Fumigant toxicity of eleven Chinese herbal essential oils against an ectoparasitic mite (Varroa destructor) of the honey bee (Apis mellifera)

References

• Amdam, G. V., Hartfelder, K., Norberg, K., Hagen, A., & Omholt, S. W. (2004). Altered physiology in worker honey bees (Hymenoptera: Apidae) infested with the mite Varroa destructor (Acari: Varroidae): A factor in colony loss during overwintering. Journal of Economic Entomology, 97(3), 741–747. doi:10.1093/jee/97.3.741
   PubMed Web of Science ®Google Scholar
• Ariana, A., Ebadi, R., & Tahmasebi, G. (2002). Laboratory evaluation of some plant essences to control Varroa destructor (Acari: Varroidae). Experimental & Applied Acarology, 27(4), 319.
   PubMed Web of Science ®Google Scholar
• Bogdanov, S. (2006). Contaminants of bee products. Apidologie, 37(1), 1–18. doi:10.1051/apido:2005043
   Web of Science ®Google Scholar
• Calderone, N. W. (1999). Evaluation of formic acid and a thymol-based blend of natural products for the fall control of Varroa jacobsoni (Acari: Varroidae) in colonies of Apis mellifera (Hymenoptera: Apidae). Journal of Economic Entomology, 92(2), 253–260. doi:10.1093/jee/92.2.253
   Web of Science ®Google Scholar
• Dietemann, V., Pflugfelder, J., Anderson, D., Charrière, J.-D., Chejanovsky, N., Dainat, B., … Neumann, P. (2012). Varroa destructor: Research avenues towards sustainable control. Journal of Apicultural Research, 51(1), 125–132. doi:10.3896/IBRA.1.51.1.15
   Web of Science ®Google Scholar
• Ebadollahi, A., Jalali Sendi, J., Aliakbar, A., & Razmjou, J. (2014). Chemical composition and acaricidal effects of essential oils of Foeniculum vulgare Mill.(Apiales: Apiaceae) and Lavandula angustifolia Miller (Lamiales: Lamiaceae) against Tetranychus urticae Koch (Acari: Tetranychidae). Psyche: A Journal of Entomology, 2014(3), 1–6. doi:10.1155/2014/424078
   Google Scholar
• Ellis, J. D., & Munn, P. A. (2005). The worldwide health status of honey bees. Bee World, 86(4), 88–101. doi:10.1080/0005772X.2005.11417323
   Web of Science ®Google Scholar
• Elzen, P. J., Baxter, J. R., Spivak, M., & Wilson, W. T. (2000). Control of Varroa jacobsoni Oud. resistant to fluvalinate and amitraz using coumaphos. Apidologie, 31(3), 437–441. doi:10.1051/apido:2000134
   Web of Science ®Google Scholar
• Fathy, H. M., & Fouly, A. H. (1997). The effect of natural volatile oil plants on Apis mellifera honey bee and on the Varroa jacobsoni in the bee colonies. Apiacta, 32(1), 5–12.
   Google Scholar
• Fernández, M., Picó, Y., & Manes, J. (2002). Analytical methods for pesticide residue determination in bee products. Journal of Food Protection, 65(9), 1502–1511. doi:10.4315/0362-028X-65.9.1502
   PubMed Web of Science ®Google Scholar
• Floris, I., Satta, A., Cabras, P., Garau, V. L., & Angioni, A. (2004). Comparison between two thymol formulations in the control of Varroa destructor: Effectiveness, persistence, and residues. Journal of Economic Entomology, 97(2), 187–191. doi:10.1093/jee/97.2.187
   PubMed Web of Science ®Google Scholar
• Fouly, A. H., & Al-Dehhairi, M. A. (2009). Evaluation of infestation levels of the ectoparasitic mite Varroa destructor infesting honeybee Apis mellifera and its control using essential oil in Qassim Region, Saudi Arabia. Journal of Entomology, 6(3), 135–144. doi:10.3923/je.2009.135.144
   Google Scholar
• Gashout, H. A., & Guzmán-Novoa, E. (2009). Acute toxicity of essential oils and other natural compounds to the parasitic mite, Varroa destructor, and to larval and adult worker honey bees (Apis mellifera L.). Journal of Apicultural Research, 48(4), 263–269. doi:10.3896/IBRA.1.48.4.06
   Web of Science ®Google Scholar
• Goswami, V., & Khan, M. S. (2013). Management of varroa mite, Varroa destructor by essential oil and formic acid in Apis mellifera Linn. Colonies. Journal of Natural Products, 6, 206–210.
   Google Scholar
• Helander, I. M., Alakomi, H. L., Latva-Kala, K., Mattila-Sandholm, T., Pol, I., Smid, E. J., … von Wright, A. (1998). Characterization of the action of selected essential oil components on Gram-negative bacteria. Journal of Agricultural and Food Chemistry, 46(9), 3590–3595. doi:10.1021/jf980154m
   Web of Science ®Google Scholar
• Imdorf, A., Bogdanov, S., Ochoa, R. I., & Calderone, N. W. (1999). Use of essential oils for the control of Varroa jacobsoni Oud. in honey bee colonies. Apidologie, 30(2–3), 209–228. doi:10.1051/apido:19990210
   Web of Science ®Google Scholar
• Isman, M. B. (2000). Plant essential oils for pest and disease management. Crop Protection, 19(8–10), 603–608. doi:10.1016/S0261-2194(00)00079-X
   Web of Science ®Google Scholar
• Knobloch, K., Pauli, A., Iberl, B., Weigand, H., & Weis, N. (1989). Antibacterial and antifungal properties of essential oil components. Journal of Essential Oil Research, 1(3), 119–128. doi:10.1080/10412905.1989.9697767
   Google Scholar
• Korpela, S., Aarhus, A., Fries, I., & Hansen, H. (1992). Varroa jacobsoni Oud. in cold climates: Population growth, winter mortality and influence on the survival of honey bee colonies. Journal of Apicultural Research, 31(3–4), 157–164. doi:10.1080/00218839.1992.11101278
   Web of Science ®Google Scholar
• Kostyukovsky, M., Rafaeli, A., Gileadi, C., Demchenko, N., & Shaaya, E. (2002). Activation of octopaminergic receptors by essential oil constituents isolated from aromatic plants: Possible mode of action against insect pests. Pest Management Science, 58(11), 1101–1106. doi:10.1002/ps.548
   PubMed Web of Science ®Google Scholar
• Le Conte, Y., Ellis, M., & Ritter, W. (2010). Varroa mites and honey bee health: Can Varroa explain part of the colony losses?. Apidologie, 41(3), 353–363. doi:10.1051/apido/2010017
   Web of Science ®Google Scholar
• Lee, B. H., Choi, W. S., Lee, S. E., & Park, B. S. (2001). Fumigant toxicity of essential oils and their constituent compounds towards the rice weevil, Sitophilus oryzae (L.). Crop Protection, 20(4), 317–320. doi:10.1016/S0261-2194(00)00158-7
   Web of Science ®Google Scholar
• Li, L., Lin, Z.-G., Wang, S., Su, X.-L., Gong, H.-R., Li, H.-L., … Zheng, H.-Q. (2017). The effects of clove oil on the enzyme activity of Varroa destructor Anderson and Trueman (arachnida: Acari: Varroidae). Saudi Journal of Biological Sciences, 24(5), 996–1000. doi:10.1016/j.sjbs.2017.01.052
   PubMed Web of Science ®Google Scholar
• Lin, Z., Qin, Y., Page, P., Wang, S., Li, L., Wen, Z., … Dietemann, V. (2018). Reproduction of parasitic mites Varroa destructor in original and new honeybee hosts. Ecology and Evolution, 8(4), 2135–2145.
   PubMed Web of Science ®Google Scholar
• Liu, J. X., Sun, Y. H., & Li, C. P. (2015). Volatile oils of Chinese crude medicines exhibit antiparasitic activity against human Demodex with no adverse effects in vivo. Experimental and Therapeutic Medicine, 9(4), 1304–1308. doi:10.3892/etm.2015.2272
   PubMed Web of Science ®Google Scholar
• Lodesani, M. (2004). Control strategies against Varroa mites. Parassitologia, 46(1–2), 277–279.
   PubMedGoogle Scholar
• Maggi, M. D., Ruffnengo, S. R., Gende, L. B., Sarlo, E. G., Eguaras, M. J., Bailac, P. N., & Ponzi, M. I. (2010). Laboratory evaluations of Syzygium aromaticum (L.) Merr. et Perry essential oil against Varroa destructor. Journal of Essential Oil Research, 22(2), 119–122. doi:10.1080/10412905.2010.9700278
   Web of Science ®Google Scholar
• Martin, S. J. (2004). Acaricide (pyrethroid) resistance in Varroa destructor. Bee World, 85(4), 67–69. doi:10.1080/0005772X.2004.11099632
   Web of Science ®Google Scholar
• Matheson, A. (1996). World bee health update 1996. Bee World, 77(1), 45–51. doi:10.1080/0005772X.1996.11099281
   Web of Science ®Google Scholar
• Meixner, M. D., Kryger, P., & Costa, C. (2015). Effects of genotype, environment, and their interactions on honey bee health in Europe. Current Opinion in Insect Science, 10, 177–184. doi:10.1016/j.cois.2015.05.010
   PubMed Web of Science ®Google Scholar
• Milani, N. (1995). The resistance of Varroa jacobsoni Oud to pyrethroids: A laboratory assay. Apidologie, 26(5), 415–429. doi:10.1051/apido:19950507
   Web of Science ®Google Scholar
• Milani, N. (1999). The resistance of Varroa jacobsoni Oud. to acaricides. Apidologie, 30(2-3), 229–234. doi:10.1051/apido:19990211
   Web of Science ®Google Scholar
• Milani, N., & Barbattini, R. (1988). Effectiveness of Apistan (fluvalinate) in the control of Varroa jacobsoni Oude-mans and its tolerance by Apis mellifera Linnaeus. Apicoltura, 4, 39–58.
   Google Scholar
• Milani, N., & Iob, M. (1998). Plastic strips containing organophosphorous acaricides to control Varroa jacobsoni: a preliminary experiment. American Bee Journal, 138(8), 612–615.
   Google Scholar
• Momen, F. M., Amer, S. A. A., & Refaat, A. M. (2001). Influence of mint and peppermint on Tetranychus urticae and some predacious mites of the family Phytoseiidae (Acari: Tetranychidae: Phytoseiidae). Acta Phytopathologica et Entomologica Hungarica, 36(1–2), 143–153. doi:10.1556/APhyt.36.2001.1-2.17
   Google Scholar
• Nazzi, F., Brown, S. P., Annoscia, D., Del Piccolo, F., Di Prisco, G., Varricchio, P., … Pennacchio, F. (2012). Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathogens, 8(6), e1002735. doi:10.1371/journal.ppat.1002735
   PubMed Web of Science ®Google Scholar
• Nazzi, F., & Le conte, Y. L. (2016). Ecology of Varroa destructor, the major ectoparasite of the western honey bee, Apis mellifera. Annual Review of Entomology, 61(1), 417–432. doi:10.1146/annurev-ento-010715-023731
   PubMed Web of Science ®Google Scholar
• Neumann, P., & Carreck, N. L. (2010). Honey bee colony losses. Journal of Apicultural Research, 49(1), 1–6. doi:10.3896/IBRA.1.49.1.01
   Web of Science ®Google Scholar
• Oldroyd, B. P. (2007). What's killing American honey bees?. PLoS Biology, 5(6), e168. doi:10.1371/journal.pbio.0050168
   PubMed Web of Science ®Google Scholar
• Ramsey, S. D., Ochoa, R., Bauchan, G., Gulbronson, C., Mowery, J. D., Cohen, A., … vanEngelsdorp, D. (2019). Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proceedings of the National Academy of Sciences, 116(5), 1792–1801. doi:10.1073/pnas.1818371116
   PubMed Web of Science ®Google Scholar
• Rattan, R. S. (2010). Mechanism of action of insecticidal secondary metabolites of plant origin. Crop Protection, 29(9), 913–920. doi:10.1016/j.cropro.2010.05.008
   Web of Science ®Google Scholar
• Rios-Estepa, R., Turner, G. W., Lee, J. M., Croteau, R. B., & Lange, B. M. (2008). A systems biology approach identifies the biochemical mechanisms regulating monoterpenoid essential oil composition in peppermint. Proceedings of the National Academy of Sciences, 105(8), 2818–2823. doi:10.1073/pnas.0712314105
   PubMed Web of Science ®Google Scholar
• Rosenkranz, P., Aumeier, P., & Ziegelmann, B. (2010). Biology and control of Varroa destructor. Journal of Invertebrate Pathology, 103(1), S96–S119. doi:10.1016/j.jip.2009.07.016
   PubMed Web of Science ®Google Scholar
• Ruffinengo, S., Eguaras, M., Floris, I., Faverin, C., Bailac, P., & Ponzi, M. (2005). LD50 and repellent effects of essential oils from argentinian wild plant species on Varroa destructor. Journal of Economic Entomology, 98(3), 651–655. doi:10.1603/0022-0493-98.3.651
   PubMed Web of Science ®Google Scholar
• Sammataro, D., Untalan, P., Guerrero, F., & Finley, J. (2005). The resistance of varroa mites (Acari: Varroidae) to acaricides and the presence of esterase. International Journal of Acarology, 31(1), 67–74. doi:10.1080/01647950508684419
   Web of Science ®Google Scholar
• Semkiw, P., Skubida, P., & Pohorecka, K. (2013). The amitraz strips efficacy in control of Varroa destructor after many years application of amitraz in apiaries. Journal of Apicultural Science, 57(1), 107–121. doi:10.2478/jas-2013-0012
   Web of Science ®Google Scholar
• Sertkaya, E., Kaya, K., & Soylu, S. (2010). Acaricidal activities of the essential oils from several medicinal plants against the carmine spider mite (Tetranychus cinnabarinus Boisd.)(Acarina: Tetranychidae). Industrial Crops and Products, 31(1), 107–112. doi:10.1016/j.indcrop.2009.09.009
   Web of Science ®Google Scholar
• Shen, M., Yang, X., Cox-Foster, D., & Cui, L. (2005). The role of varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees. Virology, 342(1), 141–149. doi:10.1016/j.virol.2005.07.012
   PubMed Web of Science ®Google Scholar
• Su, X., Zheng, H., Fei, Z., & Hu, F. (2012). Effectiveness of herbal essential oils as fumigants to control Varroa destructor in laboratory assays. Chinese Journal of Applied Entomology, 49(5), 1189–1195.
   Google Scholar
• Tewarson, N. C. (1987). Use of host hemolymph proteins, seasonal reproduction and a hypothesis on nutritional imprinting in the honey bee mite, Varroa jacobsoni, on Apis mellifera and Apis cerana. In Eder J, Rembold H, (Eds), Chemistry and Biology of Social Insects (pp. 688–689). Munich: J Peperny.
   Google Scholar
• Wallace, R. J. (2004). Antimicrobial properties of plant secondary metabolites. Proceedings of the Nutrition Society, 63(4), 621–629. doi:10.1079/PNS2004393
   PubMed Web of Science ®Google Scholar
• Wallner, K. (1999). Varroacides and their residues in bee products. Apidologie, 30(2-3), 235–248. doi:10.1051/apido:19990212
   Web of Science ®Google Scholar
• Wu, H. Q., Li, L., Li, J., He, Z. D., Liu, Z. G., Zeng, Q. Q., & Wang, Y. S. (2012). Acaricidal activity of DHEMH, derived from patchouli oil, against house dust mite, Dermatophagoides farinae. Chemical & Pharmaceutical Bulletin, 60(2), 178–182. doi:10.1248/cpb.60.178
   PubMed Web of Science ®Google Scholar
• Yang, X., & Cox-Foster, D. (2007). Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge. Parasitology, 134(03), 405–412. doi:10.1017/S0031182006000710
   PubMed Web of Science ®Google Scholar