Abstract
Acute bee paralysis virus (ABPV), Kashmir bee virus (KBV), and Israeli acute paralysis virus (IAPV) usually persist as covert infections in honey bee colonies. They can cause rapid bee mortality in cases of severe infection, often associated with high Varroa destructor infestation, by which they are transmitted. In various countries, these viruses have been associated with colony collapse. Despite their potential danger, these viruses are often disregarded, and little information is available on their occurrence in many countries, including Italy. In 2021, 370 apiaries representing all of the Italian regions were investigated in four different months (June, September, November, and March) for the presence of ABPV, KBV, and IAPV. IAPV was not found in any of the apiaries investigated, whereas 16.45% and 0.67% of the samples tested positive for ABPV and KBV, respectively. Most ABPV cases occurred in late summer-autumn in both northern and southern regions. We observed a scattered pattern of KBV-positive colonies that did not allow any seasonal or regional trends to be discerned. Differences observed among regions and months were potentially related to the dynamics of varroa infestation, viral genetic variations, and different climatic conditions resulting in variations in bee behaviour. This study improves our understanding of the circulation of bee viruses and will contribute to better disease prevention and preservation of bee health.
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Data availability
The dataset supporting the findings of this study is available in the supplementary material (Supplementary Table S1).
References
de Miranda JR, Cordoni G, Budge G (2010) The Acute bee paralysis virus–Kashmir bee virus–Israeli acute paralysis virus complex. J Invertebr Pathol 103:S30–S47. https://doi.org/10.1016/j.jip.2009.06.014
Genersch E, Aubert M (2010) Emerging and re-emerging viruses of the honey bee (Apis mellifera L.). Vet Res 41:54. https://doi.org/10.1051/vetres/2010027
Maori E, Lavi S, Mozes-Koch R et al (2007) Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: Evidence for diversity due to intra- and inter-species recombination. J Gen Virol 88:3428–3438. https://doi.org/10.1099/VIR.0.83284-0/CITE/REFWORKS
Ratti V, Kevan PG, Eberl HJ (2017) A Mathematical model of forager loss in honeybee colonies infested with varroa destructor and the acute bee paralysis virus. Bull Math Biol 79:1218–1253. https://doi.org/10.1007/S11538-017-0281-6
Shen M, Yang X, Cox-Foster D, Cui L (2005) The role of varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees. Virology 342:141–149. https://doi.org/10.1016/j.virol.2005.07.012
Di Prisco G, Pennacchio F, Caprio E et al (2011) Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera. J Gen Virol 92:151–155. https://doi.org/10.1099/VIR.0.023853-0/CITE/REFWORKS
Bailey L, Gibbs AJ (1964) Acute infection of bees with paralysis virus. J Insect Pathol 6:395–407
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. https://doi.org/10.1128/AEM.70.12.7185-7191.2004
Chen YP, Pettis JS, Collins A, Feldlaufer MF (2006) Prevalence and transmission of honeybee viruses. Appl Environ Microbiol 72:606–611. https://doi.org/10.1128/AEM.72.1.606-611.2006
Yue C, Schröder M, Bienefeld K, Genersch E (2006) Detection of viral sequences in semen of honeybees (Apis mellifera): evidence for vertical transmission of viruses through drones. J Invertebr Pathol 92:105–108. https://doi.org/10.1016/J.JIP.2006.03.001
Ravoet J, De Smet L, Wenseleers T, de Graaf DC (2015) Vertical transmission of honey bee viruses in a Belgian queen breeding program. BMC Vet Res 11:1–6. https://doi.org/10.1186/S12917-015-0386-9/FIGURES/2
Bouuaert DC, De SL, Brunain M et al (2022) Virus prevalence in egg samples collected from naturally selected and traditionally managed honey bee colonies across Europe. Viruses 14:2442. https://doi.org/10.3390/V14112442
Nguyen BK, Ribière M, VanEngelsdorp D et al (2015) Effects of honey bee virus prevalence, Varroa destructor load and queen condition on honey bee colony survival over the winter in Belgium. J Apic Res 50:195–202. https://doi.org/10.3896/IBRA.1.50.3.03
Allen MF, Ball BV, White RF, Antoniw JF (1986) The detection of acute paralysis virus in Varroa jacobsoni by the use of a simple indirect ELISA. J Apic Res 25:100–105. https://doi.org/10.1080/00218839.1986.11100700
Ball BV, Allen MF (1988) The prevalence of pathogens in honey bee (Apis mellifera) colonies infested with the parasitic mite Varroa jacobsoni. Ann Appl Biol 113:237–244. https://doi.org/10.1111/j.1744-7348.1988.tb03300.x
Bakonyi T, Farkas R, Szendröi A et al (2002) Detection of acute bee paralysis virus by RT-PCR in honey bee and Varroa destructor field samples: rapid screening of representative Hungarian apiaries. Apidologie 33:63–74. https://doi.org/10.1051/APIDO:2001004
Békési L, Ball BV, Dobos-Kovács M et al (1999) Occurrence of acute paralysis virus of the honey bee (Apis mellifera) in a Hungarian apiary infested with the parasitic mite Varroa jacobsoni. Acta Vet Hung 47:319–324. https://doi.org/10.1556/AVET.47.1999.3.5
Bailey L, Woods RD (1974) Three previously undescribed viruses from the honey bee. J Gen Virol 25:175–186. https://doi.org/10.1099/0022-1317-25-2-175
Allen MF, Ball BV (1995) Characterisation and serological relationships of strains of Kashmir bee virus. Ann Appl Biol 126:471–484. https://doi.org/10.1111/j.1744-7348.1995.tb05382.x
Todd JH, De Miranda JR, Ball BV (2007) Incidence and molecular characterization of viruses found in dying New Zealand honey bee (Apis mellifera ) colonies infested with Varroa destructor. Apidologie 38:354–367. https://doi.org/10.1051/apido:2007021
Bailey L, Carpenter JM, Woods RD (1979) Egypt bee virus and Australian isolates of Kashmir bee virus. J Gen Virol 43:641–647. https://doi.org/10.1099/0022-1317-43-3-641/CITE/REFWORKS
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. J Gen Virol 86:2281–2289
Maori E, Paldi N, Shafir S et al (2009) IAPV, a bee-affecting virus associated with Colony Collapse Disorder can be silenced by dsRNA ingestion. Insect Mol Biol 18:55–60. https://doi.org/10.1111/J.1365-2583.2009.00847.X
Cox-Foster DL, Conlan S, Holmes EC, et al (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science (80- ) 318:283–287. https://doi.org/10.1126/SCIENCE.1146498/SUPPL_FILE/COX-FOSTER_SOM.PDF
Genersch E (2010) Honey bee pathology: current threats to honey bees and beekeeping. Appl Microbiol Biotechnol 87:87–97. https://doi.org/10.1007/S00253-010-2573-8
Kalayci G, Cagirgan AA, Kaplan M et al (2020) The role of viral and parasitic pathogens affected by colony losses in Turkish apiaries. Kafkas Univ Vet Fak Derg 26:671–677. https://doi.org/10.9775/kvfd.2020.24154
Berényi O, Bakonyi T, Derakhshifar I et al (2006) Occurrence of six honeybee viruses in diseased Austrian apiaries. Appl Environ Microbiol 72:2414–2420. https://doi.org/10.1128/AEM.72.4.2414-2420.2006
Cirkovic D, Stevanovic J, Glavinic U et al (2018) Honey bee viruses in Serbian colonies of different strength. PeerJ 2018:e5887. https://doi.org/10.7717/PEERJ.5887/SUPP-5
Morawetz L, Köglberger H, Griesbacher A et al (2019) Health status of honey bee colonies (Apis mellifera) and disease-related risk factors for colony losses in Austria. PLoS One 14:0219293. https://doi.org/10.1371/JOURNAL.PONE.0219293
Mráz P, Hýbl M, Kopecký M et al (2021) Screening of honey bee pathogens in the Czech Republic and their prevalence in various habitats. Insects 12:1051. https://doi.org/10.3390/INSECTS12121051
Forgách P, Bakonyi T, Tapaszti Z et al (2008) Prevalence of pathogenic bee viruses in Hungarian apiaries: situation before joining the European Union. J Invertebr Pathol 98:235–238. https://doi.org/10.1016/J.JIP.2007.11.002
Antúnez K, D’Alessandro B, Corbella E, Zunino P (2005) Detection of Chronic bee paralysis virus and Acute bee paralysis virus in Uruguayan honeybees. J Invertebr Pathol 90:69–72. https://doi.org/10.1016/J.JIP.2005.07.001
Teixeira EW, Chen Y, Message D et al (2008) Virus infections in Brazilian honey bees. J Invertebr Pathol 99:117–119. https://doi.org/10.1016/J.JIP.2008.03.014
Rodríguez M, Vargas M, Antúnez K et al (2014) Prevalence and phylogenetic analysis of honey bee viruses in the Biobío Region of Chile and their association with other honey bee pathogens. Chil J Agric Res 74:170–177. https://doi.org/10.4067/S0718-58392014000200007
Molineri A, Giacobino A, Pacini A et al (2017) Risk factors for the presence of Deformed wing virus and Acute bee paralysis virus under temperate and subtropical climate in Argentinian bee colonies. Prev Vet Med 140:106–115. https://doi.org/10.1016/J.PREVETMED.2017.02.019
Desai SD, Currie RW (2015) Genetic diversity within honey bee colonies affects pathogen load and relative virus levels in honey bees, Apis mellifera L. Behav Ecol Sociobiol 69:1527–1541. https://doi.org/10.1007/s00265-015-1965-2
Lester PJ, Felden A, Baty JW et al (2022) Viral communities in the parasite Varroa destructor and in colonies of their honey bee host (Apis mellifera) in New Zealand. Sci Rep 12:1–13. https://doi.org/10.1038/s41598-022-12888-w
Roberts JMKJ, Anderson DDL, Durr PAP (2017) Absence of deformed wing virus and Varroa destructor in Australia provides unique perspectives on honeybee viral landscapes and colony losses. Sci Rep 7:6925. https://doi.org/10.1038/s41598-017-07290-w
Formato G, Giacomelli A, Olivia M, et al (2015) First detection of Israeli acute paralysis virus (IAPV) in Italy 50:176–177. https://doi.org/10.3896/IBRA.1.50.2.12
Cersini A, Bellucci V, Lucci S et al (2013) First isolation of Kashmir bee virus (KBV) in Italy. J Apic Res 52:54–55. https://doi.org/10.3896/IBRA.1.52.2.08
Porrini C, Mutinelli F, Bortolotti L et al (2016) The status of honey bee health in italy: results from the nationwide bee monitoring network. PLoS One 11:e0155411. https://doi.org/10.1371/journal.pone.0155411
Bordin F, Zulian L, Granato A, et al (2022) Presence of known and emerging honey bee pathogens in apiaries of veneto region (Northeast of Italy) during Spring 2020 and 2021. Appl Sci 12: 2134. https://doi.org/10.3390/APP12042134
Cilia G, Tafi E, Zavatta L et al (2022) The epidemiological situation of the managed honey bee (Apis mellifera) colonies in the Italian Region Emilia-Romagna. Vet Sci 9:437
Yañez O, Piot N, Dalmon A et al (2020) Bee viruses: routes of infection in hymenoptera. Front Microbiol 11:943. https://doi.org/10.3389/fmicb.2020.00943
Nanetti A, Bortolotti L, Cilia G (2021) Pathogens spillover from honey bees to other arthropods. Pathog 10:1044. https://doi.org/10.3390/PATHOGENS10081044
Cilia G, Flaminio S, Zavatta L et al (2022) Occurrence of honey bee (Apis mellifera L.) pathogens in wild pollinators in northern Italy. Front Cell Infect Microbiol 12:7489. https://doi.org/10.3389/FCIMB.2022.907489
Power K, Altamura G, Martano M, Maiolino P (2022) Detection of honeybee viruses in vespa orientalis. Front Cell Infect Microbiol. https://doi.org/10.3389/FCIMB.2022.896932
Mazzei M, Cilia G, Forzan M et al (2019) Detection of replicative Kashmir bee virus and black queen cell virus in asian hornet vespa velutina (Lepelieter 1836) in Italy. Sci Rep 9:10091. https://doi.org/10.1038/s41598-019-46565-2
Giovanetti M, Bortolotti L (2021) Report on a project: BeeNet at the start. Bull Insectol 284
Cilia G, Garrido C, Bonetto M et al (2020) Effect of Api-Bioxal® and ApiHerb® Treatments against Nosema ceranae Infection in Apis mellifera Investigated by Two qPCR Methods. Vet Sci 7:125. https://doi.org/10.3390/vetsci7030125
Winston ML (1991) The biology of the honey bee
Botías C, Martín-Hernández R, Días J et al (2012) The effect of induced queen replacement on Nosema spp. infection in honey bee (Apis mellifera iberiensis) colonies. Environ Microbiol 14:845–859. https://doi.org/10.1111/J.1462-2920.2011.02647.X
Nanetti A, Ellis JD, Cardaio I, Cilia G (2021) Detection of lotmaria passim, crithidia mellificae and replicative forms of deformed wing virus and Kashmir bee virus in the small hive beetle (Aethina tumida). Pathogens 10:372. https://doi.org/10.3390/pathogens10030372
Cilia G, Luchetti G, Nanetti A (2022) Polymorphism of 16s rRNA Gene: any effect on the Biomolecular Quantitation of the Honey Bee (Apis mellifera L., 1758) pathogen nosema ceranae? Appl Sci 12:422. https://doi.org/10.3390/APP12010422
Cilia G, Zavatta L, Ranalli R, et al (2021) Replicative Deformed Wing Virus found in the head of adults from symptomatic commercial bumblebee (Bombus terrestris) colonies. Vet Sci 8:117. https://doi.org/10.3390/vetsci8070117
Nanetti A, Ugolini L, Cilia G et al (2021) Seed meals from Brassica nigra and Eruca sativa control artificial nosema ceranae infections in Apis mellifera. Microorganisms 9:949
Chantawannakul P, Ward L, Boonham N, Brown M (2006) A scientific note on the detection of honeybee viruses using real-time PCR (TaqMan) in Varroa mites collected from a Thai honeybee (Apis mellifera) apiary. J Invertebr Pathol 91:69–73. https://doi.org/10.1016/j.jip.2005.11.001
Fox J (2022) car: Companion to applied regression. https://cran.r-project.org/web/packages/car/index.html
Lüdecke D (2022) sjPlot: data visualization for statistics in social science. https://cran.r-project.org/web/packages/sjPlot/index.html
Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York
Ogle DH, Doll JC, Wheeler AP, Dinno A (2023) Simple fisheries stock assessment methods. https://cran.r-project.org/web/packages/FSA/index.html
Blanchard P, Schurr F, Celle O et al (2008) First detection of Israeli acute paralysis virus (IAPV) in France, a dicistrovirus affecting honeybees (Apis mellifera). J Invertebr Pathol 99:348–350. https://doi.org/10.1016/J.JIP.2008.07.006
Antúnez K, Anido M, Garrido-Bailón E et al (2012) Low prevalence of honeybee viruses in Spain during 2006 and 2007. Res Vet Sci 93:1441–1445. https://doi.org/10.1016/J.RVSC.2012.03.006
Pohorecka K, Bober A, Skubida M, Zdańska D (2011) Epizootic status of apiaries with massive losses of bee colonies. J Apic Sci 137
Hou C, Rivkin H, Slabezki Y, Chejanovsky N (2014) Dynamics of the presence of israeli acute paralysis virus in honey bee colonies with colony collapse disorder. Viruses 6:2012–2027. https://doi.org/10.3390/v6052012
Chen YP, Pettis JS, Corona M et al (2014) Israeli acute paralysis virus: epidemiology, pathogenesis and implications for honey bee health. PLoS Pathog 10:e1004261. https://doi.org/10.1371/journal.ppat.1004261
Foddai D, Bonato L, Pereira LA, Minelli A (2003) Phylogeny and systematics of the Arrupinae (Chilopoda: Geophilomorpha: Mecistocephalidae) with the description of a new dwarfed species. Taylor & Francis Group, Boston
Genersch E, Von Der Ohe W, Kaatz H et al (2010) The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 41:332–352. https://doi.org/10.1051/APIDO/2010014
Tlak Gajger I, Kolodziejek J, Bakonyi T, Nowotny N (2014) Prevalence and distribution patterns of seven different honeybee viruses in diseased colonies: a case study from Croatia. Apidologie 45:701–706
Toplak I, Cerne D, Ciglenecki UJ et al (2012) Detection of six honeybee viruses in clinically affected colonies of carniolan gray bee (Apis mellifera carnica). Slov Vet Res 49:89–96
Nielsen SL, Nicolaisen M, Kryger P (2008) Incidence of acute bee paralysis virus, black queen cell virus, chronic bee paralysis virus, deformed wing virus, Kashmir bee virus and sacbrood virus in honey bees (Apis mellifera) in Denmark. Apidologie 39:310–314. https://doi.org/10.1051/APIDO:2008007
Ryba S, Titera D, Schodelbauerova-Traxmandlova I, Kindlmann P (2012) Prevalence of honeybee viruses in the Czech Republic and coinfections with other honeybee disease. Biologia (Bratisl) 67:590–595. https://doi.org/10.2478/S11756-012-0038-5/MACHINEREADABLECITATION/RIS
Ward L, Waite R, Boonham N et al (2007) First detection of Kashmir bee virus in the UK using real-time PCR. Apidologie 38:181–190. https://doi.org/10.1051/apido:2006072
Meana A, Llorens-Picher M, Euba A et al (2017) Risk factors associated with honey bee colony loss in apiaries in Galicia. NW Spain. Spanish J Agric Res 15:e501. https://doi.org/10.5424/SJAR/2017151-9652
Siede R, Derakhshifar I, Otten C et al (2005) Prevalence of Kashmir bee virus in central Europe. J Apic Res 44:129–129. https://doi.org/10.1080/00218839.2005.11101164
Blanchard P, Ribière M, Celle O et al (2007) Evaluation of a real-time two-step RT-PCR assay for quantitation of Chronic bee paralysis virus (CBPV) genome in experimentally-infected bee tissues and in life stages of a symptomatic colony. J Virol Methods 141:7–13. https://doi.org/10.1016/J.JVIROMET.2006.11.021
Mockel N, Gisder S, Genersch E (2011) Horizontal transmission of deformed wing virus: pathological consequences in adult bees (Apis mellifera) depend on the transmission route. J Gen Virol 92:370–377. https://doi.org/10.1099/vir.0.025940-0
Chen YP, Siede R (2007) Honey bee viruses. Adv Virus Res
Dalmon A, Peruzzi M, Le Conte Y et al (2019) Temperature-driven changes in viral loads in the honey bee Apis mellifera. J Invertebr Pathol 160:87–94. https://doi.org/10.1016/j.jip.2018.12.005
Piot N, Schweiger O, Meeus I et al (2022) Honey bees and climate explain viral prevalence in wild bee communities on a continental scale. Sci Rep 12:1904. https://doi.org/10.1038/s41598-022-05603-2
Giacobino A, Molineri AI, Pacini A et al (2016) Varroa destructor and viruses association in honey bee colonies under different climatic conditions. Environ Microbiol Rep 8:407–412. https://doi.org/10.1111/1758-2229.12410
Antúnez K, Anido M, Branchiccela B et al (2015) Seasonal variation of honeybee pathogens and its association with pollen diversity in uruguay. Microb Ecol 70:522–533. https://doi.org/10.1007/S00248-015-0594-7/FIGURES/7
Beaurepaire A, Piot N, Doublet V et al (2020) Diversity and global distribution of viruses of the western honey bee Apis mellifera. Insects 11:239
Le Conte Y, Navajas M (2008) Climate change: impact on honey bee populations and diseases. OIE Rev Sci Tech 27:485–510. https://doi.org/10.20506/rst.27.2.1819
Ricigliano VA, Mott BM, Floyd AS et al (2018) Honey bees overwintering in a southern climate: longitudinal effects of nutrition and queen age on colony-level molecular physiology and performance. Sci Rep. https://doi.org/10.1038/S41598-018-28732-Z
Lodesani M, Costa C, Besana A, et al (2015) Impact of control strategies for Varroa destructor on colony survival and health in northern and central regions of Italy 53:155–164. https://doi.org/10.3896/IBRA153117
Bailey L, Ball BV, Perry JN (1983) Honeybee paralysis: Its natural spread and its diminished incidence in England and Wales. J Apic Res 22:191–195. https://doi.org/10.1080/00218839.1983.11100586
Siede R, Büchler R (2004) First detection of Kashmir bee virus in Hesse, Germany. Berl Munch Tierarztl Wochenschr 117:12–15
Locke B, Forsgren E, Fries I, de Miranda JR (2012) Acaricide treatment affects viral dynamics in varroa destructor-infested honey bee colonies via both host physiology and mite control. Appl Environ Microbiol 78:227. https://doi.org/10.1128/AEM.06094-11
Boncristiani H, Underwood R, Schwarz R et al (2012) Direct effect of acaricides on pathogen loads and gene expression levels in honey bees Apis mellifera. J Insect Physiol 58:613–620. https://doi.org/10.1016/J.JINSPHYS.2011.12.011
Le Conte Y, Ellis M, Ritter W (2010) Varroa mites and honey bee health: can Varroa explain part of the colony losses? Apidologie 41:353–363. https://doi.org/10.1051/APIDO/2010017
Bellucci V, Lucci S, Bianco P, et al (2019) Monitoring honey bee health in five natural protected areas in Italy. Vet Ital 55:15–25. https://doi.org/10.12834/VETIT.1209.6739.4
Erez T, Bonda E, Kahanov P et al (2022) Multiple benefits of breeding honey bees for hygienic behavior. J Invertebr Pathol 193:107788. https://doi.org/10.1016/J.JIP.2022.107788
Traynor KS, Mondet F, de Miranda JR et al (2020) Varroa destructor: a complex parasite, crippling honey bees worldwide. Trends Parasitol 36:592–606. https://doi.org/10.1016/J.PT.2020.04.004
Mendoza Y, Tomasco IH, Antúnez K et al (2020) Unraveling honey bee-varroa destructor interaction: multiple factors involved in differential resistance between two uruguayan populations. Vet Sci 7:116. https://doi.org/10.3390/vetsci7030116
de Jongh EJ, Harper SL, Yamamoto SS et al (2022) One health, one hive: a scoping review of honey bees, climate change, pollutants, and antimicrobial resistance. PLoS One 17:e0242393. https://doi.org/10.1371/JOURNAL.PONE.0242393
Wilfert L, Brown MJF, Doublet V (2021) OneHealth implications of infectious diseases of wild and managed bees. J Invertebr Pathol 186:107506. https://doi.org/10.1016/J.JIP.2020.107506
Acknowledgements
The authors are grateful to Valeria Caringi, Irene Guerra, Sergio Albertazzi, and Vittorio Capano (CREA Research Centre for Agriculture and Environment) for their effort in the sampling activity.
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This study was supported by the project BeeNet (Italian National Fund under FEASR 2014-2020) from the Italian Ministry of Agriculture and Food Sovereignty and Forestry (MASAF).
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Conceptualization: Giovanni Cilia and Antonio Nanetti. Sampling: Amanda Dettori. Methodology: Giovanni Cilia. Formal analysis: Giovanni Cilia and Elena Tafi. Investigation: Giovanni Cilia, Elena Tafi, and Laura Zavatta. Data analysis: Giovanni Cilia, Elena Tafi, Laura Zavatta, and Antonio Nanetti. Writing – original draft preparation: Giovanni Cilia, Elena Tafi, and Laura Zavatta. Writing – review and editing: Giovanni Cilia, Elena Tafi, Laura Zavatta, Amanda Dettori, Laura Bortolotti, and Antonio Nanetti. Supervision: Antonio Nanetti. Funding acquisition: Laura Bortolotti. All authors have read and agreed to the published version of the manuscript.
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Cilia, G., Tafi, E., Zavatta, L. et al. Seasonal trends of the ABPV, KBV, and IAPV complex in Italian managed honey bee (Apis mellifera L.) colonies. Arch Virol 169, 43 (2024). https://doi.org/10.1007/s00705-024-05967-y
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DOI: https://doi.org/10.1007/s00705-024-05967-y