Varroa destructor is a well-known ectoparasite of the honey bee Apis mellifera. Amitraz and fluvalinate are highly effective miticides used against V. destructor infestation in colonies of honey bee A. mellifera. Though honey bees more resistant to miticides, there are side effects of these chemicals on the reproduction, olfaction, and honey production of honey bees. We showed a negative impact of miticides amitraz and fluvalinate on honey production and reproduction of honey bee colonies. Also, we assumed the reduction of olfaction of honey bees by fluvalinate due to changes of expression of olfactory related neuropeptide genes short neuropeptide F sNPF, tachykinin TK, short neuropeptide F receptor sNPFR. The external treatment of honey bee colonies by miticides amitraz and fluvalinate along with a positive effect of pest control harms reproductivity, honey productivity, and, probably, can reduce learning and memory, gustation and olfaction of honey bees. When used for a short time and with care, miticides can be less harmful to honey bees. Breeding varroa-resistant honey bees allow to reduce the use of miticides and produce organic honey. Therefore, the further development of beekeeping should be in the direction of selection for disease and Varroa resistance and adaptation to the environment.
To the Post-Doctoral Research Programs in Incheon National University (2017-2019) and the Russian Foundation for Basic Research (RFBR) (Grant No. 19-54-70002 e-Asia_t).
References
Allsopp, M. H. (2006). Analysis of Varroa destructor infestation of Southern African honeybee populations Dissertation for the degree of Master of Sciences (pp. 1-285). Pretoria, Republic of South Africa: University of Pretoria.
Altstein, M., Nässel, DR. (2010). Neuropeptide signaling in insects. In T. G. Geary & A. G. Maule (Eds.), Neuropeptide systems as targets for parasite and pest control (Vol. 692, pp. 155-165). USA, New York: Springer Science+Business Media, LLC Landes Bioscience.
Anderson, DL., Trueman, JW. (2000). Varroa jacobsoni (Acari: Varroidae) is more than one species. Experimental and Applied Acarology, 24(3), 165-189. doi: 10.1023/a:1006456720416.
Berry, JA., Hood, WM., Pietravalle, S., Delaplane, KS. (2013). Field-level sublethal effects of approved bee hive chemicals on honey bees (Apis mellifera L). Plos One, 8(10), e76536. doi: 10.1371/journal.pone.0076536.
Çakmak, I., Fuchs, S. (2013) Exploring a treatment strategy for long-term increase of varroa tolerance on Marmara Island, Turkey. Journal of Apicultural Research, 52(5), 242-250. doi: 10.3896/IBRA.1.52.5.11.
Conlon, B. H., Frey, E., Rosenkranz, P., Locke, B., Moritz, R. F. A., Routtu, J. (2018). The role of epistatic interactions underpinning resistance to parasitic Varroa mites in haploid honey bee (Apis mellifera) drones. Journal of Evolutionary Biology, 31(6), 801-809. doi: 10.1111/jeb.13271.
Dai, P., Jack, CJ., Mortensen, AN., Ellis, JD. (2017). Acute toxicity of five pesticides to Apis mellifera larvae reared in vitro. Pest Management Science, 73(11), 2282-2286. doi: 10.1002/ps.4608.
Frost, EH., Shutler, D., Hillier, NK. (2013). Effects of fluvalinate on honey bee learning, memory, responsiveness to sucrose, and survival. The Journal of Experimental Biology, 216, 2931-2938. doi: 10.1242/jeb.086538.
Giurfa, M. (2007). Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. Journal of Comparative Physiology A, 193(8), 801-824. doi: 10.1007/s00359-007-0235-9.
Gosselin-Badaroudine, P., Chahine, M. (2017). Biophysical characterization of the Varroa destructor NaV1 sodium channel and its affinity for tau-fluvalinate insecticide. FASEB journal: official publication of the Federation of American Societies for Experimental Biology, 31(7), 3066-3071. doi: 10.1096/fj.201601338R.
Gracia, MJ., Moreno, C., Ferrer, M., Sanz, A., Peribáñez, M., Estrada, R. (2017). Field efficacy of acaricides against Varroa destructor. Plos One, 12(2), e0171633. doi: 10.1371/journal.pone.0171633.
Gregorc, A., Evans, JD., Scharf, M., Ellis, JD. (2012). Gene expression in honey bee (Apis mellifera) larvae exposed to pesticides and Varroa mites (Varroa destructor). Journal of Insect Physiology, 58(8), 1042-1049. doi: 10.1016/j.jinsphys.2012.03.015.
Gupta, R., Crissman, J. (2013). Agricultural chemicals. In W. M. Haschek, C. G. Rousseaux, M. A. Wallig, B. Bolon & R. Ochoa (Eds.), Haschek and Rousseaux's Handbook of Toxicologic Pathology (3 ed., pp. 1349-1372). Boston, United States: Academic Press.
Hauser, F., Cazzamali, G., Williamson, M., Blenau, W., Grimmelikhuijzen, CJ. (2006). A review of neurohormone GPCRs present in the fruitfly Drosophila melanogaster and the honey bee Apis mellifera. Progress in Neurobiology, 80(1), 1-19. doi: 10.1016/j.pneurobio.2006.07.005.
Hewes, RS., Taghert, PH. (2001). Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. Genome Research, 11, 1126-1142. doi: 10.1101/gr.169901.
Hummon, AB., Richmond, TA., Verleyen, P., Baggerman, G., Huybrechts, J., Ewing, MA., Sweedler, JV. (2006). From the genome to the proteome: uncovering peptides in the Apis brain. Science, 314, 647-649. doi: 10.1126/science.1124128.
Ilyasov, RA., Farkhutdinov, RG., Shareeva, ZV. (2014). Influence of acaricides amitraz and fluvalinate on average daily egg and total honey productivity of honey bee colonies. Biomics, 6(2), 73-76.
Jiang, HB., Gui, SH., Xu, L., Pei, YX., Smagghe, G., Wang, JJ. (2017). The short neuropeptide F modulates olfactory sensitivity of Bactrocera dorsalis upon starvation. Journal of Insect Physiology, 99, 78–85. doi: 10.1016/j.jinsphys.2017.03.012.
Johnson, EC. (2006). Postgenomic approaches to resolve neuropeptide signaling in Drosophila. In H. Satake (Ed.), Invertebrate neuropeptides and hormones: basic knowledge and recent advances (pp. 179-224). Trivandrum: Transworld Research Network.
Jung, JW., Kim, J-H., Pfeiffer, R., Ahn, Y-J., Page, TL., Kwon, HW. (2013). Neuromodulation of olfactory sensitivity in the peripheral olfactory organs of the American cockroach, Periplaneta americana. Plos One, 8(11), e81361. doi: 10.1371/journal.pone.0081361.
Klein, AM., Vaissière, BE., Cane, JH., Steffan-Dewenter, I., Cunningham, SA., 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. doi: 10.1098/rspb.2006.3721.
Lim, S., Yunusbaev, UB., Ilyasov, RA., Lee, HS., Kwon, HW. (2020). Abdominal contact of fluvalinate induces olfactory deficit in Apis mellifera. Pesticide Biochemistry and Physiology, 164(1), 221-227. doi: 10.1016/j.pestbp.2020.02.005.
Livak, KJ., Schmittgen, TD. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25(4), 402-408. doi: 10.1006/meth.2001.1262.
Locke, B., Fries, I. (2011). Characteristics of honey bee colonies (Apis mellifera) in Sweden surviving Varroa destructor infestation. Apidologie, 42(4), 533-542. doi: 10.1007/s13592-011-0029-5.
Mao, W., Schuler, M., Berenbaum, MR. (2011). CYP9Q-mediated detoxification of acaricides in the honey bee (Apis mellifera). Proceedings of the National Academy of Sciences of the United States of America, 108, 12657-12662. doi: 10.1073/pnas.1109535108.
Marciniak, P., Kuczer, M., Rosinski, G. (2011). New physiological activities of myosuppressin, sulfakinin and NVP-like peptide in Zophobas atratus beetle. Journal of Comparative Physiology B, 181, 721-730. doi: 10.1007/s00360-011-0563-5.
McMullan, J. (2018). Adaptation in honey bee (Apis mellifera) colonies exhibiting tolerance to Varroa destructor in Ireland. Bee World, 95(2), 39-43. doi: 10.1080/0005772X.2018.1431000.
Menzel, R. (1999). Memory dynamics in the honeybee. Journal of Comparative Physiology A, 185, 323-340. doi: 10.1007/s003590050392.
Mondragón, L., Spivak, M., Vandame, R. (2005). A multifactorial study of the resistance of honeybees Apis mellifera to the mite Varroa destructor over one year in Mexico. Apidologie, 36(3), 345-358. doi: 10.1051/apido:2005022.
Nässel, DR. (2002). Neuropeptides in the nervous system of Drosophila and other insects: multiple roles as neuromodulators and neurohormones. Progress in Neurobiology, 68, 1-84. doi: 10.1016/S0301-0082(02)00057-6.
Rangel, J., Tarpy, DR. (2015). The combined effects of miticides on the mating health of honey bee (Apis mellifera L.) queens. Journal of Apicultural Research, 54, 325-329. doi: 10.1080/00218839.2016.1147218.
Rinkevich, F. D. (2020). Detection of amitraz resistance and reduced treatment efficacy in the Varroa Mite, Varroa destructor, within commercial beekeeping operations. Plos One, 15(1), e0227264. doi: 10.1371/journal.pone.0227264.
Schoofs, L., De Loof, A., Van Hiel, MB. (2017). Neuropeptides as regulators of behavior in insects. Annual Review of Entomology, 62, 35-52. doi: 10.1146/annurev-ento-031616-035500.
Southwick, EE., Southwick, LJ. (1992). Estimating the economic value of honey bees (Hymenoptera: Apidae) as agricultural pollinators in the United States. Journal of Economic Entomology, 85(3), 621-633. doi: 10.1093/jee/85.3.621.
van Alphen, J. J. M., Fernhout, B. J. (2020). Natural selection, selective breeding, and the evolution of resistance of honeybees (Apis mellifera) against Varroa. Zoological Letters, 6, 6. doi: 10.1186/s40851-020-00158-4.
Wallace, KB. (2002). Mechanisms of pyrethroid neurotoxicity: implications for cumulative risk assessment. Toxicology, 171(1), 1. doi: https://doi.org/10.1016/S0300-483X(01)00574-1.
Xu, G., Gu, G-X., Teng, Z-W., Wu, S-F., Huang, J., Song, Q-S., Fang, Q. (2016). Identification and expression profiles of neuropeptides and their G protein-coupled receptors in the rice stem borer Chilo suppressalis. Scientific Reports, 6, 28976. doi: 10.1038/srep28976.
Zhang, Z. Q. (2000). Notes on Varroa destructor (Acari: Varroidae) parasitic on honeybees in New Zealand. Systematic and Applied Acarology, 5, 9-14. doi: 10.11158/saasp.5.1.2.
Akarisit Amitraz ve Fluvalinat'ın Bal Arısı Apis mellifera'nın Üreme ve Verimliliğine Etkisi
Varroa, bal arısı Apis mellifera'nın iyi bilinen bir ektoparazitidir. Amitraz ve fluvalinat, bal arısı A. mellifera kolonilerinde V. destructor istilasına karşı kullanılan oldukça yüksek etkili akarisitlerdir. Bal arıları, akarisitlere karşı daha dirençli olsalar da, bu kimyasalların bal arılarının üreme, koku alma ve bal üretimi üzerinde yan etkileri vardır. Bu çalışma ile Akarisitler olan amitraz ve fluvalinatın bal üretimi ve bal arısı kolonilerinin üremesi üzerinde olumsuz bir etkisi olduğu belirlenmiştir. Ayrıca, bal arılarının Fluvalinat’a bağlı olarak koku alma duyusunun azalması durumunu ilgili nöropeptid genlerinin kısa nöropeptid F sNPF, taşikinin TK, kısa nöropeptid F reseptörü sNPFR ifadesindeki değişiklik olduğunu varsaydık. Bal arısı kolonilerinin akarisitler olan amitraz ve fluvalinate ile kontrol edilmesi, haşere kontrolünün olumlu etkisiyle birlikte üremeye, bal verimliliğine zarar verir ve muhtemelen bal arılarının öğrenmesini ve hafızasını, lezzetini ve kokusunu muhtemelen azaltabilir. Kısa bir süre ve özenle kullanıldığında, akarisit kullanımı bal arılarına daha az zarar verebilir. Varroaya dirençli bal arılarının yetiştirilmesi, akarisit kullanımını azaltmaya ve organik bal üretmeye izin verir. Bu nedenle, arıcılığın daha da geliştirilmesi için seçim; hastalıklara, Varroa’ya dirençli ve çevreye uyum yönünde olmalıdır.
Allsopp, M. H. (2006). Analysis of Varroa destructor infestation of Southern African honeybee populations Dissertation for the degree of Master of Sciences (pp. 1-285). Pretoria, Republic of South Africa: University of Pretoria.
Altstein, M., Nässel, DR. (2010). Neuropeptide signaling in insects. In T. G. Geary & A. G. Maule (Eds.), Neuropeptide systems as targets for parasite and pest control (Vol. 692, pp. 155-165). USA, New York: Springer Science+Business Media, LLC Landes Bioscience.
Anderson, DL., Trueman, JW. (2000). Varroa jacobsoni (Acari: Varroidae) is more than one species. Experimental and Applied Acarology, 24(3), 165-189. doi: 10.1023/a:1006456720416.
Berry, JA., Hood, WM., Pietravalle, S., Delaplane, KS. (2013). Field-level sublethal effects of approved bee hive chemicals on honey bees (Apis mellifera L). Plos One, 8(10), e76536. doi: 10.1371/journal.pone.0076536.
Çakmak, I., Fuchs, S. (2013) Exploring a treatment strategy for long-term increase of varroa tolerance on Marmara Island, Turkey. Journal of Apicultural Research, 52(5), 242-250. doi: 10.3896/IBRA.1.52.5.11.
Conlon, B. H., Frey, E., Rosenkranz, P., Locke, B., Moritz, R. F. A., Routtu, J. (2018). The role of epistatic interactions underpinning resistance to parasitic Varroa mites in haploid honey bee (Apis mellifera) drones. Journal of Evolutionary Biology, 31(6), 801-809. doi: 10.1111/jeb.13271.
Dai, P., Jack, CJ., Mortensen, AN., Ellis, JD. (2017). Acute toxicity of five pesticides to Apis mellifera larvae reared in vitro. Pest Management Science, 73(11), 2282-2286. doi: 10.1002/ps.4608.
Frost, EH., Shutler, D., Hillier, NK. (2013). Effects of fluvalinate on honey bee learning, memory, responsiveness to sucrose, and survival. The Journal of Experimental Biology, 216, 2931-2938. doi: 10.1242/jeb.086538.
Giurfa, M. (2007). Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. Journal of Comparative Physiology A, 193(8), 801-824. doi: 10.1007/s00359-007-0235-9.
Gosselin-Badaroudine, P., Chahine, M. (2017). Biophysical characterization of the Varroa destructor NaV1 sodium channel and its affinity for tau-fluvalinate insecticide. FASEB journal: official publication of the Federation of American Societies for Experimental Biology, 31(7), 3066-3071. doi: 10.1096/fj.201601338R.
Gracia, MJ., Moreno, C., Ferrer, M., Sanz, A., Peribáñez, M., Estrada, R. (2017). Field efficacy of acaricides against Varroa destructor. Plos One, 12(2), e0171633. doi: 10.1371/journal.pone.0171633.
Gregorc, A., Evans, JD., Scharf, M., Ellis, JD. (2012). Gene expression in honey bee (Apis mellifera) larvae exposed to pesticides and Varroa mites (Varroa destructor). Journal of Insect Physiology, 58(8), 1042-1049. doi: 10.1016/j.jinsphys.2012.03.015.
Gupta, R., Crissman, J. (2013). Agricultural chemicals. In W. M. Haschek, C. G. Rousseaux, M. A. Wallig, B. Bolon & R. Ochoa (Eds.), Haschek and Rousseaux's Handbook of Toxicologic Pathology (3 ed., pp. 1349-1372). Boston, United States: Academic Press.
Hauser, F., Cazzamali, G., Williamson, M., Blenau, W., Grimmelikhuijzen, CJ. (2006). A review of neurohormone GPCRs present in the fruitfly Drosophila melanogaster and the honey bee Apis mellifera. Progress in Neurobiology, 80(1), 1-19. doi: 10.1016/j.pneurobio.2006.07.005.
Hewes, RS., Taghert, PH. (2001). Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. Genome Research, 11, 1126-1142. doi: 10.1101/gr.169901.
Hummon, AB., Richmond, TA., Verleyen, P., Baggerman, G., Huybrechts, J., Ewing, MA., Sweedler, JV. (2006). From the genome to the proteome: uncovering peptides in the Apis brain. Science, 314, 647-649. doi: 10.1126/science.1124128.
Ilyasov, RA., Farkhutdinov, RG., Shareeva, ZV. (2014). Influence of acaricides amitraz and fluvalinate on average daily egg and total honey productivity of honey bee colonies. Biomics, 6(2), 73-76.
Jiang, HB., Gui, SH., Xu, L., Pei, YX., Smagghe, G., Wang, JJ. (2017). The short neuropeptide F modulates olfactory sensitivity of Bactrocera dorsalis upon starvation. Journal of Insect Physiology, 99, 78–85. doi: 10.1016/j.jinsphys.2017.03.012.
Johnson, EC. (2006). Postgenomic approaches to resolve neuropeptide signaling in Drosophila. In H. Satake (Ed.), Invertebrate neuropeptides and hormones: basic knowledge and recent advances (pp. 179-224). Trivandrum: Transworld Research Network.
Jung, JW., Kim, J-H., Pfeiffer, R., Ahn, Y-J., Page, TL., Kwon, HW. (2013). Neuromodulation of olfactory sensitivity in the peripheral olfactory organs of the American cockroach, Periplaneta americana. Plos One, 8(11), e81361. doi: 10.1371/journal.pone.0081361.
Klein, AM., Vaissière, BE., Cane, JH., Steffan-Dewenter, I., Cunningham, SA., 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. doi: 10.1098/rspb.2006.3721.
Lim, S., Yunusbaev, UB., Ilyasov, RA., Lee, HS., Kwon, HW. (2020). Abdominal contact of fluvalinate induces olfactory deficit in Apis mellifera. Pesticide Biochemistry and Physiology, 164(1), 221-227. doi: 10.1016/j.pestbp.2020.02.005.
Livak, KJ., Schmittgen, TD. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25(4), 402-408. doi: 10.1006/meth.2001.1262.
Locke, B., Fries, I. (2011). Characteristics of honey bee colonies (Apis mellifera) in Sweden surviving Varroa destructor infestation. Apidologie, 42(4), 533-542. doi: 10.1007/s13592-011-0029-5.
Mao, W., Schuler, M., Berenbaum, MR. (2011). CYP9Q-mediated detoxification of acaricides in the honey bee (Apis mellifera). Proceedings of the National Academy of Sciences of the United States of America, 108, 12657-12662. doi: 10.1073/pnas.1109535108.
Marciniak, P., Kuczer, M., Rosinski, G. (2011). New physiological activities of myosuppressin, sulfakinin and NVP-like peptide in Zophobas atratus beetle. Journal of Comparative Physiology B, 181, 721-730. doi: 10.1007/s00360-011-0563-5.
McMullan, J. (2018). Adaptation in honey bee (Apis mellifera) colonies exhibiting tolerance to Varroa destructor in Ireland. Bee World, 95(2), 39-43. doi: 10.1080/0005772X.2018.1431000.
Menzel, R. (1999). Memory dynamics in the honeybee. Journal of Comparative Physiology A, 185, 323-340. doi: 10.1007/s003590050392.
Mondragón, L., Spivak, M., Vandame, R. (2005). A multifactorial study of the resistance of honeybees Apis mellifera to the mite Varroa destructor over one year in Mexico. Apidologie, 36(3), 345-358. doi: 10.1051/apido:2005022.
Nässel, DR. (2002). Neuropeptides in the nervous system of Drosophila and other insects: multiple roles as neuromodulators and neurohormones. Progress in Neurobiology, 68, 1-84. doi: 10.1016/S0301-0082(02)00057-6.
Rangel, J., Tarpy, DR. (2015). The combined effects of miticides on the mating health of honey bee (Apis mellifera L.) queens. Journal of Apicultural Research, 54, 325-329. doi: 10.1080/00218839.2016.1147218.
Rinkevich, F. D. (2020). Detection of amitraz resistance and reduced treatment efficacy in the Varroa Mite, Varroa destructor, within commercial beekeeping operations. Plos One, 15(1), e0227264. doi: 10.1371/journal.pone.0227264.
Schoofs, L., De Loof, A., Van Hiel, MB. (2017). Neuropeptides as regulators of behavior in insects. Annual Review of Entomology, 62, 35-52. doi: 10.1146/annurev-ento-031616-035500.
Southwick, EE., Southwick, LJ. (1992). Estimating the economic value of honey bees (Hymenoptera: Apidae) as agricultural pollinators in the United States. Journal of Economic Entomology, 85(3), 621-633. doi: 10.1093/jee/85.3.621.
van Alphen, J. J. M., Fernhout, B. J. (2020). Natural selection, selective breeding, and the evolution of resistance of honeybees (Apis mellifera) against Varroa. Zoological Letters, 6, 6. doi: 10.1186/s40851-020-00158-4.
Wallace, KB. (2002). Mechanisms of pyrethroid neurotoxicity: implications for cumulative risk assessment. Toxicology, 171(1), 1. doi: https://doi.org/10.1016/S0300-483X(01)00574-1.
Xu, G., Gu, G-X., Teng, Z-W., Wu, S-F., Huang, J., Song, Q-S., Fang, Q. (2016). Identification and expression profiles of neuropeptides and their G protein-coupled receptors in the rice stem borer Chilo suppressalis. Scientific Reports, 6, 28976. doi: 10.1038/srep28976.
Zhang, Z. Q. (2000). Notes on Varroa destructor (Acari: Varroidae) parasitic on honeybees in New Zealand. Systematic and Applied Acarology, 5, 9-14. doi: 10.11158/saasp.5.1.2.
Sooho Lim
This is me
Department of Life Sciences and Convergence Research Center for Insect Vectors, Incheon National University0000-0002-6724-3715South Korea
Myeong Lyeol Lee
This is me
Department of Life Sciences and Convergence Research Center for Insect Vectors, Incheon National UniversitySouth Korea
Hyung Wook Kwon
This is me
Department of Life Sciences and Convergence Research Center for Insect Vectors, Incheon National University0000-0001-9340-7974South Korea
Alexey Nikolenko
This is me
Institute of Biochemistry and Genetics, Ufa Federal Research Centre, Russian Academy of Sciences0000-0002-9235-680XTürkiye
Ilyasov R, Lim S, Lee ML, Kwon HW, Nikolenko A. EFFECT OF MITICIDES AMITRAZ AND FLUVALINATE ON REPRODUCTION AND PRODUCTIVITY OF HONEY BEE APIS MELLIFERA. U.Arı D.-U.Bee J. 2021;21(1):21-30.
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