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Opposite seasonal and spatial dynamics of DWV-A and DWV-B suggest distinct transmission pathways in managed honey bees (Apis mellifera L.) colonies

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Abstract

Deformed wing virus (DWV) is a major viral pathogen of Apis mellifera, existing mainly as two genotypes, DWV-A and DWV-B, which differ in transmission dynamics and virulence. This study presents a three-year national molecular surveillance (2021–2023) of Italian honey bee colonies to investigate the spatio-temporal distribution of both variants in relation to apiary density, geographical gradients, and land-use patterns. Quantitative PCR (qPCR) and Bayesian spatio-temporal models were applied to assess viral prevalence and environmental predictors. DWV-B was the dominant variant (overall 73.7%) and displayed a marked autumnal peak in November, followed by a winter decline. In contrast, DWV-A showed a complementary trend, peaking in summer and decreasing with apiary density, suggesting an environmentally mediated transmission pathway. Spatial analysis revealed higher DWV-B prevalence in southern and insular regions, whereas DWV-A predominated in central and northeastern regions. Land-use effects further indicated that DWV-B is linked to anthropogenic landscapes with intensive beekeeping, while DWV-A is associated with more heterogeneous environments. These findings highlight distinct ecological dependencies between DWV variants: DWV-B is probably more Varroa-associated, colony-driven virus favoured by warm, stable climates, while DWV-A reflects diffuse environmental persistence. Integrating climatic and management factors is essential to predict DWV epidemiological shifts under global change.

Data availability

The dataset used in the present study is available from the authors upon request.

References

  1. Martin, S. J. & Brettell, L. E. Deformed Wing Virus in Honeybees and Other Insects. Annu. Rev. Virol. 6, 49–69. https://doi.org/10.1146/annurev-virology-092818-015700 (2019).

    Google Scholar 

  2. Paxton, R. J. et al. Epidemiology of a major honey bee pathogen, deformed wing virus: Potential worldwide replacement of genotype A by genotype B. Int. J. Parasitol. Parasites Wildl. 18, 157–171. https://doi.org/10.1016/J.IJPPAW.2022.04.013 (2022).

    Google Scholar 

  3. de Miranda, J. R. & Genersch, E. Deformed wing virus. J. Invertebr. Pathol. 103, S48–S61. https://doi.org/10.1016/j.jip.2009.06.012 (2010).

    Google Scholar 

  4. Dainat, B., Evans, J. D., Chen, Y. P., Gauthier, L. & Neumanna, P. Dead or alive: Deformed wing virus and varroa destructor reduce the life span of winter honeybees. Appl. Environ. Microbiol. 78, 981–987. https://doi.org/10.1128/AEM.06537-11 (2012).

    Google Scholar 

  5. Nazzi, F. & Le Conte, Y. Ecology of Varroa destructor, the major ectoparasite of the western honey bee, Apis mellifera. Annu. Rev. Entomol. 61, 417–432. https://doi.org/10.1146/ANNUREV-ENTO-010715-023731/CITE/REFWORKS (2016).

    Google Scholar 

  6. Francis, R. M., Nielsen, S. L. & Kryger, P. Varroa-Virus Interaction in Collapsing Honey Bee Colonies. Martin SJ, editor. PlosONE. ;8: e57540. (2013). https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0057540

  7. Natsopoulou, M. E. et al. The virulent, emerging genotype B of deformed wing virus is closely linked to overwinter honeybee worker loss. Sci. Rep. 71, 1–9. https://doi.org/10.1038/s41598-017-05596-3 (2017).

    Google Scholar 

  8. Brettell, L. E. et al. A comparison of deformed wing virus in deformed and asymptomatic honey bees. Insects 8, 28. https://doi.org/10.3390/INSECTS8010028 (2017).

    Google Scholar 

  9. Barroso-Arévalo, S. et al. High load of deformed wing virus and Varroa destructor infestation are related to weakness of honey bee colonies in Southern Spain. Front. Microbiol. 10, 457765. https://doi.org/10.3389/FMICB.2019.01331/BIBTEX (2019).

    Google Scholar 

  10. Nazzi, F., Annoscia, D., Caprio, E., Prisco, G. & Di, Pennacchio, F. Honeybee immunity and colony losses. Entomologia https://doi.org/10.4081/ENTOMOLOGIA.2014.203 (2014).

    Google Scholar 

  11. Lopes, A. R., Low, M., Martín-Hernández, R., de Miranda, J. R. & Pinto, M. A. Varroa destructor shapes the unique viral landscapes of the honey bee populations of the Azores archipelago. PLOS Pathog 20, e1012337. https://doi.org/10.1371/JOURNAL.PPAT.1012337 (2024).

    Google Scholar 

  12. Gisder, S., Aumeier, P. & Genersch, E. Deformed wing virus: Replication and viral load in mites (Varroa destructor). J. Gen. Virol. 90, 463–467 (2009).

    Google Scholar 

  13. Möckel, N., Gisder, S. & Genersch, E. 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/CITE/REFWORKS (2011).

    Google Scholar 

  14. Yañez, O. et al. Bee viruses: Routes of infection in Hymenoptera. Front. Microbiol. 11, 943. https://doi.org/10.3389/fmicb.2020.00943 (2020).

    Google Scholar 

  15. Posada-Florez, F. et al. Pupal cannibalism by worker honey bees contributes to the spread of deformed wing virus. Sci. Rep. 11, 8989. https://doi.org/10.1038/S41598-021-88649-Y (2021).

    Google Scholar 

  16. Mazzei, M. et al. Infectivity of DWV associated to flower pollen: Experimental evidence of a horizontal transmission route. PLoS One 9, e113448. https://doi.org/10.1371/journal.pone.0113448 (2014).

    Google Scholar 

  17. Figueroa, L. et al. Bee pathogen transmission dynamics: Deposition, persistence and acquisition on flowers. Proc. R. Soc. B Biol. Sci. 286, 20190603. https://doi.org/10.1098/RSPB.2019.0603 (2019).

    Google Scholar 

  18. Durrer, S. & Schmid-Hempel, P. Shared use of flowers leads to horizontal pathogen transmission. Proceeding R Soc. B Biol. Sci. 258, 299–302 (1994).

    Google Scholar 

  19. Burnham, P. A. et al. Flowers as dirty doorknobs: Deformed wing virus transmitted between Apis mellifera and Bombus impatiens through shared flowers. J. Appl. Ecol. 58, 2065–2074. https://doi.org/10.1111/1365-2664.13962 (2021).

    Google Scholar 

  20. Alger, S. A., Burnham, P. A. & Brody, A. K. Flowers as viral hot spots: Honey bees (Apis mellifera) unevenly deposit viruses across plant species. PLoS One 14, e0221800. https://doi.org/10.1371/journal.pone.0221800 (2019).

    Google Scholar 

  21. Chen, Y. P., Pettis, J. S., Collins, A. & Feldlaufer, M. F. Prevalence and Transmission of Honeybee Viruses. Appl. Environ. Microbiol. 72, 606–611. https://doi.org/10.1128/AEM.72.1.606-611.2006 (2006).

    Google Scholar 

  22. Amiri, E., Meixner, M. D. & Kryger, P. Deformed wing virus can be transmitted during natural mating in honey bees and infect the queens. Sci. Rep. 2016 61. 6, 1–7. https://doi.org/10.1038/srep33065 (2016).

    Google Scholar 

  23. Grozinger, C. M. & Flenniken, M. L. Bee viruses: Ecology, pathogenicity, and impacts. Annual Review of Entomology https://doi.org/10.1146/annurev-ento-011118-111942 (2019).

    Google Scholar 

  24. Beaurepaire, A. et al. Diversity and Global Distribution of Viruses of the Western Honey Bee, Apis mellifera. Insects. ;11: 239. (2020). http:///pmc/articles/PMC7240362/”/>

  25. Wilfert, L. et al. Honeybee disease: Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science 351, 594–597. https://doi.org/10.1126/SCIENCE.AAC9976 (2016).

    Google Scholar 

  26. Nanetti, A., Bortolotti, L. & Cilia, G. Pathogens Spillover from Honey Bees to Other Arthropods. Pathogens 10, 1044. https://doi.org/10.3390/PATHOGENS10081044 (2021).

    Google Scholar 

  27. Lanzi, G. et al. Molecular and biological characterization of deformed wing virus of honeybees (Apis mellifera L). J. Virol. 80, 4998–5009. https://doi.org/10.1128/JVI.80.10.4998-5009.2006 (2006).

    Google Scholar 

  28. McMahon, D. P. et al. Elevated virulence of an emerging viral genotype as a driver of honeybee loss. Proc. Royal Soc. B: Biolo. Sci. 283, 20160811. https://doi.org/10.1098/rspb.2016.0811 (2016).

    Google Scholar 

  29. Mordecai, G. J., Wilfert, L., Martin, S. J., Jones, I. M. & Schroeder, D. C. Diversity in a honey bee pathogen: first report of a third master variant of the Deformed Wing Virus quasispecies. ISME J. 10, 1264–1273. https://doi.org/10.1038/ismej.2015.178 (2016).

    Google Scholar 

  30. de Miranda, J. R. et al. Cold case: The disappearance of Egypt bee virus, a fourth distinct master strain of deformed wing virus linked to honeybee mortality in 1970’s Egypt. Virol. J. 2022 191. 19, 1–11. https://doi.org/10.1186/S12985-022-01740-2 (2022).

    Google Scholar 

  31. Berényi, O. et al. Phylogenetic analysis of deformed wing virus genotypes from diverse geographic origins indicates recent global distribution of the virus. Appl. Environ. Microbiol. 73, 3605–3611. https://doi.org/10.1128/AEM.00696-07/ASSET/84E1D506-53E5-4E8C-867F-48D8313985A3/ASSETS/GRAPHIC/ZAM0110778260003.JPEG (2007).

    Google Scholar 

  32. Ongus, J. R. et al. Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. J. Gen. Virol. 85, 3747–3755. https://doi.org/10.1099/VIR.0.80470-0/CITE/REFWORKS (2004).

    Google Scholar 

  33. Sircoulomb, F. et al. Genotype B of deformed wing virus and related recombinant viruses become dominant in European honey bee colonies. Sci. Rep. 2025 151. 15, 1–15. https://doi.org/10.1038/s41598-025-86937-5 (2025).

    Google Scholar 

  34. Gisder, S. & Genersch, E. Direct evidence for infection of Varroa destructor mites with the bee-pathogenic deformed wing virus variant B, but not variant A, via fluorescence in situ hybridization analysis. J. Virol. 95, e01786-20. https://doi.org/10.1128/jvi.01786-20 (2021).

    Google Scholar 

  35. Norton, A. M. et al. Adaptation to vector-based transmission in a honeybee virus. J. Anim. Ecol. 90, 2254–2267. https://doi.org/10.1111/1365-2656.13493 (2021).

    Google Scholar 

  36. Wilfert, L. Viral adaptations to vector-borne transmission can result in complex host–vector–pathogen interactions. J. Anim. Ecol. 90, 2230–2233. https://doi.org/10.1111/1365-2656.13570 (2021).

    Google Scholar 

  37. Hesketh-Best, P. J. et al. Dominance of recombinant DWV genomes with changing viral landscapes as revealed in national US honey bee and varroa mite survey. Commun. Biol. 7, 1623. https://doi.org/10.1038/S42003-024-07333-9 (2024).

    Google Scholar 

  38. Cilia, G., Tafi, E., Zavatta, L., Caringi, V. & Nanetti, A. The Epidemiological Situation of the Managed Honey Bee (Apis mellifera) Colonies in the Italian Region Emilia-Romagna. Vet Sci. ;9: 437. (2022). https://www.mdpi.com/2306-7381/9/8/437/htm

  39. Porrini, C. et al. 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 (2016).

    Google Scholar 

  40. Mutinelli, F. et al. Honey bee colony losses in Italy. J. Apic. Res. 49, 119–120. https://doi.org/10.3896/IBRA.1.49.1.24 (2010).

    Google Scholar 

  41. Molinatto, G. et al. Seasonal variations of the five main honey bee viruses in a three-year longitudinal survey. Apidologie 56, 1–20. https://doi.org/10.1007/S13592-025-01147-2/TABLES/4 (2025).

    Google Scholar 

  42. Cilia, G., Caringi, V., Zavatta, L. & Bortolotti, L. Pathogen occurrence in different developmental stages of the invasive Vespa velutina nigrithorax (Buysson, 1905). Pest Manag. Sci. https://doi.org/10.1002/PS.8325 (2024).

    Google Scholar 

  43. Forzan, M., Sagona, S., Mazzei, M. & Felicioli, A. Detection of deformed wing virus in Vespa crabro. Bull. Insectology 70, 261–265 (2017).

    Google Scholar 

  44. Tiritelli, R., Giannetti, D., Schifani, E., Grasso, D. A. & Cilia, G. Neighbors sharing pathogens: the intricate relationship between Apis mellifera and ants (Hymenoptera: Formicidae) nesting in hives. Insect Sci https://doi.org/10.1111/1744-7917.13433 (2024).

    Google Scholar 

  45. Cilia, G. et al. Occurrence of honey bee (Apis mellifera L.) pathogens in wild pollinators in Northern Italy. Front. Cell. Infect. Microbiol. 12, 814. https://doi.org/10.3389/FCIMB.2022.907489 (2022).

    Google Scholar 

  46. Tiritelli, R. et al. Ecological and social factors influence interspecific pathogens occurrence among bees. Sci. Rep. 2024 141. 14, 1–16. https://doi.org/10.1038/s41598-024-55718-x (2024).

    Google Scholar 

  47. Maggio, E. L. et al. First Description of the Occurrence of Slow Bee Paralysis Virus-1 and Deformed Wing Virus B in Apis mellifera ligustica Honeybee in Italy. Applied Sciences 14(2), 626. https://doi.org/10.3390/APP14020626 (2024).

    Google Scholar 

  48. Amšiejūtė-Graziani, P. et al. Molecular Characterization and Phylogenetic Analysis of Honeybee (Apis mellifera) Mite-Borne Pathogen DWV-A and DWV-B Isolated from Lithuania. Microorganisms 12, 1884. https://doi.org/10.3390/MICROORGANISMS12091884/S1 (2024).

    Google Scholar 

  49. Capela, N. & Cilia, G. First detection of genotype B of deformed wing virus (DWV) in mainland Portugal. J. Apic. Res. https://doi.org/10.1080/00218839.2026.2620225 (2026). [cited 11 Mar 2026].

    Google Scholar 

  50. Zioni, N., Soroker, V. & Chejanovsky, N. Replication of Varroa destructor virus 1 (VDV-1) and a Varroa destructor virus 1–deformed wing virus recombinant (VDV-1–DWV) in the head of the honey bee. Virology 417, 106–112. https://doi.org/10.1016/j.virol.2011.05.009 (2011).

    Google Scholar 

  51. Moore, J. et al. Recombinants between Deformed wing virus and Varroa destructor virus-1 may prevail in Varroa destructor-infested honeybee colonies. J. Gen. Virol. 92, 156–161. https://doi.org/10.1099/vir.0.025965-0 (2011).

    Google Scholar 

  52. Dalmon, A. et al. Evidence for positive selection and recombination hotspots in Deformed wing virus (DWV). Sci. Rep. 2017 71. 7, 1–12. https://doi.org/10.1038/srep41045 (2017).

    Google Scholar 

  53. Wang, H. et al. Sequence recombination and conservation of Varroa destructor virus-1 and Deformed Wing Virus in field collected honey bees (Apis mellifera). PLoS One 8, e74508. https://doi.org/10.1371/journal.pone.0074508 (2013).

    Google Scholar 

  54. Cornman, R. S. et al. Population-genomic variation within RNA viruses of the Western honey bee, Apis mellifera, inferred from deep sequencing. BMC Genomics 14154-. https://doi.org/10.1186/1471-2164-14-154 (2013).

    Google Scholar 

  55. Ryabov, E. V. et al. A virulent strain of Deformed Wing Virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission. PLoS Pathog 10, e1004230. https://doi.org/10.1371/journal.ppat.1004230 (2014).

    Google Scholar 

  56. Dubois, E. et al. Outcomes of honeybee pupae inoculated with deformed wing virus genotypes A and B. Apidologie 51, 18–34. https://doi.org/10.1007/s13592-019-00701-z (2019).

    Google Scholar 

  57. Barroso-Arévalo, S., Vicente-Rubiano, M., Molero, F., Puerta, F. & Sánchez-Vizcaíno, J. M. Nucleotide sequence variations may be associated with virulence of deformed wing virus. Apidologie 50, 482–496. https://doi.org/10.1007/S13592-019-00660-5/FIGURES/4 (2019).

    Google Scholar 

  58. Mutinelli, F., Pinto, A., Barzon, L. & Toson, M. Some Considerations about Winter Colony Losses in Italy According to the Coloss Questionnaire. Insects 13, 1059. https://doi.org/10.3390/INSECTS13111059 (2022).

    Google Scholar 

  59. Alger, S. A., Burnham, P. A., Boncristiani, H. F. & Brody, A. K. RNA virus spillover from managed honeybees (Apis mellifera) to wild bumblebees (Bombus spp.). PLoS One 14, e0217822. https://doi.org/10.1371/journal.pone.0217822 (2019).

    Google Scholar 

  60. Molineri, A. et al. 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 (2017).

    Google Scholar 

  61. Dalmon, A., Peruzzi, M., Le Conte, Y., Alaux, C. & Pioz, M. 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 (2019).

    Google Scholar 

  62. Tuerlings, T., Buydens, L., Smagghe, G. & Piot, N. The impact of mass-flowering crops on bee pathogen dynamics. Int. J. Parasitol. Parasites Wildl. 18, 135–147. https://doi.org/10.1016/J.IJPPAW.2022.05.001 (2022).

    Google Scholar 

  63. Saleh, D. S. et al. Deformed wing virus in bee bread: Infectivity and thermal inactivation. J. Apic. Res. (4), https://doi.org/10.1080/00218839.2024.2357448 (2024).

    Google Scholar 

  64. Palmer-Young, E. C. et al. Host-driven temperature dependence of Deformed wing virus infection in honey bee pupae. Commun. Biol. 6(1), 1–7. https://doi.org/10.1038/s42003-023-04704-6 (2023).

    Google Scholar 

  65. Rowland, B. W., Rushton, S. P., Shirley, M. D. F., Brown, M. A. & Budge, G. E. Identifying the climatic drivers of honey bee disease in England and Wales. Sci. Rep. 11, 21953. https://doi.org/10.1038/s41598-021-01495-w (2021).

    Google Scholar 

  66. McAfee, A. et al. Regional patterns and climatic predictors of viruses in honey bee (Apis mellifera) colonies over time. Sci. Rep. 2024 151. 15, 1–21. https://doi.org/10.1038/s41598-024-79675-7 (2025).

    Google Scholar 

  67. Ray, A. M., Davis, S. L., Rasgon, J. L. & Grozinger, C. M. Simulated vector transmission differentially influences dynamics of two viral variants of deformed wing virus in honey bees (Apis mellifera). J. Gen. Virol. 102, 001687. https://doi.org/10.1099/JGV.0.001687/CITE/REFWORKS (2021).

    Google Scholar 

  68. Cilia, G. et al. Presence of Apis mellifera pathogens in different developmental stages of wild Hymenoptera species. Bull. Insectology. 76, 147–154 (2023).

    Google Scholar 

  69. Dalmon, A. et al. Possible spillover of pathogens between bee communities foraging on the same floral resource. Insects 12, 122. https://doi.org/10.3390/insects12020122 (2021).

    Google Scholar 

  70. Tehel, A., Streicher, T., Tragust, S. & Paxton, R. J. Experimental cross species transmission of a major viral pathogen in bees is predominantly from honeybees to bumblebees. Proc. R. Soc. B 289, 20212255. https://doi.org/10.1098/RSPB.2021.2255 (2022).

    Google Scholar 

  71. Doublet, V., Doyle, T. D., Carvell, C., Brown, M. J. F. & Wilfert, L. Host ecology and phylogeny shape the temporal dynamics of social bee viromes. Nat. Commun. 16(1), 1–11. https://doi.org/10.1038/s41467-025-57314-7 (2025).

    Google Scholar 

  72. Giovanetti, M. & Bortolotti, L. Report on a project: Beenet at the start. Bull. Insectol. 74, 284 (2021).

    Google Scholar 

  73. Cilia, G., Tafi, E., Zavatta, L., Dettori, A. & Bortolotti, L. Nanetti · Antonio. Seasonal trends of the ABPV, KBV, and IAPV complex in Italian managed honey bee (Apis mellifera L.) colonies. Arch. Virol. 2024 1693. 169, 1–9. https://doi.org/10.1007/S00705-024-05967-Y (2024).

    Google Scholar 

  74. Tafi, E., Capano, V., Nanetti, A. & Cilia, G. A nationwide molecular survey on Trypanosomatids occurrence in Italian honey bee (Apis mellifera L.) colonies. Vet. Parasitol. Reg. Stud. Rep. 60, 101253. https://doi.org/10.1016/J.VPRSR.2025.101253 (2025).

    Google Scholar 

  75. Zavatta, L. et al. Spatiotemporal evolution of the distribution of Chronic bee paralysis virus (CBPV) in honey bee colonies. Virology 598, 110191. https://doi.org/10.1016/J.VIROL.2024.110191 (2024).

    Google Scholar 

  76. Botías, C. et al. 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 (2012).

    Google Scholar 

  77. Winston, M. The biology of the honey bee (Harvard Univ) (1991).

  78. McMahon, D. P. et al. A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees. J Anim Ecol 84, 615–624. https://doi.org/10.1111/1365-2656.12345 (2015).

    Google Scholar 

  79. De Miranda, J. R. et al. Standard methods for virus research in Apis mellifera. J Apic Res https://doi.org/10.3896/IBRA.1.52.4.22 (2013).

    Google Scholar 

  80. Banerjee, S., Carlin, B. P. & Gelfand, A. E. Hierarchical Modeling and Analysis for Spatial Data. Hierarchical Model Anal Spat Data. [cited 30 Oct 2025]. (2014). https://doi.org/10.1201/B17115

  81. Cecconi, L. et al. Preferential sampling in veterinary parasitological surveillance. Geospat. Health 11, 62–69. https://doi.org/10.4081/GH.2016.412 (2016).

    Google Scholar 

  82. Porrini, C. The death of honey bees and environmental pollution by pesticides: the honey bees as biological indicators. Bulletin of insectology. Bologna: Dept of Agroenvironmental Sciences and Technologies, Bologna University. 147–152. doi:info:doi/ (2003).

  83. Porrini, C., Caprio, E., Tesoriero, D. & Prisco, G. D. Using honey bee as bioindicator of chemicals in Campanian agroecosystems (South Italy). Bull. Insectol. 67, 137–146 (2014).

    Google Scholar 

  84. Resci, I. et al. Predictive statistical models for monitoring antimicrobial resistance spread in the environment using Apis mellifera (L. 1758) colonies. Environ. Res. 248, 118365. https://doi.org/10.1016/J.ENVRES.2024.118365 (2024).

    Google Scholar 

  85. Aitchison, J. The statistical analysis of compositional data. J. R. Stat. Soc. Ser. B 44, 139–177 (1982).

    Google Scholar 

  86. Lunn, D. J., Thomas, A., Best, N. & Spiegelhalter, D. WinBUGS – A Bayesian modelling framework: Concepts, structure, and extensibility. Stat Comput 10, 325–337. https://doi.org/10.1023/A:1008929526011/METRICS (2000).

    Google Scholar 

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Acknowledgements

Data elaboration was supported by techniques acquired during the Master’s program in ’Geostatistics for Human, Animal, and Environmental Health’ offered by the University of Padua.

Author information

Author notes

  1. These authors contributed equally: Rossella Tiritelli and Allegra Sartore.

  2. These authors jointly supervised this work: Antonio Nanetti and Giovanni Cilia.

Authors and Affiliations

  1. CREA Research Centre for Agriculture and Environment, Bologna, Italy

    Rossella Tiritelli, Sergio Albertazzi, Vittorio Capano, Valeria Caringi, Irene Guerra, Elena Tafi, Laura Bortolotti, Antonio Nanetti & Giovanni Cilia

  2. Unit of Biostatistics, Epidemiology and Public Health, Department of Cardiac, Thoracic, Vascular Sciences and Public Health, University of Padua, Padua, Italy

    Rossella Tiritelli, Allegra Sartore & Dolores Catelan

  3. PhD Program in Translational Specialistic Medicine “G.B. Morgagni”, Curriculum “Biostatistics and Clinical Epidemiology”, University of Padua, Padua, Italy

    Allegra Sartore

  4. Department of Agricultural and Food Sciences Alma Mater Studiorum, University of Bologna, Bologna, Italy

    Laura Zavatta

  5. Department of Life Sciences, University of Siena, Siena, Italy

    Elena Tafi

Authors

  1. Rossella Tiritelli
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  2. Allegra Sartore
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  3. Laura Zavatta
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  4. Sergio Albertazzi
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  5. Vittorio Capano
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  6. Valeria Caringi
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  7. Irene Guerra
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  10. Dolores Catelan
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  11. Antonio Nanetti
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  12. Giovanni Cilia
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Conceptualization : Dolores Catelan, Giovanni Cilia, Antonio Nanetti Data Curation : Rossella Tiritelli, Allegra Sartore, Laura Zavatta, Dolores Catelan, Giovanni Cilia Formal Analysis : Rossella Tiritelli, Allegra Sartore, Laura Zavatta, Dolores Catelan, Giovanni Cilia Funding Acquisition : Laura Bortolotti Investigation : Rossella Tiritelli, Sergio Albertazzi, Vittorio Capano, Valeria Caringi, Irene Guerra, Elena Tafi, Laura Bortolotti, Antonio Nanetti, Giovanni Cilia Project Administration : Laura Bortolotti, Antonio Nanetti, Giovanni Cilia Resources : Laura Bortolotti Software : Rossella Tiritelli, Allegra Sartore, Laura Zavatta, Dolores Catelan, Giovanni Cilia Supervision : Dolores Catelan, Giovanni Cilia, Antonio Nanetti Validation : Dolores Catelan, Giovanni Cilia, Laura Bortolotti, Antonio Nanetti Visualization : Rossella Tiritelli, Allegra Sartore, Laura Zavatta, Sergio Albertazzi, Vittorio Capano, Valeria Caringi, Irene Guerra, Elena Tafi, Laura Bortolotti, Dolores Catelan, Antonio Nanetti, Giovanni Cilia Writing—Original Draft Preparation : Rossella Tiritelli, Allegra Sartore, Laura Zavatta, Dolores Catelan, Giovanni Cilia Writing—Review & Editing : Rossella Tiritelli, Allegra Sartore, Laura Zavatta, Sergio Albertazzi, Vittorio Capano, Valeria Caringi, Irene Guerra, Elena Tafi, Laura Bortolotti, Dolores Catelan, Antonio Nanetti, Giovanni Cilia.

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Tiritelli, R., Sartore, A., Zavatta, L. et al. Opposite seasonal and spatial dynamics of DWV-A and DWV-B suggest distinct transmission pathways in managed honey bees (Apis mellifera L.) colonies.
Sci Rep (2026). https://doi.org/10.1038/s41598-026-47121-5

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