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تاثیرات دز زیرکشنده ایمیداکلوپرید بر واکنش پذیری زنبور عسل معمولیApis mellifera

نوع مقاله : مقاله پژوهشی

نویسندگان

1 گروه گیاهپزشکی، دانشکده علوم و مهندسی کشاورزی، پردیس کشاورزی و منابع طبیعی دانشگاه تهران، کرج

2 گروه گیاهپزشکی، پردیس کشاورزی و منابع طبیعی دانشگاه تهران، کرج، ایران

3 دپارتمان روانشناسی، دانشگاه ایالتی اوکلاهما، استیل واتر، امریکا

چکیده

ایمیداکلوپرید حشره‌کشی از گروه نئونیکوتینوئیدها که برای کنترل آفات کشاورزی به طور گسترده مورد استفاده قرار می‌گیرد. این حشره‌کش می‌تواند علاوه بر تاثیر بر روی حشرات آفت روی حشرات مفید از جمله زنبور عسل (Apis mellifera) تاثیر بگذارد. از آنجایی که یادگیری و حافظه، نقش مهمی در رفتار و ارتباط اجتماعی زنبور عسل دارد، هدف از این تحقیق بررسی یادگیری و حافظه زنبورهای عسل تیمارشده با دز زیرکشنده ایمیداکلوپرید با استفاده از روش واکنش انبساط خرطوم در شرایط کنترل شده آزمایشگاهی بود. در این آزمایش زنبور‌ عسل در پاسخ به تحریک شاخک‌ با ساکارز خرطوم خود را باز می‌کند. داده‌های حاصل از این تحقیق نشان داد که تیمار گوارشی زنبور عسل با این حشره‌کش بر مصرف آب، شربت غیرآلوده، و واکنش‌پذیری به آب، تاثیری نگذاشت. اما سبب کاهش عملکرد یادگیری، حافظه بویایی، بینایی، و واکنش پذیری به غلظت‌های مختلف ساکارز شد. نتایج ما نشان می‌دهد که تغییرات ایجاد شده توسط دز زیر کشنده ایمیداکلوپرید روی زنبور عسل معمولی برفعالیت واکنش پذیری آنها اثر گذاشته، که منجر به اختلال در رفتار چراگری شده و در نهایت سبب کاهش سلامت کلنی می‌شود

کلیدواژه‌ها


عنوان مقاله [English]

Effects of sublethal dose of imidacloprid on honey bee responsiveness Apis mellifera

نویسندگان [English]

  • Sahar Delkash-Roudsari 1
  • Seyed Hossein Goldansaz 2
  • Khalil Telebi-Jahromi 2
  • Ahmad Ashouri 2
  • Charles I. Abramson 3
1 Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran
2 Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran
3 Department of Psychology ,Oklahoma State University, Stillwater, Oklahoma, United States of America
چکیده [English]

Imidacloprid is an insecticide from the family of the neonicotinoids that is widely used to control agricultural pests. Furthermore, this insecticide can affect beneficial insects such as honey bee (Apis mellifera). Since learning and memory play an important role in honey bee behavior and social communication, the aim of this study was to investigate the learning and memory of honey bees treated with sublethal dose of imidacloprid using the proboscis extension reflex method under controlled laboratory conditions. In this experiment, honey bee extends its proboscis in response to antennal stimulation with sucrose. Data from this study showed that the oral treatment of honey bees with this insecticide did not affect water consumption, uncontaminated syrup and water responsiveness. But it reduced olfactory and visual learning and memory performances, and responsiveness to various sucrose concentrations. Therefore, our results show that the changes made by sublethal dose of imidacloprid have affected honey bee's responsiveness, which ultimately reduced colony health.

کلیدواژه‌ها [English]

  • Imidacloprid
  • Responsiveness
  • Learning and Memory
  • honey bee
  1. Abrol, D. P. (2013). Safety of Bees in Relation to Pest Management. In Asiatic Honey bee Apis cerana (pp. 575-640): Springer.
  2. Agin, V., Chichery, R., & Chichery, M.-P. (2001). Effects of learning on cytochrome oxidase activity in cuttlefish brain. Neuroreport, 12(1), 113-116.
  3. Aizen, M. A. & Harder, L. D. (2009). The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Current Biology, 19(11), 915-918.
  4. Al Naggar, Y., Wiseman, S., Sun, J., Cutler, G. C., Aboul-Soud, M., Naiem, E., Mona, M., Seif, A., & Giesy, J. P. (2015). Effects of environmentally-relevant mixtures of four common organophosphorus insecticides on the honey bee (Apis mellifera L.). Journal of Insect Physiology, 82, 85-91.
  5. Aliouane, Y., El Hassani, A. K., Gary, V., Armengaud, C., Lambin, M. & Gauthier, M. (2009). Subchronic exposure of honeybees to sublethal doses of pesticides: effects on behavior. Environmental Toxicology and Chemistry, 28(1), 113-122.
  6. Bascompte, J., Jordano, P. & Olesen, J. M. (2006). A symmetric coevolutionary networks facilitate biodiversity maintenance. Science, 312(5772), 431-433.
  7. Bee Culture. (2018). Iran is either third, or fourth in global honey production. Maybe. Bee Culture.
  8. Belzunces, L. P., Tchamitchian, S., & Brunet, J.-L. (2012). Neural effects of insecticides in the honey bee. Apidologie, 43(3), 348-370.
  9. Bitterman, M., Menzel, R., Fietz, A. & Schäfer, S. (1983). Classical conditioning of proboscis extension in honey bees (Apis mellifera). Journal of Comparative Psychology, 97(2), 107.

10. Bonmatin, J., Moineau, I., Charvet, R., Fleche, C., Colin, M. & Bengsch, E. (2003). A LC/APCI-MS/MS method for analysis of imidacloprid in soils, in plants, and in pollens. Analytical Chemistry, 75(9), 2027-2033.

11. Cresswell, J. E., Desneux, N. & van Engelsdorp, D. (2012). Dietary traces of neonicotinoid pesticides as a cause of population declines in honey bees: an evaluation by Hill's epidemiological criteria. Pest Management Science, 68(6), 819-827.

12. Cure, G., Schmidt, H. & Schmuck, R. (2000). Results of a comprehensive field research programme with the systemic insecticide imidacloprid (Gaucho). IOBC WPRS Bulletin, 23(3), 6-6.

13. Decourtye, A., Devillers, J., Genecque, E., Le Menach, K., Budzinski, H., Cluzeau, S. & Pham-Delegue, M. (2005). Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honey bee Apis mellifera. Archives of Environmental Contamination and Toxicology, 48(2), 242-250.

14. Démares, F. J., Crous, K. L., Pirk, C. W., Nicolson, S. W. & Human, H. (2016). Sucrose sensitivity of honey bees is differently affected by dietary protein and a neonicotinoid pesticide. PloS One, 11(6), e0156584.

15. Desneux, N., Decourtye, A. & Delpuech, J.-M. (2007). The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52, 81-106.

16. Dobrin, S. E. & Fahrbach, S. E. (2012). Visual associative learning in restrained honey bees with intact antennae. PloS One, 7(6), e37666.

17. Eiri, D. M. & Nieh, J. C. (2012). A nicotinic acetylcholine receptor agonist affects honey bee sucrose responsiveness and decreases waggle dancing. Journal of Experimental Biology, 215(12), 2022-2029.

18. 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, 11779.

19. European and Mediterranean Plant Protection Organization (EPPO). (1992). Guideline on test methods for evaluating the side-effects of plant protection products on honey bees. EPPO Bulletin, 22, 203–215.

20. Fontaine, C., Dajoz, I., Meriguet, J. & Loreau, M. (2005). Functional diversity of plant–pollinator interaction webs enhances the persistence of plant communities. PLoS Biology, 4(1), e1.

21. Frings, H. & Frings, M. (1949). The loci of contact chemoreceptors in insects. A review with new evidence. American Midland Naturalist, 602-658.

22. Giurfa, M. (2007). Behavioral and neural analysis of associative learning in the honey bee: a taste from the magic well. Journal of Comparative Physiology A, 193(8), 801-824.

23. Giurfa, M. & Sandoz, J.-C. (2012). Invertebrate learning and memory: fifty years of olfactory conditioning of the proboscis extension response in honey bees. Learning & Memory, 19(2), 54-66.

24. Goulson, D. (2013). An overview of the environmental risks posed by neonicotinoid insecticides. Journal of Applied Ecology, 50(4), 977-987.

25. Goulson, D., Nicholls, E., Botías, C. & Rotheray, E. L. (2015). Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347(6229), 1255957.

26. Han, P., Niu, C.-Y., Lei, C.-L., Cui, J.-J. & Desneux, N. (2010). Use of an innovative T-tube maze assay and the proboscis extension response assay to assess sublethal effects of GM products and pesticides on learning capacity of the honey bee Apis mellifera L. Ecotoxicology, 19(8), 1612-1619.

27. Iqbal, J., Alqarni, A. & Raweh, H. (2018). Effect of sub-lethal doses of imidacloprid on learning and memory formation of indigenous Arabian bee (Apis mellifera jemenitica Ruttner) adult foragers. Neotropical Entomology, 1-8.

28. Jeschke, P. & Nauen, R. (2008). Neonicotinoids—from zero to hero in insecticide chemistry. Pest Management Science : Formerly Pesticide Science, 64(11), 1084-1098.

29. Klein, A. M., Vaissiere, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C. & Tscharntke, T. (2006). Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences, 274(1608), 303-313.

30. Laurino, D., Manino, A., Patetta, A. & Porporato, M. (2013). Toxicity of neonicotinoid insecticides on different honey bee genotypes. Bulletin of Insectology, 66(1), 119-126.

31. Lonsdorf, E., Ricketts, T., Kremen, C., Winfree, R., Greenleaf, S. & Williams, N. (2011). Crop pollination services. Natural capital. Theory and practice of mapping ecosystem services. Oxford University Press, Oxford, 168-187.

32. Matsumoto, Y., Menzel, R., Sandoz, J.-C & .Giurfa, M. (2012). Revisiting olfactory classical conditioning of the proboscis extension response in honey bees: a step toward standardized procedures. Journal of Neuroscience Methods, 211(1), 159-167.

33. 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.

34. Menzel, R. (1999). Memory dynamics in the honeybee. Journal of Comparative Physiology A, 185(4), 323-340.

35. Miranda, J. E., Navickiene, H. M. D., Nogueira-Couto, R. H., De Bortoli, S. A., Kato, M. J., da Silva Bolzani, V. & Furlan, M. (2003). Susceptibility of Apis mellifera (Hymenoptera: Apidae) to pellitorine, an amide isolated from Piper tuberculatum (Piperaceae). Apidologie, 34(4), 409-415.

36. Müller, U. (2000). Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honey bees. Neuron, 27(1), 159-168.

37. Page Jr, R., Erber, J. & Fondrk, M. (1998). The effect of genotype on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.). Journal of Comparative Physiology A, 182(4), 489-500.

38. Pankiw, T. & Page, R. (2003). Effect of pheromones, hormones, and handling on sucrose response thresholds of honey bees (Apis mellifera L.). Journal of Comparative Physiology A, 189(9), 675-684.

39. Pavlov, I. (1927). Conditioned Reflexes.(1960 reprint). In: New York: Dover Books.

40. Pham-Delègue, M.-H., Decourtye, A., Kaiser, L. & Devillers, J. (2002). Behavioural methods to assess the effects of pesticides on honey bees. Apidologie, 33(5), 425-432.

41. Ramirez-Romero, R., Desneux, N., Decourtye, A., Chaffiol, A. & Pham-Delègue, M. (2008). Does Cry1Ab protein affect learning performances of the honey bee Apis mellifera L.(Hymenoptera, Apidae)? Ecotoxicology and Environmental Safety, 70(2), 327-333.

42. Ramirez-Romero, R., Chaufaux, J., Pham-Delègue, M. (2005). Effects of Cry1Ab protoxin, deltamethrin and imidacloprid on the foraging activity and the learning performances of the honey bee Apis mellifera, a comparative approach. Apidologie. 36, 601-611.

43. Scheiner, R., Page, R. E. & Erber, J. (2004). Sucrose responsiveness and behavioral plasticity in honey bees (Apis mellifera). Apidologie, 35(2), 133-142.

44. Schmuck, R., Nauen, R. & Ebbinghaus-Kintscher, U. (2003). Effects of imidacloprid and common plant metabolites of imidacloprid in the honey bee: toxicological and biochemical considerations. Bulletin of Insectology, 56(1), 27-34.

45. Schmuck, R., Schöning, R., Stork, A. & Schramel, O. (2001). Risk posed to honey bees (Apis mellifera L, Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Management Science: formerly Pesticide Science, 57(3), 225-238.

46. Suchail, S., Debrauwer, L. & Belzunces, L. P. (2004). Metabolism of imidacloprid in Apis mellifera. Pest Management Science: formerly Pesticide Science, 60(3), 291-296.

47. Tavares, D. A., Dussaubat, C., Kretzschmar, A., Carvalho, S. M., Silva-Zacarin, E. C., Malaspina, O., Geraldine, B., Brunet, J. L. & Belzunces, L. P. (2017). Exposure of larvae to thiamethoxam affects the survival and physiology of the honey bee at post-embryonic stages. Environmental Pollution, 229, 386-393.

48. Tavares, D. A., Roat, T. C., Carvalho, S. M., Silva-Zacarin, E. C. M. & Malaspina, O. (2015). In vitro effects of thiamethoxam on larvae of Africanized honey bee Apis mellifera (Hymenoptera: Apidae). Chemosphere, 135, 370-378.

49. Thompson, H. M. (2003). Behavioural effects of pesticides in bees–their potential for use in risk assessment. Ecotoxicology, 12(1-4), 317-330.

50. Whitehorn, P. R., O’connor, S., Wackers, F. L. & Goulson, D. (2012). Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science, 1215025.

51. Williamson, S. M., Baker, D. D. & Wright, G. A. (2013). Acute exposure to a sublethal dose of imidacloprid and coumaphos enhances olfactory learning and memory in the honey bee Apis mellifera. Invertebrate Neuroscience, 13(1), 63-70.

52. Wu, J. Y., Anelli, C. M. & Sheppard, W. S. (2011). Sub-lethal effects of pesticide residues in brood comb on worker honey bee (Apis mellifera) development and longevity. PloS One, 6(2), e14720.

53. Yang, E., Chuang, Y., Chen, Y. & Chang, L. (2008). Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). Journal of Economic Entomology, 101(6), 1743-1748.