Summer brood interruption as integrated management strategy for effective Varroa control in Europe

References

• Al Toufailia, H., Scandian, L., & Ratnieks, F. L. W. (2015). Towards integrated control of varroa: 2) comparing application methods and doses of oxalic acid on the mortality of phoretic Varroa destructor mites and their honey bee hosts. Journal of Apicultural Research, 54(2), 108–120. https://doi.org/10.1080/00218839.2015.1106777
   Web of Science ®Google Scholar
• Allais, L., Giudo, G., Panella, F. (2010). Stagione 2010 e varroa: il blocco della covata. Open Publication. https://ita.calameo.com/read/002493353a756fed5710a
   Google Scholar
• 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. https://doi.org/10.1093/jee/97.3.741
   PubMed Web of Science ®Google Scholar
• Bogdanov, S., Charrière, J.-D., Imdorf, A., Kilchenmann, V., & Fluri, P. (2002). Determination of residues in honey after treatments with formic and oxalic acid under field conditions. Apidologie, 33(4), 399–409. https://doi.org/10.1051/apido:2002029
   Web of Science ®Google Scholar
• Bolli, H. K., Bogdanov, S., Imdorf, A., & Fluri, P. (1993). Action of formic acid on Varroa jacobsoni Oud and the honeybee (Apis mellifera L.). Apidologie, 24(1), 51–57. https://doi.org/10.1051/apido:19930106
   Web of Science ®Google Scholar
• Brodschneider, R., Brus, J., & Danihlík, 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
   Web of Science ®Google Scholar
• Brodschneider, R., Gray, A., van der Zee, R., Adjlane, N., Brusbardis, V., Charrière, J.-D., Chlebo, R., Coffey, M. F., Crailsheim, K., Dahle, B., Danihlík, J., Danneels, E., de Graaf, D. C., Dražić, M. M., Fedoriak, M., Forsythe, I., Golubovski, M., Gregorc, A., Grzęda, U., … Woehl, S. (2016). Preliminary analysis of loss rates of honey bee colonies during winter 2015/16 from the COLOSS survey. Journal of Apicultural Research, 55(5), 375–378. https://doi.org/10.1080/00218839.2016.1260240
   Web of Science ®Google Scholar
• Bubalo, D., Pechhacker, H., Licek, E., Kezic, N., & Sulimanovic, D. (2005). The effect of Varroa destructor infestation on flight activity and mating efficiency of drones (Apis mellifera L.). Vet.Med.Austria, 92, 11–15.
   Google Scholar
• Büchler, R., Berg, S., & Le Conte, Y. (2010). Breeding for resistance to Varroa destructor in Europe. Apidologie, 41(3), 393–408. https://doi.org/10.1051/apido/2010011
   Web of Science ®Google Scholar
• Büchler, R., Moritz, R., Garrido, C., Bienefeld, K., Ehrhardt, K. (2006). Male fitness in relation to colony development and varroosis infection. Proceedings of the 2nd European Conference of Apidology (pp. 44–45). Prague.
   Google Scholar
• Büchler, R., & Uzunov, A. (2016). Mach mal Pause, Varroa-Bekämpfungsstrategie neu ausrichten! Die Biene, 152(3), 7–9.
   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. https://doi.org/10.1093/jee/92.2.253
   Web of Science ®Google Scholar
• Chauzat, P., Laurent, M., Rivière, M. P., Saugeon, C., Hendrikx, P., & Ribière-Chabert, M. (2014). A pan-European epidemiological study on honey bee colony losses 2012–2013. European Union Reference Laboratory for Honeybee Health, Brussels, Rapport technique.
   Google Scholar
• Coffey, M. F., & Breen, J. (2016). The efficacy and tolerability of Api-Bioxal® as a winter varroacide in a cool temperate climate. Journal of Apicultural Research, 55(1), 65–73. https://doi.org/10.1080/00218839.2016.1200866
   Web of Science ®Google Scholar
• DeGrandi-Hoffman, G., Ahumada, F., Zazueta, V., Chambers, M., Hidalgo, G., & de Jong, E. W. (2016). Population growth of Varroa destructor (Acari: Varroidae) in honey bee colonies is affected by the number of foragers with mites. Experimental & Applied Acarology, 69(1), 21–34. https://doi.org/10.1007/s10493-016-0022-9
   PubMed Web of Science ®Google Scholar
• Duay, P., de Jong, D., & Engels, W. (2003). Decreased flight performance and sperm production in drones of the honey bee (Apis mellifera) slightly infested by Varroa destructor mites. Apidologie, 34(1), 61–65. https://doi.org/10.1051/apido:2002052
   Web of Science ®Google Scholar
• Eguaras, M., Palacio, M. A., Faverin, C., Basualdo, M., Del Hoyo, M. L., Velis, G., & Bedascarrasbure, E. (2003). Efficacy of formic acid in gel for Varroa control in Apis mellifera L.: Importance of the dispenser position inside the hive. Veterinary Parasitology, 111(2–3), 241–245. https://doi.org/10.1016/S0304-4017(02)00377-1
   PubMed Web of Science ®Google Scholar
• European Parliament. (2018). Prospects and challenges for the EU apiculture sector. P8_TA(2018)0057 (2017/2115(INI)). https://www.europarl.europa.eu/doceo/document/TA-8-2018-0057_EN.html
   Google Scholar
• Forster, I. W. (1969). Swarm control in honey bee colonies. New Zealand Journal of Agricultural Research, 12(3), 605–610. https://doi.org/10.1080/00288233.1969.10421245
   Web of Science ®Google Scholar
• Fries, I. (1991). Treatment of sealed honey-bee brood with formic-acid for control of Varroa jacobsoni. American Bee Journal, 131(5), 313–314.
   Google Scholar
• Fries, I., Hansen, H., Imdorf, A., & Rosenkranz, P. (2003). Swarming in honey bees (Apis mellifera) and Varroa destructor population development in Sweden. Apidologie, 34(4), 389–397. https://doi.org/10.1051/apido:2003032
   Web of Science ®Google Scholar
• Genersch, E., von der Ohe, W., Kaatz, H., Schroeder, A., Otten, C., Büchler, R., Berg, S., Ritter, W., Mühlen, W., Gisder, S., Meixner, M., Liebig, G., & Rosenkranz, P. (2010). The German bee monitoring project: A long term study to understand periodically high winter losses of honey bee colonies. Apidologie, 41(3), 332–352. https://doi.org/10.1051/apido/2010014
   Web of Science ®Google Scholar
• 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
   Web of Science ®Google Scholar
• Gregorc, A., Adamczyk, J., Kapun, S., & Planinc, I. (2016). Integrated varroa control in honey bee (Apis mellifera carnica) colonies with or without brood. Journal of Apicultural Research, 55(3), 253–258. https://doi.org/10.1080/00218839.2016.1222700
   Web of Science ®Google Scholar
• 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
   Web of Science ®Google Scholar
• 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 US beekeeping operations. Journal of Economic Entomology, 112(4), 1509–1525. https://doi.org/10.1093/jee/toz088
   PubMed Web of Science ®Google Scholar
• Hatjina, F., Costa, C., Büchler, R., Uzunov, A., Drazic, M., Filipi, J., Charistos, L., Ruottinen, L., Andonov, S., Meixner, M. D., Bienkowska, M., Dariusz, G., Panasiuk, B., Conte, Y. L., Wilde, J., Berg, S., Bouga, M., Dyrba, W., Kiprijanovska, H., … Kezic, N. (2014). Population dynamics of European honey bee genotypes under different environmental conditions. Journal of Apicultural Research, 53(2), 233–247. https://doi.org/10.3896/IBRA.1.53.2.05
   Web of Science ®Google Scholar
• Imdorf, A., Buehlmann, G., Gerig, L., Kilchenmann, V., & Wille, H. (1987). Überprüfung der Schätzmethode zur Ermittlung der Brutfläche und der Anzahl Arbeiterinnen in freifliegenden Bienenvölkern. Apidologie, 18(2), 137–146. https://doi.org/10.1051/apido:19870204
   Web of Science ®Google Scholar
• Imdorf, A., Buehlmann, G., Gerig, L., Kilchenmann, V., Wille, H. (2019). Examination of the method for estimating the brood area and number of worker bees in free-flying bee colonies. https://doi.org/10.5281/zenodo.3341580.
   Google Scholar
• Locke, B. (2016). Natural Varroa mite-surviving Apis mellifera honeybee populations. Apidologie, 47 (3), 467–482. https://doi.org/10.1007/s13592-015-0412-8
   Google Scholar
• Lodesani, M., Franceschetti, S., & Dall’Ollio, R. (2019). Evaluation of early spring bio-technical management techniques to control varroosis in Apis mellifera. Apidologie, 50(2), 131–140. https://doi.org/10.1007/s13592-018-0621-z
   Web of Science ®Google Scholar
• Martel, A.-C., Zeggane, S., Aurières, C., Drajnudel, P., Faucon, J.-P., & Aubert, M. (2007). Acaricide residues in honey and wax after treatment of honey bee colonies with Apivar or Asuntol. Apidologie, 38(6), 534–544. https://doi.org/10.1051/apido:2007038
   Web of Science ®Google Scholar
• Martin, S. J. (2002). The role of Varroa and viral pathogens in the collapse of honeybee colonies: A modelling approach. Journal of Applied Ecology, 38(5), 1082–1093. https://doi.org/10.1046/j.1365-2664.2001.00662.x
   Web of Science ®Google Scholar
• Maul, V., Klepsch, A., & Assmann-Werthmüller, U. (1988). Das Bannwabenverfahren als Element Imkerlicher Betriebweise bei starkem Befall mit Varroa jacobsoni Oud. Apidologie, 19(2), 139–154. https://doi.org/10.1051/apido:19880204
   Web of Science ®Google Scholar
• Meixner, M. D., Francis, R. M., Gajda, A., Kryger, P., Andonov, S., Uzunov, A., Topolska, G., Costa, C., Amiri, E., Berg, S., Bienkowska, M., Bouga, M., Büchler, R., Dyrba, W., Gurgulova, K., Hatjina, F., Ivanova, E., Janes, M., Kezic, N., … Wilde, J. (2014). Occurrence of parasites and pathogens in honey bee colonies used in a European genotype-environment interactions experiment. Journal of Apicultural Research, 53(2), 215–229. https://doi.org/10.3896/IBRA.1.53.2.04
   Web of Science ®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
• Moosbeckhofer, R., Pechhacker, H., Unterweger, H., Bandion, F., & Heinrich-Lenz, A. (2003). Investigations on the oxalic acid content of honey from oxalic acid treated and untreated bee colonies. European Food Research and Technology, 217(1), 49–52. https://doi.org/10.1007/s00217-003-0698-z
   Web of Science ®Google Scholar
• Mozes-Koch, R., Slabezki, Y., Efrat, H., Kalev, H., Kamer, Y., Yakobson, B. A., & Dag, A. (2000). First detection in Israel of fluvalinate resistance in the Varroa mite using bioassay and biochemical methods. Experimental and Applied Acarology, 24(1), 35–43. https://doi.org/10.1023/A:1006379114942
   PubMed Web of Science ®Google Scholar
• Nanetti, A., Besana, A. M., Baracani, G., Romanelli, R., Galuppi, R. (2011). Artificial brood interruption in combination with oxalic acid trickling in the control of varroa mite. In Proceedings of 42nd International Apicultural Congress.
   Google Scholar
• Nanetti, A., Büchler, R., Charriere, J.-D., Fries, I., Helland, S., Imdorf, A., Korpela, S., & Kristiansen, P. (2003). Oxalic acid treatments for varroa control (review). Apiacta, 38, 81–87.
   Google Scholar
• Nolan, M. P., & Delaplane, K. S. (2017). Distance between honey bee Apis mellifera colonies regulates populations of Varroa destructor at a landscape scale. Apidologie, 48(1), 8–16. https://doi.org/10.1007/s13592-016-0443-9
   Web of Science ®Google Scholar
• Pietropaoli, M., Giacomelli, A., Scholl, F., & Formato, G. (2010). L’ingabbiamento della regina. Apitalia, 11, 8–10.
   Google Scholar
• Ramsey, S. D., Ochoa, R., Bauchan, G., Gulbronson, C., Mowery, J. D., Cohen, A., Lim, D., Joklik, J., Cicero, J. M., Ellis, J. D., Hawthorne, D., & vanEngelsdorp, D. (2019). Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proceedings of the National Academy of Sciences of the United States of America, 116(5), 1792–1801. https://doi.org/10.1073/pnas.1818371116
   PubMed Web of Science ®Google Scholar
• Ratti, V., Kevan, P. G., & Eberl, H. J. (2016). A discrete-continuous modeling framework to study the role of swarming in a honeybee-Varroa destrutor-virus system. In Mathematical and computational approaches in advancing modern science and engineering (pp. 299–308). Springer.
   Google Scholar
• Rivera Gomis, J., Pietropaoli, M., Belardo, V., Cersini, A., Antognetti, V., Formato, G. (2017, March, 21–22). Comparison of the performances of two different cages (Cassian and Var Control®) used for the autumn brood interruption in Central Italy. Proceedings of COLOSS Workshop: “Assessment of Alternative Methods for Varroa Control”.
   Google Scholar
• Rosenkranz, P., Aumeier, P., & Ziegelmann, B. (2010). Biology and control of Varroa destructor. Journal of Invertebrate Pathology, 103, S96–S119. https://doi.org/10.1016/j.jip.2009.07.016
   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. https://doi.org/10.1080/01647950508684419
   Web of Science ®Google Scholar
• Satta, A., Floris, I., Eguaras, M., Cabras, P., Garau, V. L., & Melis, M. (2005). Formic acid-based treatments for control of Varroa destructor in a Mediterranean area. Journal of Economic Entomology, 98(2), 267–273. DOI: 10.1603/0022-0493-98.2.267.
   PubMed Web of Science ®Google Scholar
• Seeley, T. D., & Smith, M. L. (2015). Crowding honeybee colonies in apiaries can increase their vulnerability to the deadly ectoparasite Varroa destructor. Apidologie, 46(6), 716–727. https://doi.org/10.1007/s13592-015-0361-2
   Web of Science ®Google Scholar
• Simpson, J. (1958). The problem of swarming in beekeeping practice. Bee World, 39(8), 193–202. https://doi.org/10.1080/0005772X.1958.11095063
   Google Scholar
• Szabo, T. I. (2008). The effects of swarming and other factors on the development of varroa destructor populations in honey bee colonies. American Bee Journal, 148(7), 642–645.
   Google Scholar
• Thompson, H. M., Brown, M. A., Ball, R. F., & Bew, M. H. (2002). First report of Varroa destructor resistance to pyrethroids in the UK. Apidologie, 33(4), 357–366. https://doi.org/10.1051/apido:2002027
   Web of Science ®Google Scholar
• Underwood, R. M., & Currie, R. W. (2003). The effects of temperature and dose of formic acid on treatment efficacy against Varroa destructor (Acari: Varroidae), a parasite of Apis mellifera (Hymenoptera: Apidae). Experimental & Applied Acarology, 29(3–4), 303–313. https://doi.org/10.1023/a:1025892906393
   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