Bioinsecticides and Honey Bees

Abstract

Biopesticides, which are natural compounds or microorganisms, have been gaining increasing importance as alternatives to synthetic pesticides within sustainable agricultural practices. The adverse effects of chemical pesticides on non-target pollinators such as honey bees have accelerated the shift toward bioinsecticides. However, the fact that biopesticides are of natural origin does not imply that they are entirely harmless. This review evaluates current scientific findings that reveal the lethal and sublethal effects of microbial and botanical bioinsecticides on honey bees, together with their general definitions. Among microbial bioinsecticides, Bacillus thuringiensis (Bt) is generally considered safe; nevertheless, certain strains and formulations can cause disruptions in larval development, flight performance, and gut microbiota. Entomopathogenic fungi such as Beauveria bassiana and Metarhizium anisopliae typically exhibit low toxicity, though increased mortality or behavioral alterations have been reported at high doses. In contrast, spinosad can induce pronounced neurotoxic and immunosuppressive effects in honey bees. Among botanical bioinsecticides, compounds such as azadirachtin have been reported to impair larval development, reduce flight activity, or cause mortality at elevated doses. Conversely, some essential oils exhibit low toxicity profiles. In conclusion, although bioinsecticides are generally regarded as more ecologically safe alternatives, further research addressing their potential risks to bees is needed.

Keywords

• Biopesticide
• Honey bee (Apis mellifera L.)
• Sublethal effects
• Microbial biopesticide
• Botanical bioinsecticide

Biyoinsektisitler ve Bal Arıları

Abstract

Biyopestisitler, sürdürülebilir tarım uygulamalarında sentetik pestisitlere alternatif olarak giderek önem kazanan, doğal kökenli bileşikler veya mikroorganizmalardır . Kimyasal pestisitlerin bal arıları gibi hedef dışı tozlayıcılar üzerindeki olumsuz etkileri biyoinsektisitlere yönelimi hızlandırmıştır. Ancak biyopestisitlerin doğal olmaları, tamamen zararsız oldukları anlamına gelmemektedir. Bu derlemede, mikrobiyal ve botanik biyoinsektisitler genel tanımlamaları ile birlikte bal arıları üzerindeki letal ve subletal etkilerini ortaya koyan güncel bilimsel bulgular değerlendirilmiştir. Mikrobiyal biyoinsektisitlerden Bacillus thuringiensis (Bt) genellikle güvenli kabul edilse de bazı suş ve formülasyonların larval gelişim, uçuş performansı ve bağırsak mikrobiyotasında bozulmalara yol açabilmektedir. Beauveria bassiana ve Metarhizium anisopliae gibi entomopatojenik funguslar çoğunlukla düşük toksisite gösterse de yüksek dozlarda mortalite artışı veya davranışsal değişiklikler bildirilmiştir. Spinosad ise bal arıları için ciddi nörotoksik ve immün baskılayıcı etkiler oluşturabilmektedir. Botanik biyoinsektisitlerden azadirachtin başta olmak üzere bazı bileşiklerin larva dönemindeki gelişimini bozduğu, uçuş aktivitesini azalttığı veya yüksek dozlarda mortaliteye yol açtığı bildirilmiştir. Buna karşın bazı uçucu yağlar düşük toksisite profili sergilemektedir. Sonuç olarak biyoinsektisitlerin ekolojik açıdan daha güvenli seçenekler olduğu kabul edilse de arılar üzerindeki potansiyel risklerini ele alan yeni araştırmalara ihtiyaç bulunmaktadır.

Keywords

• Biyopestisit
• Bal arısı (Apis mellifera L.)
• Subletal etki
• Mikrobiyal biyopestisit
• Botanik biyoinsektisit

References

1. Ağar, S., Aydınoğlu, H., Temel, O., İkizünal, K., Ece, H., 1991. Pestisit kullanımının tarihçesi, bugünü ve geleceği. Türkiye Entomoloji Dergisi, 15(4): 247-256.
2. Al-Mazra'Awi, M.S., Kevan, P.G., Shipp, L., 2007. Development of Beauveria bassiana dry formulation for vectoring by honey bees Apis mellifera (Hymenoptera: Apidae) to the flowers of crops for pest control. Biocontrol Science and Technology, 17(7): 733-741.
3. Araujo, R.D.S., Lopes, M.P., Viana, T.A., Bastos, D.S.S., Machado-Neves, M., Botina, L.L., Martins, G.F., 2023. Bioinsecticide spinosad poses multiple harmful effects on foragers of Apis mellifera. Environmental Science and Pollution Research, 30(25): 66923-66935.
4. Ayilara, M.S., Adeleke, B.S., Akinola, S.A., Fayose, C.A., Adeyemi, U.T., Gbadegesin, L.A., Omole, R.K., Johnson, R.M., Uthman, Q.O., Babalola, O.O., 2023. Biopesticides as a promising alternative to synthetic pesticides: A case for microbial pesticides, phytopesticides, and nanobiopesticides. Frontiers in Microbiology, 14: 1040901.
5. Azizoğlu, U., Bulut, S., Yılmaz, S., 2012. Organik tarımda biyolojik mücadele; entomopatojen biyoinsektisitler. Erciyes Üniversitesi Fen Bilimleri Enstitüsü Fen Bilimleri Dergisi, 28(5): 375-381.
6. Balcı, H., Durmuşoğlu, E., 2020. Bitki koruma ürünü olarak biyopestisitler: tanımları, sınıflandırılmaları, mevzuat ve pazarları üzerine bir değerlendirme. Türkiye Biyolojik Mücadele Dergisi, 11(2): 261-274.
7. Cai, P., Dimopoulos, G., 2024. Microbial biopesticides: A one health perspective on benefits and risks. One Health, 20: 100962.
8. Carlesso, D., Smargiassi, S., Sassoli, L., Cappa, F., Cervo, R., Baracchi, D., 2020. Exposure to a biopesticide interferes with sucrose responsiveness and learning in honey bees. Scientific Reports, 10: 19929.

9. Catania, R., Lima, M.A.P., Potrich, M., Sgolastra, F., Zappala, L., Mazzeo, G., 2023. Are botanical biopesticides safe for bees (Hymenoptera, Apoidea)? Insects, 14(3): e0247.
10. Daraban, G.M., Hlihor, R.-M., Suteu, D., 2023. Pesticides vs. biopesticides: from pest management to toxicity and impacts on the environment and human health. Toxics, 11: 983.
11. Eze, S.C., Mba, C.L., Ezeaku, P.I., 2016. Analytical review of pesticide formulation trends and application: The effects on the target organisms and environment. International Journal of Science and Environment Technology, 5(1): 253-266.
12. Gupta, S., Dikshit, A.K., 2010. Biopesticides: an ecofriendly approach for pest control. Journal of Biopesticides, 3(1): 186-188.
13. Hurley, T.M., 2005. Bacillus thuringiensis resistance management: experiences from the USA. In: Wesseler, J.H.H. (Ed.), Environmental Costs and Benefits of Transgenic Crops. Springer, Dordrecht, the Netherlands.
14. Jena, M.K., Sahoo, S., 2022. Biopesticides: The future of agricultural pest management. Just Agriculture, 2(8): 1-6.
15. Kekillioğlu, A., Bıçak, Z., 2020. Pestisitler ve arılar üzerindeki etkilerinin incelenmesi. EJONS International Journal on Mathematic, Engineering and Natural Sciences, 13: 26-44.
16. Kumar, S., 2012. Biopesticides: a need for food and environmental safety. Journal of Fertilizers and Pesticides, 3(4): 1000e107.
17. Libardoni, G., Neves, P.M.O.J., Abati, R., 2021. Possible interference of Bacillus thuringiensis on the survival and behavior of African honey bees (Apis mellifera). Scientific Reports, 11: 3482.
18. Lord, J.C., 2005. From Metchnikoff to Monsanto and beyond: the path of microbial control. Journal of Invertebrate Pathology, 89: 19–29.
19. Mascarin, G.M., Jaronski, S.T., 2016. Production and use of Beauveria bassiana as a microbial insecticide. World Journal of Microbiology and Biotechnology, 32: 177.
20. Meikle, W.G., Mercadier, G., Holst, N., et al., 2008. Effects of Beauveria bassiana (Deuteromycota: Hyphomycetes) treatment on honey bee (Apis mellifera) colony health and Varroa destructor mites (Acari: Varroidae). Apidologie, 39: 247–259.
21. Mishra, J., Tewari, S., Singh, S., Arora, K., 2015. Biopesticides: where we stand? In: Arora, N.K. (Ed.), Plant Microbes Symbiosis. Springer, India, pp. 37–75.
22. Ndolo, D.E., Njuguna, C.O., Adetunji, C., Harbor, A., Rowe, A., Den Breeyen, J., Sangeetha, G., Singh, B., Szewczyk, T.S., Anjorin, D., Thangadurai, R., Hospeti, V., 2019. Research and development of biopesticides: challenges and prospects. Outlooks on Pest Management, 30(6): 267–276.
23. Oguh, C.E., Okpaka, C.O., Ubani, C.S., Okekeaji, U., Joseph, P.S., Amadi, E.U., 2019. Natural pesticides (biopesticides) and uses in pest management – a critical review. Asian Journal of Biotechnology and Genetic Engineering, 9(2): 1–18.
24. Popp, J., Peto, K., Nagy, J., 2013. Pesticide productivity and food security: a review. Agronomie, 33: 243–255.
25. Rad, S.M., Ray, A.K., Barghi, S., 2022. Water pollution and agriculture pesticide. Clean Technologies, 4(4): 1088-1102.
26. Santos, A.C., Cristaldo, P.F., Araujo, A.P., Melo, C.R., Lima, A.P., Santana, E.D., Oliveira, B.M., Oliveira, J.W., Vieira, J.S., Blank, A.F., Bacci, L., 2018. Apis mellifera in the target of neonicotinoids: A one-way ticket? Bioinsecticides can be an alternative. Ecotoxicology and Environmental Safety, 163: 28–36.
27. Shamsuddeen, R., Mathew, T.S., Haladu, M., Ahmad, K.B., Adam, A.B., Abubakar, M.Y., 2024. Recent advances in biopesticides: a review of efficacy and environmental impact. African Journal of Biochemistry and Molecular Biology Research, 1(1): 706–725.
28. Soni, J., Thakur, M., 2011. Effect of biopathogens on honey bees. Pest Technology, 5(1): 86-90.
29. Steinigeweg, C., Alkassab, A.T., Beims, H., Eckert, J.H., Richter, D., Pistorius, J., 2021. Assessment of the impacts of microbial plant protection products containing Bacillus thuringiensis on the survival of adults and larvae of the honeybee (Apis mellifera). Environmental Science and Pollution Research, 28: 29773–29780.
30. Tadesse Mawcha, K., Malinga, L., Muir, D., Ge, J., Ndolo, D., 2024. Recent advances in biopesticide research and development: a focus on microbial. F1000Research, 13: 1071.
31. Tullah, Z., Ain, Q., Ahmad, F., 2023. Pesticides’ taxonomy, functioning, their associated risks to human and environment, and degradation technologies. Journal of Chemical Reviews, 5(1): 31–55.