Effect of Flupyradifurone Insecticides on Memory and Learning Behavior in Bombus terrestris Workers

Öz

This study aimed to determine the effects of Flupyradifurone (FPF), identified as a novel insecticide, on the learning and memory abilities of Bombus terrestris workers. In the research, the learning and memory performance of workers fed with sugar syrup containing different concentrations of FPF (0, 1/100, 1/10, 1/1, 2/1 of the recommended application dose of 60 ml/100 L water) was tested. The study involved applications that assessed the worker bees’ responses to lavender scent through classical conditioning and tested their memory at specific time intervals. The findings revealed that exposure to FPF did not significantly impair the bees' learning and memory abilities. However, the group exposed to the highest concentration demonstrated slower learning rates and reduced memory performance. This study highlights the potential neurotoxic effects of FPF and its negative impact on the foraging abilities of bumblebees, emphasizing the ecological risks of insecticides marketed as environmentally friendly. The results underscore the need for further comprehensive research on the environmental impacts of FPF.

Anahtar Kelimeler

• Bumblebee
• Bombus terrestris
• Flupyradifurone
• Learning and memory

Yeni Nesil İnsektisit Flupyradifurone’un Bombus terrestris İşçi Arılarının Öğrenme ve Hafıza Davranışına Etkisi

Öz

Bu çalışmada, yeni nesil insektisit olarak tanımlanan Flupyradifurone’un (FPF) Bombus terrestris işçi arılarının öğrenme ve hafıza yetenekleri üzerine etkilerinin belirlenmesi amaçlanmıştır. Araştırmada, FPF’nin önerilen uygulama dozunu (60 ml/100 L.su) farklı oranlarda (0, 1/100, 1/10, 1/1, 2/1) içeren şeker şurubu ile beslenen arıların öğrenme ve hafıza performansları test edilmiştir. Araştırma kapsamında, işçi arıların lavanta kokusuna klasik koşullandırma yöntemiyle tepkileri ve belirli zaman dilimlerinde hafızalarını test eden uygulamalar gerçekleştirilmiştir. Bulgulara göre, FPF’ye maruz kalan arıların öğrenme ve hafıza yeteneklerinin önemli ölçüde etkilenmediği belirlenmiştir. Ancak, en yüksek doz uygulanan grupta öğrenme hızının ve hafıza yeteneğinin düşük olduğu tespit edilmiştir. Bu çalışma, FPF’nin nörotoksik etkilerini ve bombus arılarının tarlacılık yeteneklerini olumsuz etkileyebileceğini ortaya koyarak, çevre dostu olarak sunulan insektisitlerin ekolojik risklerini vurgulamaktadır. Çalışma sonuçları, FPF’nin çevresel etkileri üzerine daha kapsamlı araştırmalara duyulan ihtiyacı ortaya koymaktadır.

Anahtar Kelimeler

• bombus arısı
• Bombus terrestris
• Flupyradifurone
• Öğrenme ve hafıza

Kaynakça

1. Akçay, A., Erkan, C., 2024. Bombus Arılarında Polen Tercihi. Hayvan Bilimi ve Ürünleri Dergisi. 7(2): 112-120.
2. 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: An International Journal. 28(1): 113-122.
3. Allsopp, M. H., De Lange, W. J., Veldtman, R., 2008. Valuing insect pollination services with cost of replacement. PloS One. 3(9): e3128.
4. Annoscia, D., Di Prisco, G., Becchimanzi, A., Caprio, E., Frizzera, D., Linguadoca, A., Pennacchio, F., 2020. Neonicotinoid Clothianidin reduces honey bee immune response and contributes to Varroa mite proliferation. Nature Communications. 11(1): 5887.
5. Bell, H. C., Montgomery, C. N., Benavides, J. E., Nieh, J. C., 2020. Effects of Nosema ceranae (Dissociodihaplophasida: Nosematidae) and flupyradifurone on olfactory learning in honey bees, Apis mellifera (Hymenoptera: Apidae). Journal of Insect Science. 20(6): 29.
6. Belsky, J., Joshi, N. K., 2019. Impact of biotic and abiotic stressors on managed and feral bees. Insects. 10(8): 233.
7. Bitterman, M. E., Menzel, R., Fietz, A., Schäfer, S., 1983. Classical conditioning of proboscis extension in honeybees (Apis mellifera). Journal of Comparative Psychology. 97(2): 107.
8. Branchiccela, B., Castelli, L., Corona, M., Díaz-Cetti, S., Invernizzi, C., Martínez De La Escalera, G., Antúnez, K., 2019. Impact of nutritional stress on the honeybee colony health. Scientific Reports. 9(1): 10156.

9. Brandt, A., Gorenflo, A., Siede, R., Meixner, M., Büchler, R., 2016. The neonicotinoids thiacloprid, imidacloprid, and clothianidin affect the immunocompetence of honey bees (Apis mellifera L.). Journal of Insect Physiology. 86: 40-47.
10. Buluş, İ. Y., Uzun, A., Demirözer, O., Gösterit, A., 2020. Acetamipridin Bombus (Bombus terrestris L.) Arılarında Kuluçka Gelişimi Üzerine Etkisi. Ziraat Fakültesi Dergisi. 15(1): 91-99.
11. Buluş, İ. Y., Timuroğlu, S., Gösterit, A., 2024. Neonikotinoid İnsektisitlerin Bombus (Bombus terrestris L.) Arısı Bireylerinde Hafıza ve Öğrenme Davranışına Etkisi. Hayvan Bilimi ve Ürünleri Dergisi. 7(1): 30-41.
12. Çakıcı, Ö., Uysal, M., Demirözer, O., Gösterit, A., 2023a. Effects of thiamethoxam on brain structure of Bombus terrestris (Hymenoptera: Apidae) workers. Chemosphere. 338: 139595.
13. Çakıcı, Ö., Uysal, M., Demirözer, O., & Gösterit, A., 2023b. Sublethal effects of thiamethoxam on immune system cells in the workers of Bombus terrestris (Hymenoptera: Apidae). Environmental Science and Pollution Research. 30(37): 87424-87432.
14. Chen, Y. R., Tzeng, D. T., Lin, S. S., Yang, E. C., 2024. Sublethal imidacloprid administration to honey bee workers is more lethal to the queen larvae. Environmental Toxicology and Chemistry. 43(10): 2232-2242.
15. Decourtye, A., Armengaud, C., Renou, M., Devillers, J., Cluzeau, S., Gauthier, M., Pham-Delègue, M. H., 2004.
16. Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.). Pesticide Biochemistry and Physiology. 78(2): 83-92.
17. Desneux, N., Decourtye, A., Delpuech, J. M., 2007. The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology. 52(1): 81-106.
18. El Hassani, A. K., Dacher, M., Gary, V., Lambin, M., Gauthier, M., Armengaud, C., 2008. Effects of sublethal doses of acetamiprid and thiamethoxam on the behavior of the honeybee (Apis mellifera). Archives of Environmental Contamination and Toxicology. 54: 653-661.
19. FAO, 2024. Pesticides use and trade – 1990–2022. FAOSTAT Analytical Briefs, No. 89. Rome.
20. Gill, R. J., Raine, N. E., 2014. Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure. Functional Ecology. 28(6): 1459-1471.
21. Goulson, D., Nicholls, E., 2022. Anthropogenic influences on bee foraging. Science. 375(6584): 970-972.
22. Gösterit, A., Erkan, C., 2021. Growth characteristics of commercial bumblebee colonies in open field conditions may be evidence for their invasion potential. Bee Studies. 13(1): 5-8.
23. Gray, L. K., Hulsey, M., Siviter, H., 2024. A novel insecticide impairs bumblebee memory and sucrose responsiveness across high and low nutrition. Royal Society Open Science. 11(5): 231798.
24. Hendriksma, H. P., Shafir, S., 2016. Honey bee foragers balance colony nutritional deficiencies. Behavioral Ecology and Sociobiology. 70: 509-517.
25. 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(6079): 348-350.
26. Hesselbach, H., Scheiner, R., 2018. Effects of the novel pesticide flupyradifurone (Sivanto) on honeybee taste and cognition. Scientific Reports. 8(1): 4954.
27. Hesselbach, H., Seeger, J., Schilcher, F., Ankenbrand, M., Scheiner, R., 2020. Chronic exposure to the pesticide flupyradifurone can lead to premature onset of foraging in honeybees Apis mellifera. Journal of Applied Ecology. 57(3): 609-618.
28. Ichikawa, N., Sasaki, M., 2003. Importance of social stimuli for the development of learning capability in honeybees. Applied Entomology and Zoology. 38(2): 203-209.
29. IRAC, Insecticide Resistance Action Committee. https://irac-online.org/mode-of-action/classification-online/ Erişim Tarihi: 11.12.2024.
30. Iwasa, T., Motoyama, N., Ambrose, J. T., Roe, R. M., 2004. Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Protection. 23(5): 371-378.
31. Keodara, A., Jeker, L., Straub, L., Grossar, D., Müller, J., Christen, V., 2024. Novel fungicide and neonicotinoid insecticide impair flight behavior in pollen foraging honey bees, Apis mellifera. Scientific Reports. 14(1): 22865.
32. Klein, A. M., Vaissière, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C., Tscharntke, T., 2007. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences. 274(1608): 303-313.
33. Koch, H., Brown, M. J., Stevenson, P. C., 2017. The role of disease in bee foraging ecology. Current Opinion in Insect Science. 21: 60-67.
34. Laloi, D., Pham-Delègue, M. H., 2004. Bumble bees show asymmetrical discrimination between two odors in a classical conditioning procedure. Journal of Insect Behavior. 17: 385-396.
35. Laycock, I., Lenthall, K. M., Barratt, A. T., Cresswell, J. E., 2012. Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology. 21: 1937-1945.
36. Li, Y., Miao, R., Khanna, M., 2020. Neonicotinoids and decline in bird biodiversity in the United States. Nature Sustainability. 3(12): 1027-1035.
37. Macias-Macias, J. O., Tapia-Rivera, J. C., De la Mora, A., Tapia-González, J. M., Contreras-Escareño, F., Petukhova, T., ..., Guzman-Novoa, E., 2020. Nosema ceranae causes cellular immunosuppression and interacts with thiamethoxam to increase mortality in the stingless bee Melipona colimana. Scientific Reports. 10(1): 17021.
38. Menzel, R., 1993. Associative learning in honey bees. Apidologie. 24(3): 157-168.
39. Mc Cabe, S. I., Hartfelder, K., Santana, W. C., Farina, W. M., 2007. Odor discrimination in classical conditioning of proboscis extension in two stingless bee species in comparison to Africanized honeybees. Journal of Comparative Physiology A. 193: 1089-1099.
40. Monchanin, C., Henry, M., Decourtye, A., Dalmon, A., Fortini, D., Bœuf, E., ..., Fourrier, J., 2019. Hazard of a neonicotinoid insecticide on the homing flight of the honeybee depends on climatic conditions and Varroa infestation. Chemosphere. 224: 360-368.
41. Morfin, N., Goodwin, P. H., Correa-Benitez, A., Guzman-Novoa, E. 2019. Sublethal exposure to clothianidin during the larval stage causes long-term impairment of hygienic and foraging behaviours of honey bees. Apidologie. 50: 595-605.
42. Nauen, R., Jeschke, P., Velten, R., Beck, M. E., Ebbinghaus‐Kintscher, U., Thielert, W., ..., Raupach, G., 2015. Flupyradifurone: a brief profile of a new butenolide insecticide. Pest Management Science. 71(6): 850-862.
43. Özkan, B., Akçaöz, H. V., Karaman, S., Taşcıoğlu, Y., 2002. Antalya ilinde serada sebze üretiminde pestisit kullanımının ekonomik açıdan değerlendirilmesi. Bahçe. 31(1): 9-16.
44. Paoli, M., Giurfa, M., 2024. Pesticides and pollinator brain: How do neonicotinoids affect the central nervous system of bees?. European Journal of Neuroscience. 60: 5927–5948
45. Raine, N. E., Chittka, L., 2008. The correlation of learning speed and natural foraging success in bumble-bees. Proceedings of the Royal Society B: Biological Sciences. 275(1636): 803-808.
46. Riveros, A. J., Gronenberg, W., 2009. Olfactory learning and memory in the bumblebee Bombus occidentalis. Naturwissenschaften. 96: 851-856.
47. Samson-Robert, O., Labrie, G., Chagnon, M., Fournier, V., 2017. Planting of neonicotinoid-coated corn raises honey bee mortality and sets back colony development. PeerJ. 5: e3670.
48. Siviter, H., Johnson, A. K., Muth, F., 2021. Bumblebees exposed to a neonicotinoid pesticide make suboptimal foraging decisions. Environmental Entomology. 50(6): 1299-1303.
49. Siviter, H., Muth, F., 2022. Exposure to the novel insecticide flupyradifurone impairs bumblebee feeding motivation, learning, and memory retention. Environmental Pollution. 307: 119575.
50. Stanley, D. A., Russell, A. L., Morrison, S. J., Rogers, C., Raine, N. E., 2016. Investigating the impacts of field‐realistic exposure to a neonicotinoid pesticide on bumblebee foraging, homing ability and colony growth. Journal of Applied Ecology. 53(5): 1440-1449.
51. Stokstad, E., 2013. Pesticides under fire for risks to pollinators. Science. 340: 674–676.
52. Stuligross, C., Williams, N. M., 2021. Past insecticide exposure reduces bee reproduction and population growth rate. Proceedings of the National Academy of Sciences. 118(48): e2109909118.
53. Tan, L., Li, Q., Xie, X. S., 2015. Olfactory sensory neurons transiently express multiple olfactory receptors during development. Molecular Systems Biology. 11(12): 844.
54. Tan, K., Wang, C., Dong, S., Li, X., Nieh, J. C., 2017. The pesticide flupyradifurone impairs olfactory learning in Asian honey bees (Apis cerana) exposed as larvae or as adults. Scientific Reports. 7(1): 17772.
55. van Nest, B. N., 2018. The olfactory proboscis extension response in the honey bee: a laboratory exercise in classical conditioning. Journal of Undergraduate Neuroscience Education. 16(2): A168.
56. Worden, B. D., Skemp, A. K., Papaj, D. R., 2005. Learning in two contexts: the effects of interference and body size in bumblebees. Journal of Experimental Biology. 208(11): 2045-2053.