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01.03.2024 | Original Article

Seasonal trends of the ABPV, KBV, and IAPV complex in Italian managed honey bee (Apis mellifera L.) colonies

verfasst von: Giovanni Cilia, Elena Tafi, Laura Zavatta, Amanda Dettori, Laura Bortolotti, Antonio Nanetti

Erschienen in: Archives of Virology | Ausgabe 3/2024

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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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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.2009.06.014CrossRefPubMed

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/REFWORKSCrossRefPubMed

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/S11538-017-0281-6MathSciNetCrossRefPubMed

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.2005.07.012CrossRefPubMed

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/REFWORKSCrossRefPubMed

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.70.12.7185-7191.2004ADSCrossRefPubMedPubMedCentral

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.72.1.606-611.2006ADSCrossRefPubMedPubMedCentral

10.

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.2006.03.001CrossRefPubMed

11.

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/2CrossRef

12.

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/V14112442CrossRef

13.

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.1.50.3.03CrossRef

14.

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/10.1080/00218839.1986.11100700CrossRef

15.

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.xCrossRef

16.

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:2001004CrossRef

17.

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.47.1999.3.5CrossRefPubMed

18.

Bailey L, Woods RD (1974) Three previously undescribed viruses from the honey bee. J Gen Virol 25:175–186. https://doi.org/10.1099/0022-1317-25-2-175CrossRefPubMed

19.

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.xCrossRef

20.

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:2007021CrossRef

21.

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/REFWORKSCrossRef

22.

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 86:2281–2289CrossRefPubMed

23.

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.XCrossRefPubMed

24.

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

25.

Genersch E (2010) Honey bee pathology: current threats to honey bees and beekeeping. Appl Microbiol Biotechnol 87:87–97. https://doi.org/10.1007/S00253-010-2573-8CrossRefPubMed

26.

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.2020.24154CrossRef

27.

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.72.4.2414-2420.2006ADSCrossRefPubMedPubMedCentral

28.

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-5CrossRef

29.

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.0219293CrossRef

30.

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/INSECTS12121051CrossRefPubMedPubMedCentral

31.

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.2007.11.002CrossRefPubMed

32.

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.2005.07.001CrossRefPubMed

33.

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.2008.03.014CrossRefPubMed

34.

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/S0718-58392014000200007CrossRef

35.

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.2017.02.019CrossRefPubMed

36.

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/s00265-015-1965-2CrossRef

37.

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-wCrossRef

38.

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-wADSCrossRefPubMedPubMedCentral

39.

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

40.

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.1.52.2.08CrossRef

41.

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.0155411CrossRefPubMedPubMedCentral

42.

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

43.

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 9:437CrossRefPubMedPubMedCentral

44.

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.2020.00943CrossRefPubMedPubMedCentral

45.

Nanetti A, Bortolotti L, Cilia G (2021) Pathogens spillover from honey bees to other arthropods. Pathog 10:1044. https://doi.org/10.3390/PATHOGENS10081044CrossRef

46.

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.2022.907489CrossRef

47.

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.2022.896932CrossRefPubMedPubMedCentral

48.

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/s41598-019-46565-2ADSCrossRefPubMedPubMedCentral

49.

Giovanetti M, Bortolotti L (2021) Report on a project: BeeNet at the start. Bull Insectol 284

50.

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/vetsci7030125CrossRefPubMedPubMedCentral

51.

Winston ML (1991) The biology of the honey bee

52.

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.XCrossRefPubMed

53.

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/pathogens10030372CrossRefPubMedPubMedCentral

54.

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/APP12010422CrossRef

55.

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

56.

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 9:949CrossRefPubMedPubMedCentral

57.

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.2005.11.001CrossRefPubMed

58.

Fox J (2022) car: Companion to applied regression. https://cran.r-project.org/web/packages/car/index.html

59.

Lüdecke D (2022) sjPlot: data visualization for statistics in social science. https://cran.r-project.org/web/packages/sjPlot/index.html

60.

Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New YorkCrossRef

61.

Ogle DH, Doll JC, Wheeler AP, Dinno A (2023) Simple fisheries stock assessment methods. https://cran.r-project.org/web/packages/FSA/index.html

62.

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.2008.07.006CrossRefPubMed

63.

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.2012.03.006CrossRefPubMed

64.

Pohorecka K, Bober A, Skubida M, Zdańska D (2011) Epizootic status of apiaries with massive losses of bee colonies. J Apic Sci 137

65.

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/v6052012CrossRefPubMedPubMedCentral

66.

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.1004261CrossRefPubMedPubMedCentral

67.

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, BostonCrossRef

68.

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/2010014CrossRef

69.

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 45:701–706CrossRef

70.

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

71.

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:2008007CrossRef

72.

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/RISCrossRef

73.

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:2006072CrossRef

74.

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/2017151-9652CrossRef

75.

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/10.1080/00218839.2005.11101164CrossRef

76.

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.2006.11.021CrossRefPubMed

77.

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.0.025940-0CrossRefPubMed

78.

Chen YP, Siede R (2007) Honey bee viruses. Adv Virus Res

79.

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.2018.12.005CrossRefPubMed

80.

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/s41598-022-05603-2ADSCrossRefPubMedPubMedCentral

81.

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/10.1111/1758-2229.12410CrossRefPubMed

82.

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/7ADSCrossRefPubMed

83.

Beaurepaire A, Piot N, Doublet V et al (2020) Diversity and global distribution of viruses of the western honey bee Apis mellifera. Insects 11:239CrossRefPubMedPubMedCentral

84.

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

85.

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-ZCrossRefPubMedPubMedCentral

86.

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

87.

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/10.1080/00218839.1983.11100586CrossRef

88.

Siede R, Büchler R (2004) First detection of Kashmir bee virus in Hesse, Germany. Berl Munch Tierarztl Wochenschr 117:12–15PubMed

89.

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.06094-11ADSCrossRefPubMedPubMedCentral

90.

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.2011.12.011CrossRefPubMed

91.

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/2010017CrossRef

92.

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

93.

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.2022.107788CrossRefPubMed

94.

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.2020.04.004CrossRefPubMed

95.

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/vetsci7030116CrossRefPubMedPubMedCentral

96.

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.0242393CrossRefPubMedPubMedCentral

97.

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.2020.107506CrossRefPubMed

Titel: Seasonal trends of the ABPV, KBV, and IAPV complex in Italian managed honey bee (Apis mellifera L.) colonies
verfasst von: Giovanni Cilia
Elena Tafi
Laura Zavatta
Amanda Dettori
Laura Bortolotti
Antonio Nanetti
Publikationsdatum: 01.03.2024
Verlag: Springer Vienna
Erschienen in: Archives of Virology / Ausgabe 3/2024
Print ISSN: 0304-8608
Elektronische ISSN: 1432-8798
DOI: https://doi.org/10.1007/s00705-024-05967-y

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Weitere Artikel der Ausgabe 3/2024

Characterization of antibodies targeting severe fever with thrombocytopenia syndrome virus glycoprotein Gc

Genomic diversity of group A rotaviruses from wild boars and domestic pigs in Japan: wide prevalence of NSP5 carrying the H2 genotype

Complete genome sequence of a novel partitivirus with a dsRNA3 segment, isolated from Fusarium commune strain CP-SX-3 causing strawberry root rot

Emergence of lumpy skin disease virus (LSDV) infection in domestic Himalayan yaks (Bos grunniens) in Himachal Pradesh, India

Chimeric provirus of bovine leukemia virus/SMAD family member 3 in cattle with enzootic bovine leukosis

Isolation and genome-wide analysis of the novel Acinetobacter baumannii bacteriophage vB_AbaM_AB3P2

Leitlinien kompakt für die Innere Medizin

Neu im Fachgebiet Innere Medizin

Erhebliches Risiko für Kehlkopfkrebs bei mäßiger Dysplasie

Nach Herzinfarkt mit Typ-1-Diabetes schlechtere Karten als mit Typ 2?

15% bedauern gewählte Blasenkrebs-Therapie

Costims – das nächste heiße Ding in der Krebstherapie?

Update Innere Medizin