doi: 10.1016/S0076-6879(85)13064-8.
Jefferies, H., Coster, J., Khalil, A., Bot, J., McCauley, R.D. & Hall, J.C. (2003). Glutathione. ANZ Journal of Surgery, 73: 517-522. doi: 10.1046/j.1445-1433.2003.02682.x.
Kapoor, U., Srivastava, M.K., Bhardwaj, S. & Srivastava, L.P. (2010). Effect of imidacloprid on antioxidant enzymes and lipid peroxidation in female rats to derive its No Observed Effect Level (NOEL). The Journal of Toxicological Sciences, 35: 577-581. doi: 10.2131/jts.35.577.
Kirkman, H.N. & Gaetani, G.F. (2007). Mammalian catalase: a venerable enzyme with new mysteries. Trends in Biochemical Sciences, 32: 44-50. doi: 10.1016/j.tibs.2006.11.003.
Lee, K. (1991). Glutathione S-transferase activities in phytophagous insects: induction and inhibition by plant phototoxins and phenols. Insect Biochemistry, 21: 353-361. doi: 10.1016/0020-1790(91)90001-U.
Lehane, M.J. (1997). Peritrophic matrix structure and function. Annual Review of Entomology, 42: 525-550. doi: 10.1146/annurev.ento.42.1.525.
Luck, H. (1963). Methods of enzymatic analysis. Enzyme Assays in-vivo. New York, London: Academic Press.
Mannervik, B. (1985). Glutathione peroxidase. In Methods in Enzymology, 113: 490-495. Academic Press. doi: 10.1016/S0076-6879(85)13063-6.
Matsuda, K., Buckingham, S.D., Kleier, D., Rauh, J.J., Grauso, M. & Sattelle, D.B. (2001). Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends in Pharmacological Sciences, 22: 573-580. doi: 10.1016/S0165-6147(00)01820-4.
Medrzycki, P., Giffard, H., Aupinel, P., Belzunces, L.P., Chauzat, M.P., Claßen, C. & Vidau, C. (2013). Standard methods for toxicology research in Apis mellifera. Journal of Apicultural Research, 52: 1-60. doi: 10.3896/IBRA.1.52.4.14.
Medrzycki, P., Montanari, R., Bortolotti, L., Sabatini, A.G., Maini, S. & Porrini, C. (2003). Effects of imidacloprid administered in sub-lethal doses on honey bee behaviour. Laboratory tests. Bulletin of Insectology, 56: 59-62.
Milton, N.G. (2004). Role of hydrogen peroxide in the aetiology of Alzheimer’s disease. Drugs and Aging, 21: 81-100.
Nicodemo, D., Maioli, M.A., Medeiros, H.C., Guelfi, M., Balieira, K.V., De Jong, D. & Mingatto, F.E. (2014). Fipronil and imidacloprid reduce honeybee mitochondrial activity. Environmental Toxicology and Chemistry, 33: 2070-2075. doi:10.2165/00002512-200421020-00002.
Paoletti, F., Aldinucci, D., Mocali, A. & Caparrini, A. (1986). A sensitive spectrophotometric method for the determination of superoxide dismutase activity in tissue extracts. Analytical
Biochemistry, 154: 536-541. doi: 10.1016/0003-2697(86)90026-6.
Pawert, M., Triebskorn, R., Graff, S., Berkus, M., Schulz, J. & Köhler, H.R. (1996). Cellular alterations in collembolan midgut cells as a marker of heavy metal exposure: ultrastructure and intracellular metal distribution. Science of The Total Environment, 181: 187-200. doi: 10.1016/0048-9697(95)05009-4.
Reddy, K.P., Subhani, S.M., Khan, P.A., & Kumar, K.B. (1985). Effect of light and benzyladenine on dark-treated growing rice (Oryza sativa) leaves II. Changes in peroxidase activity. Plant and Cell Physiology, 26: 987-994. doi: 10.1093/oxfordjournals.pcp.a077018.
Rotruck, T.T., Ganther, H.E., Swanson, A.B., Hafeman, D.G. & Hoeckstra, W.G. (1973). Selenium: Biochemical role as a component of glutathione peroxidase. Science, 179: 588-590. doi: 10.1126/science.179.4073.588.
Snodgrass, R.E. (2018). Anatomy of the honey bee. Cornell University Press.
Strachecka, A., Chobotow, J., Paleolog, J., Los, A., Schulz, M., Teper, D. & Grzybek, M. (2017). Insights into the biochemical defence and methylation of the solitary bee Osmia rufa L: A foundation for examining eusociality development. Plos One, 12: e0176539. doi: 10.1371/journal.pone.0176539.
Strachecka, A., Krauze M., Olszewski, K., Borsuk, G., Paleolog, J., Merska M., Chobotow, J., Bajda, M. & Grzywnowicz, K. (2014). Unexpectedly strong effect of caffeine on the vitality of western honeybees (Apis mellifera). Biochemistry, 79: 1192-1201. doi: 10.1134/S0006297914110066.
Suchail, S., Debrauwer, L. & Belzunces, L.P. (2004). Metabolism of imidacloprid in Apis mellifera. Pest Management Science: formerly Pesticide Science, 60: 291-296. doi: 10.1002/ps.772.
Szymas, B. & Przybyl, A. (2007). Midgut histological picture of the honey bee (Apis mellifera L.) following consumption of substitute feeds supplemented with feed additives. Nauka Przyroda Technologie, 1: 48.
Szymas, B., Langowska, A. & Kazimierczak-Baryczko, M. (2012). Histological structure of the midgut of honeybees (Apis mellifera L.) fed pollen substitutes fortified with probiotics. Journal of Apicultural Science, 56: 5-12. doi: 10.2478/v10289- 012-0001-2.
Terra, W.R., Espinoza-Fuentes, F.P., Ribeiro, A.F. & Ferreira, C. (1988). The larval midgut of the housefly (Musca domestica): ultrastructure, fluid fluxes and ion secretion in relation to the organization of digestion. Journal of Insect Physiology, 34: 463-472. doi: 10.1016/0022-1910(88)90187-4.
Thangudu, S. & Su, C.H., (2021). Peroxidase mimetic nanozymes in cancer phototherapy: Progress and perspectives. Biomolecules, 11: 1015. doi: 10.3390/biom11071015.
Townsend, D.M. & Tew, K.D., (2003). The role of glutathione-S-transferase in anti-cancer drug resistance. Oncogene, 22: 7369-7375. doi:10.1038/sj.onc.1206940.
Verma, R.S., Mehta, A. & Srivastava, N. (2007). In vivo chlorpyrifos induced oxidative stress: attenuation by antioxidant vitamins. Pesticide Biochemistry and Physiology, 88: 191-196. doi: 10.1016/j.pestbp.2006.11.002.
Weirich, G.F., Collins, A.M. & Williams, V.P. (2002). Antioxidant enzymes in the honeybee, Apis mellifera. Apidologie, 33: 3-14 doi: 10.1051/apido:200100.
Yang, E.C., Chuang, Y.C., Chen, Y.L. & Chang, L.H. (2008). Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). Journal of Economic Entomology, 101: 1743-1748. doi: 10.16 03/0022-0493-101.6.1743.
Younus, H. (2018). Therapeutic potentials of superoxide dismutase. International Journal of Health Sciences, 12: 88.
Yucel, M.S. & Kayis, T. (2019). Imidacloprid induced alterations in oxidative stress, biochemical, genotoxic, and immunotoxic biomarkers in non-mammalian model organism Galleria mellonella L. (Lepidoptera: Pyralidae). Journal of Environmental Science and Health, Part B, 54: 27-34. doi: 10.1080/03601234.2018.1530545.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2022 Syama P. S., Sreeranjit Kumar C. V.
This work is licensed under a Creative Commons Attribution 4.0 International License.
Sociobiology is a diamond open access journal which means that all content is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles in this journal without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of open access.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
eISSN 2447-8067
