Evaluating the efficacy of HiveClean® in controlling the Varroa mite (Varroa destructor) and its potential side effects on the honey bee (Apis mellifera) colonies in Alborz province

Akyol, E. & Yeninar, H. (2008) Controlling Varroa destructor (Acari: Varroidae) in honeybee Apis mellifera (Hymenoptera: Apidae) colonies by using Thymovar^® and BeeVital^®. Italian Journal of Animal Science, 7, 237-242. https://doi.org/10.4081/ijas.2008.237

Albero, B., Miguel, E. & García-Valcárcel, A. I. (2023) Acaricide residues in beeswax. Implications in honey, brood and honeybee. Environmental Monitoring and Assessment, 195, 454. https://doi.org/10.1007/s10661-023-11047-6

Bahreini, R. (2003) A comparison of two methods of applying oxalic acid for control of varroa, Journal of Apicultural Research, 42:4, 82-83. http://dx.doi.org/10.1080/00218839.2003.11101098

Bahreini, R., Docherty, C., Feindel, D. & Muirhead, S. (2023) Comparing the efficacy of synthetic Varroacides and Varroa destructor phenotypic resistance using Apiarium and Mason jar bioassay techniques. Pest Management Science, 80(3), 1577-1592. https://doi.org/10.1002/ps.7891

Bahreini, R., Tahmasebi, G. H., Nowzari, J. & Talebi, M. (2004) A study of the efficacy of formic acid in controlling Varroa destructor and its correlation with temperature in Iran. Journal of Apicultural Research, 43(4), 158-161. https://doi.org/10.1080/00218839.2004.11101129

Benito-Murcia, M., Bartolomé, C., Maside, X., Bernal, J., Bernal, J. L., del Nozal, M. J., Meana, A., Botías, C., Martín-Hernández, R. & Higes, M. (2021) Residual Tau-Fluvalinate in honey bee colonies is coupled with evidence for selection for Varroa destructor resistance to pyrethroids. Insects, 12, 731. https://doi.org/10.3390/insects12080731

Berry, J. A., Bartlett, L. J., Bruckner, S., Baker, C., Braman, S. K., Delaplane, K. S. & Williams, G. R. (2022) Assessing repeated oxalic acid vaporization in honey bee (Hymenoptera: Apidae) colonies for control of the ectoparasitic mite Varroa destructor. Journal of Insect Science, 22(1), 15. https://doi.org/10.1093/jisesa/ieab089

Berry, J. A., Braman, S. K., Delaplane, K. S. & Bartlett, L. J. (2023) Inducing a summer brood break increases the efficacy of oxalic acid vaporization for Varroa destructor (Mesostigmata: Varroidae) control in Apis mellifera (Hymenoptera: Apidae) colonies. Journal of Insect Science, 23(6), 14. https://doi.org/10.1093/jisesa/iead085

Brodschneider, R., Brus, J. & Danihlik, J. (2019) Comparison of apiculture and winter mortality of honey bee colonies (Apis mellifera) in Austria and Czechia. Agriculture, Ecosystems & Environment, 274, 24-32. https://doi.org/10.1016/j.agee.2019.01.002

Büchler , R., Uzunov, A., Kovačić, M., Prešern, J., Pietropaoli, M., Hatjina, F., Pavlov, B., Charistos, L., Formato, G., Galarza, E., Gerula, D., Gregorc, A., Malagnini, V., Meixner, M., Nedić, N., Puškadija, Z., Rivera-Gomis, J., Jenko, M. R., Smodiš Škerl, M. I., Vallon, J., Vojt, D., Wilde, J. & Nanetti, A. (2020) Summer brood interruption as integrated management strategy for effective Varroa control in Europe. Journal of Apicultural Research, 59, 5,764-773. https://doi.org/10.1080/00218839.2020.1793278

Charrière, J. D. & Imdorf, A. (2002) Oxalic acid treatment by trickling against Varroa destructor: Recommendations for use in central Europe and under temperate climate conditions. Bee World, 83(2), 51-60. https://doi.org/10.1080/0005772X.2002.11099541

Coffey, M. F. & Breen, J. (2013) Efficacy of Apilife Var^® and Thymovar^® against Varroa destructor as an autumn treatment in a cool climate. Journal of Apicultural Research, 52, 5, 210-218. https://dx.doi.org/10.3896/IBRA.1.52.5.07

Coffey, M. F. (2007) Biotechnical methods in colony management, and the use of Apiguard^® and Exomite™ Apis for the control of the varroa mite (Varroa destructor) in Irish honey bee (Apis mellifera) colonies. Journal of Apicultural Research, 46, 4, 213-219. https://dx.doi.org/10.1080/00218839.2007.11101397

Delaplane, K. S., Van der Steen, J. & Guzman, N. E. (2013) Standard methods for estimating strength parameters of Apis mellifera colonies. Journal of Apicultural Research, 52(1), 1-12. https://doi.org/10.3896/IBRA.1.52.1.03

Dietemann, V., Nazzi, F., Martin, S. J., Anderson, D. L., Locke, B., Delaplane, K. S., Wauquiez, Q, Tannahil, C., Frey, E., Ziegelmann, B., Rosenkranz, P. & Ellis, J. D. (2013) Standard methods for varroa research. Journal of Apicultural Research, 52(1), 1-54. http://dx.doi.org/10.3896/IBRA.1.52.1.09

Elzen, P. J., Eischen, F. A., Baxter, J. R., Elzen, G. W. & Wilson, W. T. (1999) Detection of resist­ance in US Varroa jacobsoni Oud. (Mesostigmata: Varroidae) to the acar­icide fluvalinate. Apidologie, 30(1), 13-17. https://doi.org/10.1051/apido:19990102

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, 187-191. https://doi.org/10.1093/jee/97.2.187

Fries, I. & Rosenkranz, P. (1996) Number of reproductive cycles of Varroa jacobsoni in honeybee (Apis mellifera) colonies. Experimental and Applied Acarology, 20, 103-112 (1996). https://doi.org/10.1007/BF00051156

Giacomelli, A., Pietropaoli, M., Carvelli, A., Iacoponi, F. & Formato, G. (2016) Combination of thymol treatment (Apiguard^®) and caging the queen technique to fight Varroa destructor. Apidologie. 47(4), 606–616. https://doi.org/10.1007/s13592-015-0408-4

Giusti, M., Sabelli, C., Di Donato, A., Lamberti, D., Paturzo, C. E., Polignano, V., Lazzari, R.  & Felicioli, A. (2017) Efficacy and safety of Varterminator, a new formic acid medicine against the varroa mite. Journal of Apicultural Research, 56(2), 162-167. http://dx.doi.org/10.1080/00218839.2017.1291207

Gregorc, A. & Planinc, I. (2004) Dynamics of falling Varroa mites in honeybee (Apis mellifera) colonies following oxalic acid treatments. Acta Veterinaria Brno, 73, 385-391. https://doi.org/10.2754/AVB200473030385

Gregorc, A., Alburaki, M., Sampson, B., Knight, P. R. & Adamczyk, J. (2018) Toxicity of selected acaricides to honey bees (Apis mellifera) and Varroa (Varroa destructor Anderson and Trueman) and their use in controlling Varroa within honey bee colonies. Insects, 9, 55. https://doi.org/10.3390/insects9020055

Gregorc, A., Alburaki, M., Werle, C., Knight, P. R. & Adamczyk, J. (2017) Brood removal or queen caging combined with oxalic acid treatment to control varroa mites (Varroa destructor) in honey bee colonies (Apis mellifera). Apidologie, 48(6), 821–832. https://doi.org/10.1007/s13592-017-0526-2

Guzman-Novoa, E., Eccles, L., Calvete, Y., Mcgowan, J., Kelly, P. G. & Correa-Benítez, A. (2010) Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apidologie, 41, 443-450. https://doi.org/10.1051/apido/2009076

Haber, A. I., Steinhauer, N. A. & vanEngelsdorp. D (2019) Use of chemical and nonchemical methods for the control of Varroa destructor (Acari: Varroidae) and associated winter colony losses in U.S. beekeeping operations. Journal of Economic Entomology, 112, 1509–1525. https://doi.org/10.1093/jee/toz088

Hung, K-L. J., Kingston, J. M., Albrecht, M., Holway, D. A. & Kohn, J. R. (2018) The worldwide importance of honey bees as pollinators in natural habitats. Proceedings of the Royal Scociety B, 285, 20172140. http://dx.doi.org/10.1098/rspb.2017.2140

Kanelis, D., Tananaki, C., Liolios, V. & Rodopoulou, M. A. (2023) Evaluation of oxalic acid with glycerin efficacy against Varroa destructor (Varroidae): a four-year assay. Journal of Apicultural Research, 1-9. https://doi.org/10.1080/00218839.2023.2169368 

Kevan, P. G., Eisikowitch, D., Kinuthia, W., Martin, P., Mussen, E. C., Partap, U., Taylor, O. R., Thomas, V. G., Thorp, R.W., Vergara, C. H. & Winter, K. (2007) High quality bee products are important to agriculture: why, and what needs to be done. Journal of Apicultural Research, 46(1), 59-64. https://doi.org/10.1080/00218839.2007.11101368

Kovacic, M., Uzunov, A., Tlak Gajger, I., Pietropaoli, M., Soroker, V., Adjlane, N., Benko, V., Charistos, L., Dall’Olio, R., Formato, G., Hatjina, F., Malagnini, V., Freda, F., Otmi, A., Puškadija, Z., Villar, C. & Büchler, R. (2023) Honey vs. mite: a trade-off strategy by applying summer brood interruption for Varroa destructor control in the Mediterranean region. Insects, 14, 751. https://doi.org/10.3390/insects14090751

Lodesani, M., Costa, C. Besana, A., Dall’Olio, D., Franceschetti, S., Tesoriero, D. & Vaccari, G. (2014) Impact of control strategies for Varroa destructor on colony survival and health in northern and central regions of Italy. Journal of Apicultural Research, 53(1), 155–164. https://doi.org/10.3896/IBRA.1.53.1.17

Lodesani, M., Franceschetti, S. & Dall’Ollio, R. (2019) Evaluation of early spring bio-technical management techniques to control varroosis in Apis mellifera. Apidologie, 50, 131-140. https://doi.org/10.1007/s13592-018-0621-z  

Maggi, M, Tourn, E., Negri, P., Szawarski, N., Marconi, A., Gallez, L., Medici, S., Ruffinengo, S., Brasesco, C., De Feudis, L., Quintana, S., Sammataro, D. & Eguaras, M. (2016) A new formulation of oxalic acid for Varroa destructor control applied in Apis mellifera colonies in the presence of brood. Apidologie, 47, 596-605. https://doi.org/10.1007/s13592-015-0405-7

Maggi, M., Damiani, N., Ruffinengo, S. R., Brasesco, M. C., Szawarski, N., Mitton, G. A., Mariani, F., Sammataro, D., Quintana, S. & Eguaras, M. J. (2017) The susceptibility of Varroa destructor against oxalic acid: a study case. Bulletin of Insectology, 70(1), 39-44.

Martin, S. J. & Kemp, D. (1997) Average number of reproductive cycles performed by Varroa jacobsoni in honey bee (Apis mellifera) colonies. Journal of Apicultural Research, 36(3-4), 113-123. https://doi.org/10.1080/00218839.1997.11100937

McMenamin, A. J. & Genersch, E. (2015) Honey bee colony losses and associated viruses. Current Opinion in Insect Science, 8, 121-129. https://doi.org/10.1016/j.cois.2015.01.015

Mitton, G. A., Meroi Arcerito, F., Cooley, H., Fernández de Landa, G., Eguaras, M. J., Ruffinengo, S. R. & Maggi, M. D. (2022) More than sixty years living with Varroa destructor: a review of acaricide resistance. International Journal of Pest Management, 68, 1-18. https://doi.org/10.1080/09670874.2022.2094489

Ostiguy, N., Drummond, F. A., Aronstein, K., Eitzer, B., Ellis, J. D., Spivak, M. & Sheppard, W. S. (2019) Honey bee exposure to pesticides: a four-year nationwide study. Insects, 10(1), 13. https://doi.org/10.3390/insects10010013

Papa, G., Maier, R., Durazzo, A., Lucarini, M., Karabagias, I. K., Plutino, M., Bianchetto, E., Aromolo, R., Pignatti, G., Ambrogio, A., Pellecchia, M. & Negri, I. (2022) The honey bee Apis mellifera: an insect at the interface between human and ecosystem health. Biology, 11, 233. https://doi.org/10.3390/biology11020233

Papežíková, I., Palíková, M., Kremserová, S., Zachová, A., Peterová, H., Babák, V. & Navrátil, S. (2017) Effect of oxalic acid on the mite Varroa destructor and its host the honey bee Apis mellifera. Journal of Apicultural Research, 56(4), 1-9. https://doi.org/10.1080/00218839.2017.1327937

Prouty, C., Abou-Shaara, H. F., Stanford, B., Ellis, J. D. & Jack, C. (2023) Oxalic acid application method and treatment intervals for reduction of Varroa destructor (Mesostigmata: Varroidae) populations in Apis mellifera (Hymenoptera: Apidae) colonies. Journal of Insect Science, 23(6), 13, 1-8. https://doi.org/10.1093/jisesa/iead086

Rademacher, E. & Harz, M. (2006) Oxalic acid for the control of varroosis in honey bee colonies - a review. Apidologie, 37, 98-120. https://doi.org/10.1051/apido:2005063

Rashid, B., Khani, A., Ghasemi, V., Ghadamyari, M., Sahebzadeh, N. & Moharramipour, S. (2020) Evaluation of a new plant-based formulation for the treatment of varroosis in the honey bee colonies: efficacy and safety. Apidologie, 51, 1074-1090. https://doi.org/10.1007/s13592-020-00786-x

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. https://doi.org/10.1371/journal.pone.0227264

Rodriguez-Dehaibes, S. R., Parido Sedas, V. T., Luna-Olivars, G. & Villanuva-Jimenez, J. A. (2017) Two commercial formulations of natural compounds for Varroa destructor (Acari: Varroidae) control on Africanized bees under tropical climatic conditions. Journal of Apicultural Research, 56, 58-62. https://doi.org/10.1080/00218839.2016.1268323

Rosenkranz, P., Aumeier, P. & Ziegelmann, B. (2010) Biology and control of Varroa destructor. Journal of Invertebrate Pathology, 103, S96-119. https://doi.org/10.1016/j.jip.2009.07.016

Sabahi, Q., Morfin, N., Emsen, B., Gashout, H. A., Kelly, P. G., Otto, S., Merrill, A. R. & Guzman-Novoa, E. (2020) Evaluation of dry and wet formulations of oxalic acid, thymol, and oregano oil for Varroa mite (Acari: Varroidae) control in honey bee (Hymenoptera: Apidae) colonies. Journal of Economic Entomology, 113(6), 2588-2594. https://doi.org/10.1093/jee/toaa218

Smodiš Škerl, M. I., Rivera-Gomis, J., Tlak Gajger, I., Bubnic, J., Talakic, G., Formato, G., Baggio, A., Mutinelli, F., Tollenaers, W., Laget, D., Malagnini, V., Zanotelli, L. & Pietropaoli, M. (2021) Efficacy and toxicity of Varromed^® used for controlling Varroa destructor infestation in different seasons and geographical areas. Applied Sciences, 11, 8564. https://doi.org/10.3390/app11188564

Sun, Y. P. & Shepard, H. H. (1947) Methods of calculating and correcting the mortality of insects. Journal of Economic Entomology, 40(5), 710-715. https://doi.org/10.1093/jee/40.5.710

Thurston, D., Eccles, L., Kempers, M., Borges, D., Ducsharm, K., Ovinge, L., Stotesbury, D., Scarlett, R., Kozak, P., Petukhova, T., Guzman-Novoa, E. & Morfin, N. (2025) Efficacy and safety of an oxalic acid and glycerin formulation for Varroa destructor control in honey bee colonies during summer in a northern climate. Pathogens, 14, 724. https://doi.org/10.3390/pathogens14080724

Tlak Gajger, I. & Susec, P. (2019) Efficacy of varroacidal food additive appliance during summer treatment of honeybee colonies (Apis mellifera). Veterinarski Arhiv, 89, 87-96. https://doi.org/10.24099/vet.arhiv.0441

vanEngelsdorp, D., Evans, J. D., Saegerman, C., Mullin, C., Haubruge, E., Nguyen, B. K., Frazier, M., Frazier, J., Cox-Foster, D., Chen, Y., Underwood, R., Tarpy, D. R. & Pettis, J. S. (2009) Colony collapse disorder: a descriptive study. PLoS ONE, 4(8): e6481. https://doi.org/10.1371/journal.pone.0006481

Zhang, S., Ma, J., Zhang, L., Sun, Z., Zhao, Z. & Khan, N. (2022) Does adoption of honeybee pollination promote the economic value of kiwifruit farmers? Evidence from China. International Journal of Environmental Research and Public Health, 19, 8305. https://doi.org/10.3390/ijerph19148305