Essential oils against Varroa destructor: a soft way to fight the parasitic mite of Apis mellifera

References

• Accorti, M., Guarcini, R., & PersanoOddo, L. (1991). L’ape: Indicatorebiologico e insetto test. Redia, 74, 1–15.
   Google Scholar
• Adams, R. P. (2007). Identification of essential oil components by gas chromatography/mass spectroscopy (4th ed.). Allured Publ. Corp.
   Google Scholar
• Allen-Wardell, G., Bernhardt, P., Bitner, R., Burquez, A., Buchmann, S., Cane, J., Cox, P. A., Dalton, V., Feinsinger, P., Inouye, D., Jones, C. E., Kennedy, K., Kevan, P., Koopowitz, H., Medellin-Morales, S., & Nabhan, G. P. (1998). The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Conservation Biology, 12(1), 8–17.
   Web of Science ®Google Scholar
• Athanassiou C. G., Rani P. U., & Kavallieratos N. G. (2014) The use of plant extracts for stored product protection. In: Singh D. (Ed.), Advances in plant biopesticides. Springer.
   Google Scholar
• Bedini, S., Bougherra, H. H., Flamini, G., Cosci, F., Belhamel, K., Ascrizzi, R., & Conti, B. (2016a). Repellency of anethole-and estragole-type fennel essential oils against stored grain pests: The different twins. Bulletin of Insectology, 69(1), 149–157.
   Web of Science ®Google Scholar
• Bedini, S., Flamini, G., Cosci, F., Ascrizzi, R., Benelli, G., & Conti, B. (2016b). Cannabis sativa and Humulus lupulus essential oils as novel control tools against the invasive mosquito Aedes albopictus and fresh water snail Physella acuta. Industrial Crops and Products, 85, 318–323. https://doi.org/10.1016/j.indcrop.2016.03.008
   Web of Science ®Google Scholar
• Bedini, S., Flamini, G., Cosci, F., Ascrizzi, R., Echeverria, M. C., Guidi, L., Landi, M., Lucchi, A., & Conti, B. (2017). Artemisia spp. essential oils against the disease-carrying blowfly Calliphora vomitoria. Parasites & Vectors, 10(1), 80. https://doi.org/10.1186/s13071-017-2006-y
   PubMed Web of Science ®Google Scholar
• Bedini, S., Flamini, G., Girardi, J., Cosci, F., & Conti, B. (2015). Not just for beer: Evaluation of spent hops (Humulus lupulus L.) as a source of eco-friendly repellents for insect pests of stored foods. Journal of Pest Science, 88(3), 583–592. https://doi.org/10.1007/s10340-015-0647-1
   Web of Science ®Google Scholar
• Benelli, G., Bedini, S., Cosci, F., Toniolo, C., Conti, B., & Nicoletti, M. (2015). Larvicidal and ovideterrent properties of neem oil and fractions against the filariasis vector Aedes albopictus (Diptera: Culicidae): A bioactivity survey across production sites. Parasitology Research, 114(1), 227–236.
   PubMed Web of Science ®Google Scholar
• Benelli, G., Canale, A., & Conti, B. (2014). Eco-friendly control strategies against the Asian tiger mosquito, Aedes albopictus (Diptera: Culicidae): Repellency and toxic activity of plant essential oils and extracts. Pharmacologyonline, 1, 44–51.
   Google Scholar
• Bogdanov, S., Lüllmann, C., Martin, P., von der Ohe, W., Russmann, H., Vorwohl, G., Oddo, L. P., Sabatini, A.-G., Marcazzan, G. L., Piro, R., Flamini, C., Morlot, M., Lhéritier, J., Borneck, R., Marioleas, P., Tsigouri, A., Kerkvliet, J., Ortiz, A., Ivanov, T., … Vit, P. (1999). Honey quality and international regulatory standards: Review by the International Honey Commission. Bee World, 80(2), 61–69. https://doi.org/10.1080/0005772X.1999.11099428
   Web of Science ®Google Scholar
• Bougherra, H. H., Bedini, S., Flamini, G., Cosci, F., Belhamel, K., & Conti, B. (2015). Pistacia lentiscus essential oil has repellent effect against three major insect pests of pasta. Industrial Crops and Products, 63, 249–255. https://doi.org/10.1016/j.indcrop.2014.09.048
   Web of Science ®Google Scholar
• Bowen-Walker, P. L., & Gunn, A. (2001). The effect of the ectoparasitic mite, Varroa destructor on adult worker honeybee (Apis mellifera) emergence weights, water, protein, carbohydrate, and lipid levels. Entomologia Experimentalis et Applicata, 101(3), 207–217. https://doi.org/10.1046/j.1570-7458.2001.00905.x
   Web of Science ®Google Scholar
• Bowen-Walker, P. L., Martin, S. J., & Gunn, A. (1999). The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa Jacobsoni Oud. Journal of Invertebrate Pathology, 73(1), 101–106. https://doi.org/10.1006/jipa.1998.4807
   PubMed Web of Science ®Google Scholar
• Brasesco, C., Gende, L., Negri, P., Szawarski, N., Iglesias, A., Eguaras, M., Ruffinengo, S., & Maggi, M. (2017). Assessing in vitro acaricidal effect and joint action of a binary mixture between essential oil compounds (thymol, phellandrene, eucalyptol, cinnamaldehyde, myrcene, carvacrol) over ectoparasitic mite Varroa Destructor (Acari: Varroidae). Journal of Apicultural Science, 61(2), 203–215. https://doi.org/10.1515/jas-2017-0008
   Web of Science ®Google Scholar
• Campolo, O., Malacrinò, A., Zappalà, L., Laudani, F., Chiera, E., Serra, D., Russo, M., & Palmeri, V. (2014). Fumigant bioactivity of five Citrus essential oils against Tribolium confusum. Phytoparasitica, 42(2), 223–233. https://doi.org/10.1007/s12600-013-0355-4
   Web of Science ®Google Scholar
• Carayon, J. L., Téné, N., Bonnafé, E., Alayrangues, J., Hotier, L., Armengaud, C., & Treilhou, M. (2014). Thymol as an alternative to pesticides: Persistence and effects of Apilife Var on the phototactic behavior of the honeybee Apis mellifera. Environmental Science and Pollution Research International, 21(7), 4934–4939. https://doi.org/10.1007/s11356-013-2143-6
   PubMed Web of Science ®Google Scholar
• Chen, Y., Zhao, Y., Hammond, J., Hsu, H. T., Evans, J., & Feldlaufer, M. (2004). Multiple virus infections in the honey bee and genome divergence of honey bee viruses. Journal of Invertebrate Pathology, 87(2-3), 84–93. https://doi.org/10.1016/j.jip.2004.07.005
   PubMed Web of Science ®Google Scholar
• Commission of the European Communities (2002). Concerted Action 3686: “Coordination in Europe of research on integrated control of varroa mites in honey bee colonies”. Technical guidelines for the evaluation of treatments for control of varroa mites in honey bee colonies, Recommendations from the CA3686. Document prepared during discussions within the CA3686 working group: “Evaluation of treatment for control of varroa mites in honeybee colonies.”
   Google Scholar
• Conti, B., Benelli, G., Leonardi, M., Afifi, F. U., Cervelli, C., Profeti, R., Pistelli, L., & Canale, A. (2012). Repellent effect of Salvia dorisiana, S. longifolia, and S. sclarea (Lamiaceae) essential oils against the mosquito Aedes albopictus Skuse (Diptera: Culicidae). Parasitology Research, 111(1), 291–299.
   PubMed Web of Science ®Google Scholar
• Delaplane, K. S., Mayer, D. R., & Mayer, D. F. (2000). Crop pollination by bees. Cabi Publishing.
   Google Scholar
• Dietemann, V., Nazzi, F., Martin, S. J., Anderson, D. L., Locke, B., Delaplane, K. S., Wauquiez, Q., Tannahill, C., Frey, E., Ziegelmann, B., Rosenkranz, P., & Ellis, J. D. (2013). Standard methods for varroa research. Journal of Apicultural Research, 52(1), 1–54. https://doi.org/10.3896/IBRA.1.52.1.09
   Web of Science ®Google Scholar
• Di Prisco, G., Pennacchio, F., Caprio, E., Boncristiani, H. F., Jr., Evans, J. D., & Chen, Y. (2011). Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera. The Journal of General Virology, 92(Pt 1), 151–155. https://doi.org/10.1099/vir.0.023853-0
   PubMed Web of Science ®Google Scholar
• Downey, D. L., & Winston, M. L. (2001). Honey bee colony mortality and productivity with single and dual infestations of parasitic mite species. Apidologie, 32(6), 567–575. https://doi.org/10.1051/apido:2001144
   Web of Science ®Google Scholar
• Evans, J. D., Pettis, J. S., Hood, W. M., & Shimanuki, H. (2003). Tracking an invasive honey bee pest: Mitochondrial DNA variation in North American small hive beetles. Apidologie, 34(2), 103–109. https://doi.org/10.1051/apido:2003004
   Web of Science ®Google Scholar
• Gallai, N., Salles, J. M., Settele, J., & Vaissière, B. E. (2009). Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics, 68(3), 810–821. https://doi.org/10.1016/j.ecolecon.2008.06.014
   Web of Science ®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. https://doi.org/10.3896/IBRA.1.48.4.06
   Web of Science ®Google Scholar
• Ghasemi, V., Moharramipour, S., & Tahmasbi, G. (2011). Biological activity of some plant essential oils against Varroa destructor (Acari: Varroidae), an ectoparasitic mite of Apis mellifera (Hymenoptera: Apidae). Experimental & Applied Acarology, 55(2), 147–154. https://doi.org/10.1007/s10493-011-9457-1
   PubMed Web of Science ®Google Scholar
• Gunes, N., Aydın, L., Belenli, D., Hranitz, J. M., Mengilig, S., & Selova, S. (2017). Stress responses of honey bees to organic acid and essential oil treatments against varroa mites. Journal of Apicultural Research, 56(2), 175–181. https://doi.org/10.1080/00218839.2017.1291229
   Web of Science ®Google Scholar
• Higes, M., Martín, R., & Meana, A. (2006). Nosema ceranae, a new microsporidian parasite in honeybees in Europe. Journal of Invertebrate Pathology, 92(2), 93–95. https://doi.org/10.1016/j.jip.2006.02.005
   PubMed 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. https://doi.org/10.1051/apido:19990210
   Web of Science ®Google Scholar
• Ingram, M., Nabhan, G. C., & Buchmann, S. L. (1996). Impending pollination crisis threatens biodiversity and agriculture. Tropinet, 7, 1.
   Google Scholar
• Islam, N., Amjad, M., Ehsan-Ul-Haq, E. S., & Naz, F. (2016). Management of Varroa destructor by essential oils and formic acid in Apis Mellifera Linn. colonies. Journal of Entomology and Zoology Studies, 4(6), 97–104.
   Google Scholar
• Klein, A. M., Vaissiere, 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
   PubMed Web of Science ®Google Scholar
• Kraus, B., & Berg, S. (1994). Effect of a lactic acid treatment during winter in temperate climate upon Varroa jacobsoni Oud. and the bee (Apis mellifera L.) colony. Experimental and Applied Acarology, 18(8), 459–468. https://doi.org/10.1007/BF00051468
   Web of Science ®Google Scholar
• Li, X., Zhou, W., Liu, F., Zhu, G. Z., Shamsuzzoha, M., Celler, K., … Shao, Y. T. (2017). About materials science. Journal of Materials Research, 32, 12–28.
   Google Scholar
• Lima, T. C., da Silva, T. K. M., Silva, F. L., Barbosa-Filho, J. M., Marques, M. O. M., Santos, R. L. C., Cavalcanti, S. C. d H., & de Sousa, D. P. (2014). Larvicidal activity of Mentha x villosa Hudson essential oil, rotundifolone and derivatives. Chemosphere, 104, 37–43.
   PubMed Web of Science ®Google Scholar
• Lindberg, C. M., Melathopoulos, A. P., & Winston, M. L. (2000). Laboratory evaluation of miticides to control Varroa jacobsoni (Acari: Varroidae), a honey bee (Hymenoptera: Apidae) parasite. Journal of Economic Entomology, 93(2), 189–198. https://doi.org/10.1603/0022-0493-93.2.189
   PubMed Web of Science ®Google Scholar
• Lodesani, M., Colombo, M., & Spreafico, M. (1995). Ineffectiveness of Apistan® treatment against the mite Varroa jacobsoni Oud in several districts of Lombardy (Italy). Apidologie, 26(1), 67–72. https://doi.org/10.1051/apido:19950109
   Web of Science ®Google Scholar
• Lodesani, M., & Costa, C. (2005). Limits of chemotherapy in beekeeping: Development of resistance and the problem of residues. Bee World, 86(4), 102–109. https://doi.org/10.1080/0005772X.2005.11417324
   Web of Science ®Google Scholar
• Maddaloni, M., & Pascual, D. W. (2015). Isolation of oxalotrophic bacteria associated with Varroa destructor mites. Letters in Applied Microbiology, 61(5), 411–417. https://doi.org/10.1111/lam.12486
   PubMed Web of Science ®Google Scholar
• Maini, S., Medrzycki, P., & Porrini, C. (2010). The puzzle of honey bee losses: A brief review. Bulletin of Insectology, 63(1), 153–160.
   Web of Science ®Google Scholar
• Martin, S. J., Highfield, A. C., Brettell, L., Villalobos, E. M., Budge, G. E., Powell, M., Nikaido, S., & Schroeder, D. C. (2012). Global honey bee viral landscape altered by a parasitic mite. Science, 336(6086), 1304–1306. https://doi.org/10.1126/science.1220941
   PubMed Web of Science ®Google Scholar
• Matheson, A., Buchmann, S. L., O’Toole, C., Westrich, P., & Williams, I. H. (1996). The conservation of bees (p. 628). Academic.
   Google Scholar
• McGregor, S. E. (1976). Insect pollination of cultivated crop plants (Vol. 496). Agricultural Research Service, US Department of Agriculture.
   Google Scholar
• Milani, N. (1999). The resistance of Varroa jacobsoni Oud. to acaricides. Apidologie, 30(2-3), 229–234. https://doi.org/10.1051/apido:19990211
   Web of Science ®Google Scholar
• National Institute of Standards and Technology (NIST). (2014). NIST/EPA/NIH mass spectral library, NIST standard reference database number 69. The NIST Mass Spectrometry Data Center.
   Google Scholar
• Perrucci, S., Macchioni, G., Cioni, P. L., Flamini, G., & Morelli, I. (1995). Structure/activity relationship of some natural monoterpenes as acaricides against Psoroptes cuniculi. Journal of Natural Products, 58(8), 1261–1264. https://doi.org/10.1021/np50122a018
   PubMed Web of Science ®Google Scholar
• Pietropaoli, M., & Formato, G. (2018). Liquid formic acid 60% to control varroa mites (Varroa destructor) in honey bee colonies (Apis mellifera): Protocol evaluation. Journal of Apicultural Research, 57(2), 300–307. https://doi.org/10.1080/00218839.2017.1376767
   Web of Science ®Google Scholar
• Porrini, C., Ghini, S., Girotti, S., Sabatini, A. G., Gattavecchia, E., & Celli, G. (2002). Use of honey bees as bioindicators of environmental pollution in Italy. In J. Devillers, & M. H. Pham-Delègue, (Eds.), Honey bees: Estimating the environmental impact of chemicals (p. 186). CRC Press.
   Google Scholar
• Rajendran, S., & Sriranjini, V. (2008). Plant products as fumigants for stored-product insect control. Journal of Stored Products Research, 44(2), 126–135. https://doi.org/10.1016/j.jspr.2007.08.003
   Web of Science ®Google Scholar
• Ramzi, H., Ismaili, M. R., Aberchane, M., & Zaanoun, S. (2017). Chemical characterization and acaricidal activity of Thymus satureioides C. & B. and Origanumelongatum E. &M.(Lamiaceae) essential oils against Varroa destructor Anderson &Trueman (Acari: Varroidae). Industrial Crops and Products, 108, 201–207. https://doi.org/10.1016/j.indcrop.2017.06.031
   Web of Science ®Google Scholar
• Regnault-Roger, C., Vincent, C., & Arnason, J. T. (2012). Essential oils in insect control: Low-risk products in a high-stakes world. Annual Review of Entomology, 57(1), 405–424. https://doi.org/10.1146/annurev-ento-120710-100554
   PubMed Web of Science ®Google Scholar
• Romo-Chacón, A., Martínez-Contreras, L. J., Molina-Corral, F. J., Acosta-Muñiz, C. H., Ríos-Velasco, C., León-Door, A. P. D., & Rivera, R. (2016). Evaluation of oregano (Lippia berlandieri) essential oil and entomopathogenic fungi for Varroa destructor control in colonies of honey bee, Apis mellifera. Southwestern Entomologist, 41(4), 971–982. https://doi.org/10.3958/059.041.0427
   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. https://doi.org/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.
   PubMed Web of Science ®Google Scholar
• Sammataro, D., Gerson, U., & Needham, G. (2000). Parasitic mites of honey bees: Life history, implications, and impact. Annual Review of Entomology, 45, 519–548.
   PubMed Web of Science ®Google Scholar
• Shen, M., Cui, L., Ostiguy, N., & Cox-Foster, D. (2005). Intricate transmission routes and interactions between picorna-like viruses (Kashmir bee virus and sacbrood virus) with the honeybee host and the parasitic varroa mite. The Journal of General Virology, 86(Pt 8), 2281–2289. https://doi.org/10.1099/vir.0.80824-0
   PubMed Web of Science ®Google Scholar
• Wallner, K. (1999). Varroacides and their residues in bee products. Apidologie, 30(2-3), 235–248. https://doi.org/10.1051/apido:19990212
   Web of Science ®Google Scholar
• Watanabe, M. E. (1994). Pollination worries rise as honey bees decline. Science, 265(5176), 1170. https://doi.org/10.1126/science.265.5176.1170
   PubMed Web of Science ®Google Scholar
• Williams, P. H., Humphries, C. J., & Vane-Wright, R. I. (1991). Measuring biodiversity: Taxonomic relatedness for conservation priorities. Australian Systematic Botany, 4(4), 665–679. https://doi.org/10.1071/SB9910665
   Google Scholar
• Yang, X., & Cox-Foster, D. L. (2005). Impact of an ectoparasite on the immunity and pathology of an invertebrate: Evidence for host immunosuppression and viral amplification. Proceedings of the National Academy of Sciences USA, 102(21), 7470–7475. https://doi.org/10.1073/pnas.0501860102
   PubMed Web of Science ®Google Scholar