Ankara Üniversitesi Veteriner Fakültesi Dergisi
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What has been done in the fight against Varroa destructor: from the past to the present

Year 2022, Volume: 69 Issue: 2, 229 - 240, 25.03.2022

Ales GREGORC Caio DOMİNGUES Hidayet TUTUN Sedat SEVİN

https://doi.org/10.33988/auvfd.1029296

Abstract

Bees are the major pollinators in natural ecosystems and in the agricultural production of several crops used for human consumption. However, they are exposed to multiple stressors that are causing a serious decline in their population. We highlight a major one among them, the Varroa destructor mite (Varroa) that causes severe impacts on the health of honey bee colonies, transmitting a variety of viruses that can affect the survival ability of individual bees and entire colonies. Diagnosis and mite control methods have been intensively studied in recent decades, with many studies in different areas of knowledge having been conducted. This overview summarizes these studies with a focus on colony defense systems, biological characteristics of the parasite Varroa, diagnostic methods used to establish the infestation level of colonies, and currently used control methods.

Keywords

Diagnosis, Honey bee disease, mite, parasite, Varroa control

Thanks

The study was supported, and research topics discussed by COLOSS, Varroa control TF (Prevention of honey bee COlony LOSSes).

References

  • Akyol E, Yeninar H (2009): Use of oxalic acid to control Varroa destructor in honeybee (Apis mellifera L.) colonies. Turk J Vet Anim Sci, 33, 285-288.
  • Almecija G, Poirot B, Cochard P, et al (2020): Inventory of Varroa destructor susceptibility to amitraz and tau-fluvalinate in France. Exp Appl Acarol, 82, 1-16.
  • Alquisira-Ramírez EV, Paredes-Gonzalez JR, Hernández-Velázquez VM, et al (2014): In vitro susceptibility of Varroa destructor and Apis mellifera to native strains of Bacillus thuringiensis. Apidologie, 45, 707-718.
  • Amrine Jr JW, Noel RC, Webb D (2007): Results of 50% formic acid fumigation of honey bee hives [Apis mellifera ligustica (Hymenoptera: Apidae)] to control varroa mites (Acari: Varroidae) in brood combs in Florida, USA. Int J Acarol, 33, 99-109.
  • Ayan A, Tutun H, Aldemir OS (2019): Control methods against Varroa mites. Int J Adv Stud, 11, 19-23.
  • Aziz ZA, Ahmad A, Setapar SHM, et al (2018): Essential oils: extraction techniques, pharmaceutical and therapeutic potential-a review. Curr Drug Metab, 19, 1100-1110.
  • Beetsma J, Boot WJ, Calis J (1999): Invasion behaviour of Varroa jacobsoni Oud.: from bees into brood cells. Apidologie, 30, 125-140.
  • Berthoud H, Imdorf A, Haueter M, et al (2010): Virus infections and winter losses of honey bee colonies (Apis mellifera). J Apic Res, 49, 60-65.
  • Blenau W, Rademacher E, Baumann A (2012): Plant essential oils and formamidines as insecticides/acaricides: what are the molecular targets? Apidologie, 43, 334-347.
  • Boecking O, Spivak M (1999): Behavioral defenses of honey bees against Varroa jacobsoni Oud. Apidologie, 30, 141-158.
  • Bowen-Walker PL, Gunn A (2001): The effect of the ectoparasitic mite, Varroa destructor on adult workerhoneybee (Apis mellifera) emergence weights, water, protein,carbohydrate, and lipid levels. Entomol Exp Appl, 101, 207-217.
  • Bravo A, Likitvivatanavong S, Gill SS, et al (2011): Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochem Mol Biol, 41, 423-431.
  • Brodschneider R, Gray A, Adjlane N, et al (2018): Multi-country loss rates of honey bee colonies during winter 2016/2017 from the COLOSS survey. J Apic Res, 57, 452-457.
  • Brødsgaard CJ, Ritter W, Hansen H, et al (2000): Interactions among Varroa jacobsoni mites, acute paralysis virus, and Paenibacillus larvae larvae and their influence on mortality of larval honeybees in vitro. Apidologie, 31, 543-554.
  • Büchler R, Drescher W, Tornier I (1992): Grooming behaviour of Apis cerana, Apis mellifera and Apis dorsata and its effect on the parasitic mites Varroa jacobsoni and Tropilaelaps clareae. Exp Appl Acarol, 16, 313-319.
  • Büchler R, Uzunov A, Kovačić M, et al (2020): Summer brood interruption as integrated management strategy for effective Varroa control in Europe. J Apic Res, 59, 764-773.
  • Calderone NW (2005): Evaluation of drone brood removal for management of Varroa destructor (Acari: Varroidae) in colonies of Apis mellifera (Hymenoptera: Apidae) in the northeastern United States. J Econ Entomol, 98, 645-650.
  • Calderone NW, Nasr ME (1999): Evaluation of formic acid formulation for the fall control of Varroa jacobsoni (Acari: Varroidae) in colonies of the honey bee Apis mellifera (Hymenoptera: Apidae) in a temperate climate. J Econ Entomol, 92, 526-533.
  • Cengiz MM (2018): Effectiveness of combining certain biotechnical methods with thymol treatment against Varroa destructor infestation. Afr J Agric Res, 13, 2735-2740.
  • Chandler D, Sunderland KD, Ball BV, et al (2001): Prospective biological control agents of Varroa destructor n. sp., an important pest of the European honeybee, Apis mellifera. Biocontrol Sci Technol, 11, 429-448.
  • Charrière JD, Imdorf A, Bachofen B, et al (2003): The removal of capped drone brood: an effective means of reducing the infestation of varroa in honey bee colonies. Bee World, 84, 117-124.
  • Coffey MF (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. J Apic Res, 46, 213-219.
  • Cremer S, Armitage SAO, Schmid-Hempel P (2007): Social immunity. Curr Biol, 17, 693-702.
  • Cremer S, Sixt M (2009): Analogies in the evolution of individual and social immunity. Philos Trans R Soc Lond B Biol Sci, 364, 129-142.
  • Del Piccolo F, Nazzi F, Della Vedova G, et al (2010): Selection of Apis mellifera workers by the parasitic mite Varroa destructor using host cuticular hydrocarbons. Parasitology, 137, 967-973.
  • Dillon RJ, Dillon VM (2004): The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol, 49, 71-92.
  • Dorland WA (1990): Dorland’s Illustrated Medical Dictionary. W. B. Saunders Company, Philadelphia.
  • Duay P, De Jong D, Engels W (2003): Weight loss in drone pupae (Apis mellifera) multiply infested by Varroa destructor mites. Apidologie, 34, 61-65.
  • Eischen FA (1998): Trials (and tribulations) with formic acid for Varroa control. Am Bee J, 138, 734-735.
  • Ellis AM, Hayes GW, Ellis JD (2009): The efficacy of dusting honey bee colonies with powdered sugar to reduce Varroa mite populations. J Apic Res, 48, 72-76.
  • Fagan LL, Nelson WR, Meenken ED, et al (2012): Varroa management in small bites. J Appl Entomol, 136, 473-475.
  • Fakhimzadeh K, Ellis JD, Hayes JW (2011): Physical control of varroa mites (Varroa destructor): The effects of various dust materials on varroa mite fall from adult honey bees (Apis mellifera) in vitro. J Apic Res, 50, 203-211.
  • Feldlaufer MF, Pettis JS, Kochansky JP, et al (1997): A gel formulation of formic acid for the control of parasitic mites of honey bees. Am Bee J, 137, 661-663.
  • Flint ML (2012): IPM in practice: principles and methods of integrated pest management. University of California Agriculture and Natural Resources, California.
  • Fries I, Camazine S, Sneyd J (1994): Population dynamics of varroa jacobsoni: a model and a review. Bee World, 75, 5-28.
  • Fries I, Imdorf A, Rosenkranz P (2006): Survival of mite infested (Varroa destructor) honey bee (Apis mellifera) colonies in a Nordic climate. Apidologie, 37, 564-570.
  • Fries I, Rosenkranz P (1996): Number of reproductive cycles of Varroa jacobsoni in honey-bee (Apis mellifera) colonies. Exp Appl Acarol, 20, 103-112.
  • Fries I (2001): Is the total amount or the concentration of oxalic acid critical for efficacy in varroa mite control? Report at the IVC meeting in York.
  • Fuchs S (1990): Preference for drone brood cells by Varroa jacobsoni oud in colonies of Apis mellifera carnica. Apidologie, 21, 193-199.
  • Giacomelli A, Pietropaoli M, Carvelli A, et al (2016): Combination of thymol treatment (Apiguard®) and caging the queen technique to fight Varroa destructor. Apidologie, 47, 606-616.
  • Girisgin AO, Ozuicli M, Bah SA, et al (2019): Evaluation of some synthetic acaricides against Varroa destructor (Acari: Varroidae) in Turkey: an indication of resistance or misuse of fumigant amitraz? J Res Vet Med, 38, 67-70.
  • Goulson D, Nicholls E, Botías C, et al (2015): Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347, 1-10.
  • Gramacho KP (1999): Fatores que interferem no comportamento higiênico das abelhas Apis mellifera. Tese de Doutorado. Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto da Universidade de São Paulo, Ribeirão Preto, Brasil.
  • Gray A, Brodschneider R, Adjlane N, et al (2019): Loss rates of honey bee colonies during winter 2017/18 in 36 countries participating in the COLOSS survey, including effects of forage sources. J Apic Res, 58, 479-485.
  • Gregorc A, Alburaki M, Werle C, et al (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, 821-832.
  • Gregorc A, Poklukar J (2003): Rotenone and oxalic acid as alternative acaricidal treatments for Varroa destructor in honeybee colonies. Vet Parasitol, 111, 351-360.
  • Gregorc A, Sampson B (2019): Diagnosis of Varroa Mite (Varroa destructor) and sustainable control in honey bee (Apis mellifera) colonies—A review. Diversity, 11, 243.
  • Guo L, Fan XY, Qiao X, et al (2021): An octopamine receptor confers selective toxicity of amitraz on honeybees and Varroa mites. eLife, 10, 1-20.
  • Guzman-Novoa, E, Emsen B, Unger P, et al (2012): Genotypic variability and relationships between mite infestation levels, mite damage, grooming intensity, and removal of Varroa destructor mites in selected strains of worker honey bees (Apis mellifera L.). J Invertebr Pathol, 110, 314-320.
  • Haber AI, Steinhauer NA, 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. J Econ Entomol, 112, 1509-1525.
  • Harbo JR, Harris JW (1999): Heritability in honey bees (Hymenoptera: Apidae) of characteristics associated with resistance to Varroa jacobsoni (Mesostigmata: Varroidae). J Econ Entomol, 92, 261-265.
  • Harbo JR, Harris JW (2005): Suppressed mite reproduction explained by the behaviour of adult bees. J Apic Res, 44, 21-23.
  • Harris JW (2007): Bees with varroa sensitive hygiene preferentially remove mite infested pupae aged ≤ five days post capping. J Apic Res, 46, 134-139.
  • Harris JW, Danka RG, Villa JD (2010): Honey bees (Hymenoptera: Apidae) with the trait of varroa sensitive hygiene remove brood with all reproductive stages of varroa mites (Mesostigmata: Varroidae). Ann Entomol Soc Am, 103, 146-152.
  • Harris JW, Danka RG, Villa JD (2012): Changes in infestation, cell cap condition, and reproductive status of Varroa destructor (Mesostigmata: Varroidae) in brood exposed to honey bees with varroa sensitive hygiene. Ann Entomol Soc Am, 105, 512-518.
  • Hernández-Rodríguez CS, Marín Ó, Calatayud F, et al (2021): Large-scale monitoring of resistance to coumaphos, amitraz, and pyrethroids in Varroa destructor. Insects, 12, 1-12.
  • Hossain MM, Richardson JR (2011): Mechanism of pyrethroid pesticide–induced apoptosis: role of Calpain and the ER stress pathway. Toxicol Sci, 122, 512-525.
  • Hubert J, Bicianova M, Ledvinka O, et al (2017): Changes in the bacteriome of honey bees associated with the parasite Varroa destructor, and pathogens Nosema and Lotmaria passim. Microb Ecol, 73, 685-698.
  • Hung ACF, Adams JR, Shimanuki H (1995): Bee parasitic mite syndrome. (II). The role of varroa mite and viruses. Am Bee J, 135, 702-704.
  • Ibrahim A, Reuter GS, Spivak M (2007): Field trial of honey bee colonies bred for mechanisms of resistance against Varroa destructor. Apidologie, 38, 67-76.
  • Ibrahim A, Spivak M (2006): The relationship between hygienic behavior and suppression of mite reproduction as honey bee (Apis mellifera) mechanisms of resistance to Varroa destructor. Apidologie, 37, 31-40.
  • Iglesias A, Mitton G, Szawarski N, et al (2020): Essential oils from Humulus lupulus as novel control agents against Varroa destructor. Ind Crops Prod, 158, 1-7.
  • Jack CJ, van Santen E, Ellis JD (2020): Evaluating the efficacy of oxalic acid vaporization and brood interruption in controlling the honey bee pest Varroa destructor (Acari: Varroidae). J Econ Entomol, 113, 582-588.
  • Jack CJ, Ellis JD (2021). Integrated Pest Management Control of Varroa destructor (Acari: Varroidae), the Most Damaging Pest of (Apis mellifera L.(Hymenoptera: Apidae)) Colonies. J Insect Sci, 21, 1-32.
  • Jeschke P (2016): Propesticides and their use as agrochemicals. Pest Manag Sci, 72, 210-225.
  • Jouzani GS, Valijanian E, Sharafi R (2017): Bacillus thuringiensis: a successful insecticide with new environmental features and tidings. Appl Microbiol Biotechnol, 101, 2691-2711.
  • Kanga LH, Adamczyk J, Marshall K, et al (2010): Monitoring for resistance to organophosphorus and pyrethroid insecticides in Varroa mite populations. J Econ Entomol, 103, 1797-1802.
  • Kita T, Hayashi T, Ohtani T, et al (2017): Amitraz and its metabolite differentially activate α‐and β‐adrenergic‐like octopamine receptors. Pest Manag Sci, 73, 984-990.
  • Le Conte Y, Meixner MD, Brandt A, et al (2020): Geographical distribution and selection of European honey bees resistant to Varroa destructor. Insects, 11, 1-34.
  • Liu F, Xu X, Zhang Y, et al (2020). A Meta-Analysis shows that screen bottom boards can significantly reduce Varroa destructor population. Insects, 11, 1-8.
  • Locke B (2016): Natural varroa mite-surviving Apis mellifera honeybee populations. Apidologie, 47, 467-482.
  • Loucif-Ayad W, Aribi N, Smagghe G, et al (2010): Comparative effectiveness of some acaricides used to control Varroa destructor (Mesostigmata: Varroidae) in Algeria. Afr Entomol, 18, 259-266.
  • Mahmood R, Asad S, Ahmad W, et al (2017): Efficacy of screen bottom board tray with and without soft chemicals for controlling Varroa destructor in honeybee colonies. Pak J Zool, 49, 8-12.
  • Marche MG, Satta A, Floris I, et al (2019): Quantitative variation in the core bacterial community associated with honey bees from Varroa-infested colonies. J Apic Res, 58, 444-454.
  • Martin SJ, Ball BV, Carreck NL (2010): Prevalence and persistence of deformed wing virus (DWV) in untreated or acaricide-treated Varroa destructor infested honey bee (Apis mellifera) colonies. J Apic Res, 49, 72-79.
  • Martin SJ, Hogarth A, van Breda J, et al (1998): A scientific note on Varroa jacobsoni Oudemans and the collapse of Apis mellifera colonies in the United Kingdom. Apidologie, 29, 369-370.
  • Masterman R, Ross R, Mesce K, et al (2001): Olfactory and behavioral response thresholds to odors of diseased brood differ between hygienic and non-hygienic honey bees (Apis mellifera L.). J Comp Physiol A, 187, 441-452.
  • Milani N (1999): The resistance of Varroa jacobsoni Oud. to acaricides. Apidologie, 30, 229-234.
  • Moretto G, Gonçalves LS, De Jong D (1993): Heritability of africanized and European honey bee defensive behavior against the mite Varroa jacobsoni. Brazil J Genetics, 16, 71-77.
  • Mutinelli F, Baggio A (2002): Ipereat and oxalic acid in the control of varroosis. Two years of trials, European Group for Integrated Varroa Control, Bologna.
  • Nanetti A, Büchler R, Charrière JD, et al (2003): Oxalic acid treatments for Varroa control (Review). Apiacta, 38, 81-87.
  • Nazzi F, Brown SP, Annoscia D, et al (2012): Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog, 8, 1-10.
  • Nazzi F, Milani N (1994): A technique for reproduction of Varroa jacobsoni oud under laboratory conditions. Apidologie, 25, 579-584.
  • Neumann P, Carreck NL (2010): Honey bee Colony Losses. J Apic Res, 49, 1-6.
  • Oddie MAY, Dahle B, Neumann P (2017): Norwegian honey bees surviving Varroa destructor mite infestations by means of natural selection.” Peer J, 5, 1-12.
  • Odemer R (2020): Reproductive capacity of Varroa destructor in four different honey bee subspecies.” Saudi J Biol Sci, 27, 247-250.
  • Oldroyd BP (2007): What's Killing American Honey Bees? PLoS Biol, 5, 1195-1199.
  • Papezikova I, Palíková M, Kremserová S, et al (2017): Effect of oxalic acid on the mite Varroa destructor and its host the honey bee Apis mellifera. J Apic Res, 56, 400-408.
  • Pedigo LP, Rice ME (2014): Entomology and pest management. Waveland Press, Inc., Illinois.
  • Pietropaoli M, Formato G (2018): Liquid formic acid 60% to control varroa mites (Varroa destructor) in honey bee colonies (Apis mellifera): protocol evaluation. J Apic Res, 57, 300-307.
  • Rademacher E, Harz M (2006): Oxalic acid for the control of varroosis in honey bee colonies–a review. Apidologie, 37, 98-120.
  • Rinderer TE, Harris JW, Hunt GJ, et al (2010): Breeding for resistance to Varroa destructor in North America. Apidologie, 41, 409-424.
  • Rinkevich FD (2020): Detection of amitraz resistance and reduced treatment efficacy in the Varroa Mite, Varroa destructor, within commercial beekeeping operations. PLoS One, 15, 1-12.
  • Ritter W, De Jong D (1984): Reproduction of Varroa jacobsoni O. in Europe, the Middle East and tropical South America. Z Angew Entomol, 98, 55-57.
  • Roberts JMK, Anderson DL, Durr PA (2017): Absence of deformed wing virus and Varroa destructor in Australia provides unique perspectives on honeybee viral landscapes and colony losses. Sci Rep, 7, 1-11.
  • Rondeau S, Giovenazzo P, Fournier V (2018): Risk assessment and predation potential of Stratiolaelaps scimitus (Acari: Laelapidae) to control Varroa destructor (Acari: Varroidae) in honey bees. PLoS One, 13, 1-18.
  • Rosenkranz P, Aumeier P, Ziegelmann B (2010): Biology and control of Varroa destructor. J Invertebr Pathol, 103, S96-S119.
  • Roth MA, Wilson JM, Tignor KR, et al (2020): Biology and management of Varroa destructor (Mesostigmata: Varroidae) in Apis mellifera (Hymenoptera: Apidae) colonies. J Integr Pest Manag, 11, 1-11.
  • Rothenbuhler WC (1964): Behavior genetics of nest gleaning in honey bees. IV. responses of ft and backcross generations to disease-killed brood. Am Zool, 4, 111-123.
  • Ruijter A (1987): Reproduction of Varroa jacobsoni during successive rood cycles of the honeybee. Apidologie, 18, 321-326.
  • Schmid-Hempel P (1998): Parasites in Social Insects. Princeton University Press, New Jersey.
  • Silva PM, Gauche C, Gonzaga LV, et al (2016): Honey: Chemical composition, stability and authenticity. Food Chem, 196, 309-323.
  • Simmons BI, Balmford A, Bladon AJ, et al (2019): Worldwide insect declines: An important message, but interpret with caution. Ecol Evol, 9, 3678-3680.
  • Smodiš Škerl MI, Nakrst M, Žvokelj L, et al (2011): The acaricidal effect of flumethrin, oxalic acid and amitraz against Varroa destructor in honey bee (Apis mellifera carnica) colonies. Acta Vet Brno, 80, 51-56.
  • Sokół R, Gałęcki R, Michalczyk M (2019): Controlled infestation of honeybee colonies with females. J Apic Sci, 63, 149-155.
  • Spivak M, Boecking O (2001): Honey bee resistance to Varroa Jacobsoni mites. In: Webster TC, Delaplane KS (Eds), Mites of the Honey Bee. Dadant & Sons, Hamilton, Illinois.
  • Spivak M, Masterman R, Ross R, et al (2003): Hygienic behavior in the honey bee (Apis mellifera L.) and the modulatory role of octopamine. J Neurobiol, 55, 341-354.
  • Spivak M, Reuter GS (2001): Varroa destructor infestation in untreated honey bee (Hymenoptera: Apidae) colonies selected for hygienic behavior. J Econ Entomol, 94, 326-331.
  • Strachecka A, Borsuk G, Olszewski K, et al (2015): A new detection method for a newly revealed mechanism of pyrethroid resistance development in Varroa destructor. Parasitol Res, 114, 3999-4004.
  • Tan K, Yang S, Wang Z, et al (2013): Effect of flumethrin on survival and olfactory learning in honeybees. PLoS One, 8, 1-7.
  • Tentcheva D, Gauthier L, Zappulla N, et al (2004): Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl Environ Microbiol, 70, 7185-7191.
  • Tirado R, Simon G, Johnston P (2013): Bees in decline: A review of factors that put pollinators and agriculture in Europe at risk. Greenpeace Research Laboratories Technical Report (Review), 1, 1-48.
  • Toomemaa K, Martin AJ, Williams IH (2010): The effect of different concentrations of oxalic acid in aqueous and sucrose solution on Varroa mites and honey bees. Apidologie, 41, 643-653.
  • Tsagou V, Lianou A, Lazarakis D, et al (2004): Newly isolated bacterial strains belonging to Bacillaceae (Bacillus sp.) and Micrococcaceae accelerate death of the honey bee mite, Varroa destructor (V. jacobsoni), in laboratory assays. Biotechnol Lett, 26, 529-532.
  • Tutun H, Koç N, Kart A (2018): Plant essential oils used against some bee diseases. TURJAF, 6, 34-45.
  • Underwood RM, Currie RW (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). Exp Appl Acarol, 29, 303-313.
  • Underwood RM, Traver BE, López-Uribe MM (2019): Beekeeping management practices are associated with operation size and beekeepers’ philosophy towards in-hive chemicals. Insects, 10, 1-13.
  • van der Steen J, Vejsnæs F (2021): Varroa Control: A Brief Overview of Available Methods. Bee World, 98, 50-56.
  • van Toor RF, Thompson SE, Gibson DM, et al (2015): Ingestion of Varroa destructor by pseudoscorpions in honey bee hives confirmed by PCR analysis. J Apic Res, 54, 555-562.
  • Vlogiannitis S, Mavridis K, Dermauw W, et al (2021): Reduced proinsecticide activation by cytochrome P450 confers coumaphos resistance in the major bee parasite Varroa destructor. PNAS, 118, 1-7.
  • Ward K, Danka R, Ward R (2008): Comparative performance of two mite-resistant stocks of honey bees (Hymenoptera: Apidae) in Alabama beekeeping operations. J Econ Entomol, 101, 654-659.
  • Weygoldt P (1969): Paarungsverhalten und Samenübertragung beim Pseudoskorpion Withius subruber Simon (Cheliferidae). Z Tierpsychol, 26, 230-235.
  • Wilfert L, Long G, Leggett HC, et al (2016): Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science, 351, 594-597.
  • Wilson-Rich N, Spivak M, Fefferman NH, et al (2009): Genetic, individual, and group facilitation of disease resistance in insect societies. Annu Rev Entomol, 54, 405-423.
  • Xie X, Huang ZY, Zeng Z (2016): Why do Varroa mites prefer nurse bees? Sci Rep, 6, 1-6.
  • Yang X, Cox-Foster DL (2005): Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. PNAS, 102, 7470-7475.
  • Žvokelj L, Bakonyi T, Korošec T, et al (2020): Appearance of acute bee paralysis virus, black queen cell virus and deformed wing virus in Carnolian honey bee (Apis mellifera carnica) queen rearing. J Apic Res, 59, 53-58.

Year 2022, Volume: 69 Issue: 2, 229 - 240, 25.03.2022

Ales GREGORC Caio DOMİNGUES Hidayet TUTUN Sedat SEVİN

https://doi.org/10.33988/auvfd.1029296

Abstract

References

  • Akyol E, Yeninar H (2009): Use of oxalic acid to control Varroa destructor in honeybee (Apis mellifera L.) colonies. Turk J Vet Anim Sci, 33, 285-288.
  • Almecija G, Poirot B, Cochard P, et al (2020): Inventory of Varroa destructor susceptibility to amitraz and tau-fluvalinate in France. Exp Appl Acarol, 82, 1-16.
  • Alquisira-Ramírez EV, Paredes-Gonzalez JR, Hernández-Velázquez VM, et al (2014): In vitro susceptibility of Varroa destructor and Apis mellifera to native strains of Bacillus thuringiensis. Apidologie, 45, 707-718.
  • Amrine Jr JW, Noel RC, Webb D (2007): Results of 50% formic acid fumigation of honey bee hives [Apis mellifera ligustica (Hymenoptera: Apidae)] to control varroa mites (Acari: Varroidae) in brood combs in Florida, USA. Int J Acarol, 33, 99-109.
  • Ayan A, Tutun H, Aldemir OS (2019): Control methods against Varroa mites. Int J Adv Stud, 11, 19-23.
  • Aziz ZA, Ahmad A, Setapar SHM, et al (2018): Essential oils: extraction techniques, pharmaceutical and therapeutic potential-a review. Curr Drug Metab, 19, 1100-1110.
  • Beetsma J, Boot WJ, Calis J (1999): Invasion behaviour of Varroa jacobsoni Oud.: from bees into brood cells. Apidologie, 30, 125-140.
  • Berthoud H, Imdorf A, Haueter M, et al (2010): Virus infections and winter losses of honey bee colonies (Apis mellifera). J Apic Res, 49, 60-65.
  • Blenau W, Rademacher E, Baumann A (2012): Plant essential oils and formamidines as insecticides/acaricides: what are the molecular targets? Apidologie, 43, 334-347.
  • Boecking O, Spivak M (1999): Behavioral defenses of honey bees against Varroa jacobsoni Oud. Apidologie, 30, 141-158.
  • Bowen-Walker PL, Gunn A (2001): The effect of the ectoparasitic mite, Varroa destructor on adult workerhoneybee (Apis mellifera) emergence weights, water, protein,carbohydrate, and lipid levels. Entomol Exp Appl, 101, 207-217.
  • Bravo A, Likitvivatanavong S, Gill SS, et al (2011): Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochem Mol Biol, 41, 423-431.
  • Brodschneider R, Gray A, Adjlane N, et al (2018): Multi-country loss rates of honey bee colonies during winter 2016/2017 from the COLOSS survey. J Apic Res, 57, 452-457.
  • Brødsgaard CJ, Ritter W, Hansen H, et al (2000): Interactions among Varroa jacobsoni mites, acute paralysis virus, and Paenibacillus larvae larvae and their influence on mortality of larval honeybees in vitro. Apidologie, 31, 543-554.
  • Büchler R, Drescher W, Tornier I (1992): Grooming behaviour of Apis cerana, Apis mellifera and Apis dorsata and its effect on the parasitic mites Varroa jacobsoni and Tropilaelaps clareae. Exp Appl Acarol, 16, 313-319.
  • Büchler R, Uzunov A, Kovačić M, et al (2020): Summer brood interruption as integrated management strategy for effective Varroa control in Europe. J Apic Res, 59, 764-773.
  • Calderone NW (2005): Evaluation of drone brood removal for management of Varroa destructor (Acari: Varroidae) in colonies of Apis mellifera (Hymenoptera: Apidae) in the northeastern United States. J Econ Entomol, 98, 645-650.
  • Calderone NW, Nasr ME (1999): Evaluation of formic acid formulation for the fall control of Varroa jacobsoni (Acari: Varroidae) in colonies of the honey bee Apis mellifera (Hymenoptera: Apidae) in a temperate climate. J Econ Entomol, 92, 526-533.
  • Cengiz MM (2018): Effectiveness of combining certain biotechnical methods with thymol treatment against Varroa destructor infestation. Afr J Agric Res, 13, 2735-2740.
  • Chandler D, Sunderland KD, Ball BV, et al (2001): Prospective biological control agents of Varroa destructor n. sp., an important pest of the European honeybee, Apis mellifera. Biocontrol Sci Technol, 11, 429-448.
  • Charrière JD, Imdorf A, Bachofen B, et al (2003): The removal of capped drone brood: an effective means of reducing the infestation of varroa in honey bee colonies. Bee World, 84, 117-124.
  • Coffey MF (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. J Apic Res, 46, 213-219.
  • Cremer S, Armitage SAO, Schmid-Hempel P (2007): Social immunity. Curr Biol, 17, 693-702.
  • Cremer S, Sixt M (2009): Analogies in the evolution of individual and social immunity. Philos Trans R Soc Lond B Biol Sci, 364, 129-142.
  • Del Piccolo F, Nazzi F, Della Vedova G, et al (2010): Selection of Apis mellifera workers by the parasitic mite Varroa destructor using host cuticular hydrocarbons. Parasitology, 137, 967-973.
  • Dillon RJ, Dillon VM (2004): The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol, 49, 71-92.
  • Dorland WA (1990): Dorland’s Illustrated Medical Dictionary. W. B. Saunders Company, Philadelphia.
  • Duay P, De Jong D, Engels W (2003): Weight loss in drone pupae (Apis mellifera) multiply infested by Varroa destructor mites. Apidologie, 34, 61-65.
  • Eischen FA (1998): Trials (and tribulations) with formic acid for Varroa control. Am Bee J, 138, 734-735.
  • Ellis AM, Hayes GW, Ellis JD (2009): The efficacy of dusting honey bee colonies with powdered sugar to reduce Varroa mite populations. J Apic Res, 48, 72-76.
  • Fagan LL, Nelson WR, Meenken ED, et al (2012): Varroa management in small bites. J Appl Entomol, 136, 473-475.
  • Fakhimzadeh K, Ellis JD, Hayes JW (2011): Physical control of varroa mites (Varroa destructor): The effects of various dust materials on varroa mite fall from adult honey bees (Apis mellifera) in vitro. J Apic Res, 50, 203-211.
  • Feldlaufer MF, Pettis JS, Kochansky JP, et al (1997): A gel formulation of formic acid for the control of parasitic mites of honey bees. Am Bee J, 137, 661-663.
  • Flint ML (2012): IPM in practice: principles and methods of integrated pest management. University of California Agriculture and Natural Resources, California.
  • Fries I, Camazine S, Sneyd J (1994): Population dynamics of varroa jacobsoni: a model and a review. Bee World, 75, 5-28.
  • Fries I, Imdorf A, Rosenkranz P (2006): Survival of mite infested (Varroa destructor) honey bee (Apis mellifera) colonies in a Nordic climate. Apidologie, 37, 564-570.
  • Fries I, Rosenkranz P (1996): Number of reproductive cycles of Varroa jacobsoni in honey-bee (Apis mellifera) colonies. Exp Appl Acarol, 20, 103-112.
  • Fries I (2001): Is the total amount or the concentration of oxalic acid critical for efficacy in varroa mite control? Report at the IVC meeting in York.
  • Fuchs S (1990): Preference for drone brood cells by Varroa jacobsoni oud in colonies of Apis mellifera carnica. Apidologie, 21, 193-199.
  • Giacomelli A, Pietropaoli M, Carvelli A, et al (2016): Combination of thymol treatment (Apiguard®) and caging the queen technique to fight Varroa destructor. Apidologie, 47, 606-616.
  • Girisgin AO, Ozuicli M, Bah SA, et al (2019): Evaluation of some synthetic acaricides against Varroa destructor (Acari: Varroidae) in Turkey: an indication of resistance or misuse of fumigant amitraz? J Res Vet Med, 38, 67-70.
  • Goulson D, Nicholls E, Botías C, et al (2015): Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347, 1-10.
  • Gramacho KP (1999): Fatores que interferem no comportamento higiênico das abelhas Apis mellifera. Tese de Doutorado. Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto da Universidade de São Paulo, Ribeirão Preto, Brasil.
  • Gray A, Brodschneider R, Adjlane N, et al (2019): Loss rates of honey bee colonies during winter 2017/18 in 36 countries participating in the COLOSS survey, including effects of forage sources. J Apic Res, 58, 479-485.
  • Gregorc A, Alburaki M, Werle C, et al (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, 821-832.
  • Gregorc A, Poklukar J (2003): Rotenone and oxalic acid as alternative acaricidal treatments for Varroa destructor in honeybee colonies. Vet Parasitol, 111, 351-360.
  • Gregorc A, Sampson B (2019): Diagnosis of Varroa Mite (Varroa destructor) and sustainable control in honey bee (Apis mellifera) colonies—A review. Diversity, 11, 243.
  • Guo L, Fan XY, Qiao X, et al (2021): An octopamine receptor confers selective toxicity of amitraz on honeybees and Varroa mites. eLife, 10, 1-20.
  • Guzman-Novoa, E, Emsen B, Unger P, et al (2012): Genotypic variability and relationships between mite infestation levels, mite damage, grooming intensity, and removal of Varroa destructor mites in selected strains of worker honey bees (Apis mellifera L.). J Invertebr Pathol, 110, 314-320.
  • Haber AI, Steinhauer NA, 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. J Econ Entomol, 112, 1509-1525.
  • Harbo JR, Harris JW (1999): Heritability in honey bees (Hymenoptera: Apidae) of characteristics associated with resistance to Varroa jacobsoni (Mesostigmata: Varroidae). J Econ Entomol, 92, 261-265.
  • Harbo JR, Harris JW (2005): Suppressed mite reproduction explained by the behaviour of adult bees. J Apic Res, 44, 21-23.
  • Harris JW (2007): Bees with varroa sensitive hygiene preferentially remove mite infested pupae aged ≤ five days post capping. J Apic Res, 46, 134-139.
  • Harris JW, Danka RG, Villa JD (2010): Honey bees (Hymenoptera: Apidae) with the trait of varroa sensitive hygiene remove brood with all reproductive stages of varroa mites (Mesostigmata: Varroidae). Ann Entomol Soc Am, 103, 146-152.
  • Harris JW, Danka RG, Villa JD (2012): Changes in infestation, cell cap condition, and reproductive status of Varroa destructor (Mesostigmata: Varroidae) in brood exposed to honey bees with varroa sensitive hygiene. Ann Entomol Soc Am, 105, 512-518.
  • Hernández-Rodríguez CS, Marín Ó, Calatayud F, et al (2021): Large-scale monitoring of resistance to coumaphos, amitraz, and pyrethroids in Varroa destructor. Insects, 12, 1-12.
  • Hossain MM, Richardson JR (2011): Mechanism of pyrethroid pesticide–induced apoptosis: role of Calpain and the ER stress pathway. Toxicol Sci, 122, 512-525.
  • Hubert J, Bicianova M, Ledvinka O, et al (2017): Changes in the bacteriome of honey bees associated with the parasite Varroa destructor, and pathogens Nosema and Lotmaria passim. Microb Ecol, 73, 685-698.
  • Hung ACF, Adams JR, Shimanuki H (1995): Bee parasitic mite syndrome. (II). The role of varroa mite and viruses. Am Bee J, 135, 702-704.
  • Ibrahim A, Reuter GS, Spivak M (2007): Field trial of honey bee colonies bred for mechanisms of resistance against Varroa destructor. Apidologie, 38, 67-76.
  • Ibrahim A, Spivak M (2006): The relationship between hygienic behavior and suppression of mite reproduction as honey bee (Apis mellifera) mechanisms of resistance to Varroa destructor. Apidologie, 37, 31-40.
  • Iglesias A, Mitton G, Szawarski N, et al (2020): Essential oils from Humulus lupulus as novel control agents against Varroa destructor. Ind Crops Prod, 158, 1-7.
  • Jack CJ, van Santen E, Ellis JD (2020): Evaluating the efficacy of oxalic acid vaporization and brood interruption in controlling the honey bee pest Varroa destructor (Acari: Varroidae). J Econ Entomol, 113, 582-588.
  • Jack CJ, Ellis JD (2021). Integrated Pest Management Control of Varroa destructor (Acari: Varroidae), the Most Damaging Pest of (Apis mellifera L.(Hymenoptera: Apidae)) Colonies. J Insect Sci, 21, 1-32.
  • Jeschke P (2016): Propesticides and their use as agrochemicals. Pest Manag Sci, 72, 210-225.
  • Jouzani GS, Valijanian E, Sharafi R (2017): Bacillus thuringiensis: a successful insecticide with new environmental features and tidings. Appl Microbiol Biotechnol, 101, 2691-2711.
  • Kanga LH, Adamczyk J, Marshall K, et al (2010): Monitoring for resistance to organophosphorus and pyrethroid insecticides in Varroa mite populations. J Econ Entomol, 103, 1797-1802.
  • Kita T, Hayashi T, Ohtani T, et al (2017): Amitraz and its metabolite differentially activate α‐and β‐adrenergic‐like octopamine receptors. Pest Manag Sci, 73, 984-990.
  • Le Conte Y, Meixner MD, Brandt A, et al (2020): Geographical distribution and selection of European honey bees resistant to Varroa destructor. Insects, 11, 1-34.
  • Liu F, Xu X, Zhang Y, et al (2020). A Meta-Analysis shows that screen bottom boards can significantly reduce Varroa destructor population. Insects, 11, 1-8.
  • Locke B (2016): Natural varroa mite-surviving Apis mellifera honeybee populations. Apidologie, 47, 467-482.
  • Loucif-Ayad W, Aribi N, Smagghe G, et al (2010): Comparative effectiveness of some acaricides used to control Varroa destructor (Mesostigmata: Varroidae) in Algeria. Afr Entomol, 18, 259-266.
  • Mahmood R, Asad S, Ahmad W, et al (2017): Efficacy of screen bottom board tray with and without soft chemicals for controlling Varroa destructor in honeybee colonies. Pak J Zool, 49, 8-12.
  • Marche MG, Satta A, Floris I, et al (2019): Quantitative variation in the core bacterial community associated with honey bees from Varroa-infested colonies. J Apic Res, 58, 444-454.
  • Martin SJ, Ball BV, Carreck NL (2010): Prevalence and persistence of deformed wing virus (DWV) in untreated or acaricide-treated Varroa destructor infested honey bee (Apis mellifera) colonies. J Apic Res, 49, 72-79.
  • Martin SJ, Hogarth A, van Breda J, et al (1998): A scientific note on Varroa jacobsoni Oudemans and the collapse of Apis mellifera colonies in the United Kingdom. Apidologie, 29, 369-370.
  • Masterman R, Ross R, Mesce K, et al (2001): Olfactory and behavioral response thresholds to odors of diseased brood differ between hygienic and non-hygienic honey bees (Apis mellifera L.). J Comp Physiol A, 187, 441-452.
  • Milani N (1999): The resistance of Varroa jacobsoni Oud. to acaricides. Apidologie, 30, 229-234.
  • Moretto G, Gonçalves LS, De Jong D (1993): Heritability of africanized and European honey bee defensive behavior against the mite Varroa jacobsoni. Brazil J Genetics, 16, 71-77.
  • Mutinelli F, Baggio A (2002): Ipereat and oxalic acid in the control of varroosis. Two years of trials, European Group for Integrated Varroa Control, Bologna.
  • Nanetti A, Büchler R, Charrière JD, et al (2003): Oxalic acid treatments for Varroa control (Review). Apiacta, 38, 81-87.
  • Nazzi F, Brown SP, Annoscia D, et al (2012): Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog, 8, 1-10.
  • Nazzi F, Milani N (1994): A technique for reproduction of Varroa jacobsoni oud under laboratory conditions. Apidologie, 25, 579-584.
  • Neumann P, Carreck NL (2010): Honey bee Colony Losses. J Apic Res, 49, 1-6.
  • Oddie MAY, Dahle B, Neumann P (2017): Norwegian honey bees surviving Varroa destructor mite infestations by means of natural selection.” Peer J, 5, 1-12.
  • Odemer R (2020): Reproductive capacity of Varroa destructor in four different honey bee subspecies.” Saudi J Biol Sci, 27, 247-250.
  • Oldroyd BP (2007): What's Killing American Honey Bees? PLoS Biol, 5, 1195-1199.
  • Papezikova I, Palíková M, Kremserová S, et al (2017): Effect of oxalic acid on the mite Varroa destructor and its host the honey bee Apis mellifera. J Apic Res, 56, 400-408.
  • Pedigo LP, Rice ME (2014): Entomology and pest management. Waveland Press, Inc., Illinois.
  • Pietropaoli M, Formato G (2018): Liquid formic acid 60% to control varroa mites (Varroa destructor) in honey bee colonies (Apis mellifera): protocol evaluation. J Apic Res, 57, 300-307.
  • Rademacher E, Harz M (2006): Oxalic acid for the control of varroosis in honey bee colonies–a review. Apidologie, 37, 98-120.
  • Rinderer TE, Harris JW, Hunt GJ, et al (2010): Breeding for resistance to Varroa destructor in North America. Apidologie, 41, 409-424.
  • Rinkevich FD (2020): Detection of amitraz resistance and reduced treatment efficacy in the Varroa Mite, Varroa destructor, within commercial beekeeping operations. PLoS One, 15, 1-12.
  • Ritter W, De Jong D (1984): Reproduction of Varroa jacobsoni O. in Europe, the Middle East and tropical South America. Z Angew Entomol, 98, 55-57.
  • Roberts JMK, Anderson DL, Durr PA (2017): Absence of deformed wing virus and Varroa destructor in Australia provides unique perspectives on honeybee viral landscapes and colony losses. Sci Rep, 7, 1-11.
  • Rondeau S, Giovenazzo P, Fournier V (2018): Risk assessment and predation potential of Stratiolaelaps scimitus (Acari: Laelapidae) to control Varroa destructor (Acari: Varroidae) in honey bees. PLoS One, 13, 1-18.
  • Rosenkranz P, Aumeier P, Ziegelmann B (2010): Biology and control of Varroa destructor. J Invertebr Pathol, 103, S96-S119.
  • Roth MA, Wilson JM, Tignor KR, et al (2020): Biology and management of Varroa destructor (Mesostigmata: Varroidae) in Apis mellifera (Hymenoptera: Apidae) colonies. J Integr Pest Manag, 11, 1-11.
  • Rothenbuhler WC (1964): Behavior genetics of nest gleaning in honey bees. IV. responses of ft and backcross generations to disease-killed brood. Am Zool, 4, 111-123.
  • Ruijter A (1987): Reproduction of Varroa jacobsoni during successive rood cycles of the honeybee. Apidologie, 18, 321-326.
  • Schmid-Hempel P (1998): Parasites in Social Insects. Princeton University Press, New Jersey.
  • Silva PM, Gauche C, Gonzaga LV, et al (2016): Honey: Chemical composition, stability and authenticity. Food Chem, 196, 309-323.
  • Simmons BI, Balmford A, Bladon AJ, et al (2019): Worldwide insect declines: An important message, but interpret with caution. Ecol Evol, 9, 3678-3680.
  • Smodiš Škerl MI, Nakrst M, Žvokelj L, et al (2011): The acaricidal effect of flumethrin, oxalic acid and amitraz against Varroa destructor in honey bee (Apis mellifera carnica) colonies. Acta Vet Brno, 80, 51-56.
  • Sokół R, Gałęcki R, Michalczyk M (2019): Controlled infestation of honeybee colonies with females. J Apic Sci, 63, 149-155.
  • Spivak M, Boecking O (2001): Honey bee resistance to Varroa Jacobsoni mites. In: Webster TC, Delaplane KS (Eds), Mites of the Honey Bee. Dadant & Sons, Hamilton, Illinois.
  • Spivak M, Masterman R, Ross R, et al (2003): Hygienic behavior in the honey bee (Apis mellifera L.) and the modulatory role of octopamine. J Neurobiol, 55, 341-354.
  • Spivak M, Reuter GS (2001): Varroa destructor infestation in untreated honey bee (Hymenoptera: Apidae) colonies selected for hygienic behavior. J Econ Entomol, 94, 326-331.
  • Strachecka A, Borsuk G, Olszewski K, et al (2015): A new detection method for a newly revealed mechanism of pyrethroid resistance development in Varroa destructor. Parasitol Res, 114, 3999-4004.
  • Tan K, Yang S, Wang Z, et al (2013): Effect of flumethrin on survival and olfactory learning in honeybees. PLoS One, 8, 1-7.
  • Tentcheva D, Gauthier L, Zappulla N, et al (2004): Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl Environ Microbiol, 70, 7185-7191.
  • Tirado R, Simon G, Johnston P (2013): Bees in decline: A review of factors that put pollinators and agriculture in Europe at risk. Greenpeace Research Laboratories Technical Report (Review), 1, 1-48.
  • Toomemaa K, Martin AJ, Williams IH (2010): The effect of different concentrations of oxalic acid in aqueous and sucrose solution on Varroa mites and honey bees. Apidologie, 41, 643-653.
  • Tsagou V, Lianou A, Lazarakis D, et al (2004): Newly isolated bacterial strains belonging to Bacillaceae (Bacillus sp.) and Micrococcaceae accelerate death of the honey bee mite, Varroa destructor (V. jacobsoni), in laboratory assays. Biotechnol Lett, 26, 529-532.
  • Tutun H, Koç N, Kart A (2018): Plant essential oils used against some bee diseases. TURJAF, 6, 34-45.
  • Underwood RM, Currie RW (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). Exp Appl Acarol, 29, 303-313.
  • Underwood RM, Traver BE, López-Uribe MM (2019): Beekeeping management practices are associated with operation size and beekeepers’ philosophy towards in-hive chemicals. Insects, 10, 1-13.
  • van der Steen J, Vejsnæs F (2021): Varroa Control: A Brief Overview of Available Methods. Bee World, 98, 50-56.
  • van Toor RF, Thompson SE, Gibson DM, et al (2015): Ingestion of Varroa destructor by pseudoscorpions in honey bee hives confirmed by PCR analysis. J Apic Res, 54, 555-562.
  • Vlogiannitis S, Mavridis K, Dermauw W, et al (2021): Reduced proinsecticide activation by cytochrome P450 confers coumaphos resistance in the major bee parasite Varroa destructor. PNAS, 118, 1-7.
  • Ward K, Danka R, Ward R (2008): Comparative performance of two mite-resistant stocks of honey bees (Hymenoptera: Apidae) in Alabama beekeeping operations. J Econ Entomol, 101, 654-659.
  • Weygoldt P (1969): Paarungsverhalten und Samenübertragung beim Pseudoskorpion Withius subruber Simon (Cheliferidae). Z Tierpsychol, 26, 230-235.
  • Wilfert L, Long G, Leggett HC, et al (2016): Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science, 351, 594-597.
  • Wilson-Rich N, Spivak M, Fefferman NH, et al (2009): Genetic, individual, and group facilitation of disease resistance in insect societies. Annu Rev Entomol, 54, 405-423.
  • Xie X, Huang ZY, Zeng Z (2016): Why do Varroa mites prefer nurse bees? Sci Rep, 6, 1-6.
  • Yang X, Cox-Foster DL (2005): Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. PNAS, 102, 7470-7475.
  • Žvokelj L, Bakonyi T, Korošec T, et al (2020): Appearance of acute bee paralysis virus, black queen cell virus and deformed wing virus in Carnolian honey bee (Apis mellifera carnica) queen rearing. J Apic Res, 59, 53-58.

Details

Primary Language English
Subjects Veterinary Surgery
Journal Section Review
Authors

Ales GREGORC
University of Maribor, Faculty of Agriculture and Life Sciences
0000-0001-7988-6796
Slovenia

Caio DOMİNGUES
University of Maribor, Faculty of Agriculture and Life Sciences
0000-0001-8575-2735
Slovenia

Hidayet TUTUN
BURDUR MEHMET AKİF ERSOY ÜNİVERSİTESİ
0000-0001-9512-8637
Türkiye

Sedat SEVİN
Ankara Üniversitesi Veteriner Fakültesi
0000-0003-0475-9092
Türkiye

Publication Date March 25, 2022
Published in Issue Year 2022Volume: 69 Issue: 2

Cite

Bibtex @review { auvfd1029296, journal = {Ankara Üniversitesi Veteriner Fakültesi Dergisi}, issn = {1300-0861}, eissn = {1308-2817}, address = {}, publisher = {Ankara University}, year = {2022}, volume = {69}, number = {2}, pages = {229 - 240}, doi = {10.33988/auvfd.1029296}, title = {What has been done in the fight against Varroa destructor: from the past to the present}, key = {cite}, author = {Gregorc, Ales and Domingues, Caio and Tutun, Hidayet and Sevin, Sedat} }
APA Gregorc, A. , Domingues, C. , Tutun, H. & Sevin, S. (2022). What has been done in the fight against Varroa destructor: from the past to the present . Ankara Üniversitesi Veteriner Fakültesi Dergisi , 69 (2) , 229-240 . DOI: 10.33988/auvfd.1029296
MLA Gregorc, A. , Domingues, C. , Tutun, H. , Sevin, S. "What has been done in the fight against Varroa destructor: from the past to the present" . Ankara Üniversitesi Veteriner Fakültesi Dergisi 69 (2022 ): 229-240 <http://vetjournal.ankara.edu.tr/en/pub/issue/69048/1029296>
Chicago Gregorc, A. , Domingues, C. , Tutun, H. , Sevin, S. "What has been done in the fight against Varroa destructor: from the past to the present". Ankara Üniversitesi Veteriner Fakültesi Dergisi 69 (2022 ): 229-240
RIS TY - JOUR T1 - What has been done in the fight against Varroa destructor: from the past to the present AU - AlesGregorc, CaioDomingues, HidayetTutun, SedatSevin Y1 - 2022 PY - 2022 N1 - doi: 10.33988/auvfd.1029296 DO - 10.33988/auvfd.1029296 T2 - Ankara Üniversitesi Veteriner Fakültesi Dergisi JF - Journal JO - JOR SP - 229 EP - 240 VL - 69 IS - 2 SN - 1300-0861-1308-2817 M3 - doi: 10.33988/auvfd.1029296 UR - https://doi.org/10.33988/auvfd.1029296 Y2 - 2022 ER -
EndNote %0 Ankara Üniversitesi Veteriner Fakültesi Dergisi What has been done in the fight against Varroa destructor: from the past to the present %A Ales Gregorc , Caio Domingues , Hidayet Tutun , Sedat Sevin %T What has been done in the fight against Varroa destructor: from the past to the present %D 2022 %J Ankara Üniversitesi Veteriner Fakültesi Dergisi %P 1300-0861-1308-2817 %V 69 %N 2 %R doi: 10.33988/auvfd.1029296 %U 10.33988/auvfd.1029296
ISNAD Gregorc, Ales , Domingues, Caio , Tutun, Hidayet , Sevin, Sedat . "What has been done in the fight against Varroa destructor: from the past to the present". Ankara Üniversitesi Veteriner Fakültesi Dergisi 69 / 2 (March 2022): 229-240 . https://doi.org/10.33988/auvfd.1029296
AMA Gregorc A. , Domingues C. , Tutun H. , Sevin S. What has been done in the fight against Varroa destructor: from the past to the present. Ankara Univ Vet Fak Derg. 2022; 69(2): 229-240.
Vancouver Gregorc A. , Domingues C. , Tutun H. , Sevin S. What has been done in the fight against Varroa destructor: from the past to the present. Ankara Üniversitesi Veteriner Fakültesi Dergisi. 2022; 69(2): 229-240.
IEEE A. Gregorc , C. Domingues , H. Tutun and S. Sevin , "What has been done in the fight against Varroa destructor: from the past to the present", Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 69, no. 2, pp. 229-240, Mar. 2022, doi:10.33988/auvfd.1029296
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