Déclin des abeilles mellifères : implications des infections virales amplifiées par Varroa et solutions préventives
DOI:
https://doi.org/10.46325/afj.v10i1.212Keywords:
Abeilles melliféres, biodiversité, mortalité des colonies, Varroa destructor, Stress environemental, changement climatique, gestion integrée des parasitesAbstract
Honeybees (Apis mellifera) are essential pollinators for approximately 75% of food crops, supporting biodiversity and the global agricultural economy. The main objective is to understand and reduce significant colony losses, with local winter mortality rates reaching 50–60%. These declines result from a complex combination of biological and environmental factors. The parasite Varroa destructor represents the major threat, weakening bees and acting as a vector for viruses such as Deformed Wing Virus (DWV). Microsporidia of the genus Nosema impair digestion and reduce the lifespan of worker bees. These pathogens interact with environmental stressors such as neonicotinoid pesticides, poor nutrition, and climate change, thereby amplifying their overall impact. Integrated Pest Management (IPM) is a key strategy, combining reduced chemical treatments, mechanical control methods, and the selection of hygienic bee strains. Improving nutritional conditions and enhancing floral diversity also strengthen colony resilience. Modern technologies, such as digital monitoring systems and biotechnological tools, enable early detection and targeted interventions. Finally, a holistic and coordinated approach integrating biology, agriculture, and ecology is essential to ensure the long-term health of honeybees and global food security.
References
1. Adjlane, N., & Haddad, N., 2020. Varroa destructor (Acari: Parasitiformes : Varroidae), a dangerous parasite of honey bees (Hymenoptera : Apidae). ENTOMON, 45(3), 159–170. https://doi.org/10.33307/entomon.v45i3.547
2. Adjlane, N., Dainat, B., Gauthier, L., & Dietemann, V., 2016. Atypical viral and parasitic pattern in Algerian honey bee subspecies Apis mellifera intermissa and A. m. sahariensis. Apidologie, 47(5), 631–641. https://doi.org/10.1007/s13592-015-0410-x
3. Adjlane, N., Doumandji, S., & Haddad, N., 2012a. Situation de l’apiculture en Algérie : facteurs menaçant la survie des colonies d’abeilles locales Apis mellifera intermissa. Cahiers Agricultures, 21(4), 235–241. https://doi.org/10.1684/agr.2012.0566
4. Adjlane, N., Doumandji, S., & Haddad, N., 2012b. La prévalence de la nosémose dans les colonies d’abeilles Apis mellifera intermissa dans la région médio-septentrionale de l’Algérie. Lebanese Science Journal, 13(1), 65–73.
5. Adjlane, N., Doumandji, S. E., & Haddad, N., 2013. Varroa destructor resistance to fluvalinate in Algeria. Trends in Entomology, 12, 123–125.
6. Adjlane, N., Tarek, E. O., & Haddad, N., 2016. Evaluation of oxalic acid treatments against Varroa destructor and secondary effects on honey bees Apis mellifera. Journal of Arthropod-Borne Diseases, 10(4), 501.
7. Adjlane, N., Wafdi, M., & Haddad, N., 2018. Développement de Varroa destructor dans les colonies d’abeilles locales Apis mellifera intermissa en Algérie. Revue Agriculture, 9(1), 81–88.
8. Antúnez, K., D’Alessandro, B., Corbella, E., Ramallo, G., & Zunino, P., 2006. Honeybee viruses in Uruguay. Journal of Invertebrate Pathology, 93(1), 67–70.
9. Benjeddou, M., Leat, N., Allsopp, M., & Davison, S., 2001. Detection of Acute Bee Paralysis Virus and Black Queen Cell Virus from honeybees. Applied and Environmental Microbiology, 67(5), 2384–2387.
10. Boncristiani, H., Ellis, J. D., Prouty, C., Schmehl, D. R., & Jack, C. J., 2024. Evaluating seasonal efficacy of chemical treatments on Varroa destructor. Journal of Insect Science, 24(3), 11. https://doi.org/10.1093/jisesa/ieae011
11. Bruckner, S., Straub, L., Villamar-Bouza, L., Beneduci, Z. J., Neumann, P., & Williams, G. R., 2024. Life stage dependent effects of neonicotinoid exposure on honey bee hypopharyngeal gland development. Ecotoxicology and Environmental Safety, 288, 117337..
12. Calderone, N. W., 2012. Insect pollinated crops and US agriculture: trend analysis. PLOS ONE, 7(5), e37235.
13. Calderone, N. W., & Smagghe, G., 2012. Pollination services in agriculture: importance, status and trends. Journal of Insect Conservation, 16, 733–748.
14. Chen, Y. P., & Siede, R., 2007. Honey bee viruses. Advances in Virus Research, 70, 33–80.
15. Cox-Foster, D. L., Conlan, S., Holmes, E. C., Palacios, G., Evans, J. D., Moran, N. A., Quan, P.-L., Briese, T., Hornig, M., Geiser, D. M., & Lipkin, W. I., 2007. A metagenomic survey of microbes in honey bee colony collapse disorder. Science, 318(5848), 283–287. https://doi.org/10.1126/science.1146498
16. Cox-Foster, D. L., Conlan, S., Holmes, E. C., Palacios, G., Evans, J. D., Moran, N. A., Quan, P.-L., Briese, T., Hornig, M., Geiser, D. M., & Lipkin, W. I., 2007. A metagenomic survey of microbes in honey bee colony collapse disorder. Science, 318(5848), 283–287. https://doi.org/10.1126/science.1146498
17. de Miranda, J. R., & Genersch, E., 2010. Deformed wing virus. Journal of Invertebrate Pathology, 103(Suppl 1), S48–S61. https://doi.org/10.1016/j.jip.2009.06.012
18. Dietemann, V., Nazzi, F., Martin, S. J., Anderson, D. L., Locke, B., & Delaplane, K. S., 2023. Integrated management strategies for Varroa destructor in honey bee colonies. Journal of Apicultural Research, 62(2), 150–170.
19. Doublet, V., Natsopoulou, M. E., McMahon, D. P., & al., 2024. Shift in virus composition in honeybees (Apis mellifera) following Varroa destructor invasion. Royal Society Open Science. 11-16,
20. Gallai, N., Salles, J.-M., Settele, J., & Vaissière, B. E., 2009. Economic valuation of pollinator decline. Ecological Economics, 68, 810–821.
21. Gregorc, A., & Planinc, I., 2023. Efficacy of organic acids in controlling Varroa destructor. Apidologie, 54, 1–15.
22. 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. https://doi.org/10.1126/science.1255957
23. Haddad, N. J., de Miranda, J. R., Bataille, A., 2017. Distribution of deformed wing virus in the MENA region. Insect Science, 24(1), 103–113. https://doi.org/10.1111/1744-7917.12314
24. Higes, M., Martín-Hernández, R., & Meana, A., 2006. Nosema ceranae in honey bees. Journal of Invertebrate Pathology, 92, 93–95.
25. 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. https://doi.org/10.1098/rspb.2006.3721
26. Kosch, Y., Mülling, C., & Emmerich, I. U., 2025. Resistance of Varroa destructor to formic and lactic acid. Veterinary Sciences, 12(2), 144.
27. Kulhanek, K., Steinhauer, N., Rennich, K., Caron, D. M., Sagili, R. R., Pettis, J. S., Ellis, J. D., Wilson, M. E., Wilkes, J. T., Tarpy, D. R., Rose, R., Lee, K., Rangel, J., & vanEngelsdorp, D., 2017. A national survey of managed honey bee 2015–2016 annual colony losses in the USA. Journal of Apicultural Research, 56(4), 328–340. https://doi.org/10.1080/00218839.2017.1344496
28. Leonard, S. P., Powell, J. E., Perutka, J., et al., 2023. RNA interference strategies against Varroa destructor. Scientific Reports, 13, 14567. https://doi.org/10.1038/s41598-023-14567
29. Li, J., Evans, J. D., Li, W., Zhao, Y., DeGrandi-Hoffman, G., Huang, S., & Chen, Y. P., 2013. Effects of deformed wing virus on honey bee behavior and survival. PLOS ONE, 8(10), e76450. https://doi.org/10.1371/journal.pone.0076450
30. Locke, B., 2024. Natural resistance mechanisms of honey bees to Varroa destructor. Frontiers in Ecology and Evolution, 12, 1434490.
31. López, A. R., Low, M., Martín-Hernández, R., de Miranda, J. R., & Pinto, M. A., 2024. Varroa destructor shapes viral landscape of honey bees. Virus Evolution, 10, veae053. https://doi.org/10.1093/ve/veae053
32. MacInnis, C. I., Luong, L. T., & Pernal, S. F., 2024. Effects of Nosema ceranae and Lotmaria passim on bees. International Journal for Parasitology, 2024, 12.003.
33. Martin, S. J., 1998. Reproduction of Varroa destructor. Apidologie, 29, 387–388.
34. Medina-Flores, C. A., Guzmán-Novoa, E., Hamiduzzaman, M. M., López, D., & Varghese, D., 2024. Population dynamics of Varroa destructor in honey bee (Apis mellifera) colonies in a temperate semi-arid climate. Insects, 15(9), 696. https://doi.org/10.3390/insects15090696
35. Moore, J., Wilson, M. E., Skinner, J. A., & Tarpy, D. R., 2011. Varroa destructor: How does it harm Apis mellifera honey bees and what can be done about it? Annual Review of Entomology, 56, 293–312. https://doi.org/10.1146/annurev-ento-120709-144717
36. Paxton, R. J., Klee, J., Korpela, S., & Fries, I., 2007. Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie, 38(6), 558–565. https://doi.org/10.1051/apido:2007037
37. Pettis, J. S., VanEngelsdorp, D., Johnson, J., & Dively, G., 2012. Pesticides and colony collapse disorder. Pesticide Biochemistry and Physiology, 102(1), 1–10. https://doi.org/10.1016/j.pestbp.2011.11.005
38. Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P., Schweiger, O., & Kunin, W. E., 2010. Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution, 25(6), 345–353. https://doi.org/10.1016/j.tree.2010.01.007
39. Rosenkranz, P., Aumeier, P., & Ziegelmann, B., 2010. Biology and control of Varroa destructor. Journal of Invertebrate Pathology, 103 (Suppl 1), S96–S119. https://doi.org/10.1016/j.jip.2009.07.016
40. Rosenkranz, P., Tewarson, N. C., Mühlen, W., Aumeier, P., & Ziegelmann, B., 2024.
Updated integrated pest management strategies against Varroa destructor. Apidologie, 55, 1–30.
41. Stuligross, C., & Williams, N. M., 2021. Parasites and pesticides synergistically impact bees. Science, 372, 1215–1219.
42. Taylor, R., & Rangel, J., 2024. Integrated pest management control of Varroa destructor. Journal of Economic Entomology, 117(1), 37–44.
43. Traynor, K. S., Mondet, F., de Miranda, J. R., Techer, M., Kowallik, V., Yañez, O., & Fries, I., 2020. Global spread and evolution of Varroa destructor. Journal of Apicultural Research, 59(1), 1–17. https://doi.org/10.1080/00218839.2019.1706160
44. Vanbergen, A. J., 2013. Threats to pollinators. Frontiers in Ecology and the Environment, 11, 251–259.
45. vanEngelsdorp, D., & Meixner, M. D., 2010. Managed honey bee populations review. Journal of Invertebrate Pathology, 103 (Suppl 1), S80–S95.
46. Warner, S., Pokhrel, L. R., Akula, S. M., Ubah, C. S., Richards, S. L., Jensen, H., & Kearney, G. D., 2024. Varroa destructor and honey bee decline: A global synthesis. Science of the Total Environment, 930, 172820. https://doi.org/10.1016/j.scitotenv.2024.172820
47. Zheng, H., Li, X., Wang, Y., Chen, J., Liu, M., Zhang, L., & Huang, Z., 2024. Gut microbiome and bee health: probiotic approaches for improving resistance to parasites. Microbiome Research Journal, 18(2), 101–115.
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