Urban Green Areas: Examining Honeybee Pathogen Spillover in Wild Bees Through Shared Foraging Niches
Source abstract
Abstract
In urbanized environments, the expansion of urban areas has led to the creation of fragmented green spaces such as gardens and parks. While these areas provide essential habitats for pollinators, they may also inadvertently concentrate specimens of different species, increasing opportunities for pathogen transmission. This study highlights the importance of investigating pathogen dynamics in urban ecosystems, focusing on managed pollinators, such as Apis mellifera Linnaeus, 1758, and their wild counterparts. Over a two-year monitoring period in Milan, Italy, we examined the interactions between pollinator populations in urban green spaces and the spillover of honeybee pathogens. Our findings confirm widespread RNA virus transmission between honeybees and wild pollinators, supporting the previous studies. Notably, the Acute Bee Paralysis Virus (ABPV) exhibited the highest prevalence across both sampling years, underscoring its significant role in pathogen dynamics. These results emphasize the need for regular research to mitigate pathogen spillover risks in urban pollinator communities and inform conservation strategies.
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Research context
OpenAlex topics: Plant and animal studies · Insect and Pesticide Research · Insect and Arachnid Ecology and Behavior
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
Affiliations
Department of Food Environmental and Nutritional Sciences, University of Milan, 20133 Milan, Italy
Department of Biology, University of Federico II of Naples, 80126 Naples, Italy
NBFC—National Biodiversity Future Center, 90133 Palermo, Italy
Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia-Romagna, 25124 Brescia, Italy
CREA Research Centre for Agriculture and Environment (CREA Centro di Ricerca Agricoltura e Ambiente Bologna), 40128 Bologna, Italy
Funding
Cariplo Foundation, Project Api-GIS
References (100+)
Show source-provided references
1. Marsh, W.M. (2005). Landscape Planning: Environmental Applications, Wiley.
2. Biodiversity in urban habitat patches10.1016/j.scitotenv.2005.08.035 ↗
3. Extirpation, colonization, and habitat dynamics of a keystone species along an urban gradient10.1016/j.biocon.2010.05.027 ↗
4. Dispersal by juvenile American crows (Corvus brachyrhynchos) influences population dynamics across a gradient of urbanization10.1093/auk/122.1.205 ↗
5. Giovanetti, M., Giuliani, C., Boff, S., Fico, G., and Lupi, D. (2020). A botanic garden as a tool to combine public perception of nature and life-science investigations on native/exotic plants interactions with local pollinators. PLoS ONE, 15.10.1371/journal.pone.0228965 ↗
6. Seasonal trajectories of plant-pollinator interaction networks differ following phenological mismatches along an urbanization gradient10.1016/j.landurbplan.2022.104512 ↗
7. Can green roofs provide habitat for urban bees (Hymenoptera: Apidae)?10.15365/cate.2142009 ↗
8. Ecology of urban bees: A review of current knowledge and directions for future study10.15365/cate.2132009 ↗
9. Scaling up from gardens: Biodiversity conservation in urban environments10.1016/j.tree.2009.07.016 ↗
10. Landscape and local correlates of bee abundance and species richness in urban gardens10.1093/ee/nvw025 ↗
11. Saving the honeybees in Berlin? A case study of the urban beekeeping boom10.1080/23251042.2015.1008383 ↗
12. Low resource availability drives feeding niche partitioning between wild bees and honeybees in a European city10.1002/eap.2727 ↗
13. Dalmon, A., Diévart, V., Thomasson, M., Fouque, R., Vaissière, B.E., Guilbaud, L., and Henry, M. (2021). Possible spillover of pathogens between bee communities foraging on the same floral resource. Insects, 12.10.3390/insects12020122 ↗
14. Beaurepaire, A., Piot, N., Doublet, V., Antunez, K., Campbell, E., Chantawannakul, P., Chejanovsky, N., Gajda, A., Heerman, M., and Panziera, D. (2020). Diversity and Global Distribution of Viruses of the Western Honey Bee, Apis mellifera. Insects, 11.10.3390/insects11040239 ↗
15. Bacterial pathogens of bees10.1016/j.cois.2018.02.008 ↗
16. Detection of microsporidia in pollinator communities of a mediterranean biodiversity hotspot for wild bees
17. Nanetti, A., Bortolotti, L., and Cilia, G. (2021). Pathogens spillover from honey bees to other arthropods. Pathogens, 10.10.3390/pathogens10081044 ↗
18. Disease associations between honeybees and bumblebees as a threat to wild pollinators10.1038/nature12977 ↗
19. Emerging viral disease risk to pollinating insects: Ecological, evolutionary, and anthropogenic factors
20. Impact of managed honey bee viruses on wild bees10.1016/j.coviro.2016.06.006 ↗
21. Do managed bees drive parasite spread and emergence in wild bees?10.1016/j.ijppaw.2015.10.001 ↗
22. Mallinger, R.E., Gaines-Day, H.R., and Gratton, C. (2017). Do managed bees have negative effects on wild bees?: A systematic review of the literature. PLoS ONE, 12.10.1371/journal.pone.0189268 ↗
23. Detection of Deformed Wing Virus, a Honey Bee Viral Pathogen, in Bumble Bees (Bombus Terrestris and Bombus Pascuorum) with Wing Deformities10.1016/j.jip.2005.10.002 ↗
24. Effect of oral infection with Kashmir bee virus and Israeli acute paralysis virus on bumblebee (Bombus terrestris) reproductive success10.1016/j.jip.2014.06.011 ↗
25. Mazzei, M., Carrozza, M.L., Luisi, E., Forzan, M., Giusti, M., Sagona, S., and Felicioli, A. (2014). Infectivity of DWV associated to flower pollen: Experimental evidence of a horizontal transmission route. PLoS ONE, 9.10.1371/journal.pone.0113448 ↗
26. Deformed wing virus in honeybees and other insects10.1146/annurev-virology-092818-015700 ↗
27. Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera10.1016/j.jip.2007.02.014 ↗
28. Nosema ceranae in South American native stingless bees and social wasp10.1007/s00248-017-0975-1 ↗
29. Purkiss, T., and Lach, L. (2019). Pathogen spillover from Apis mellifera to a stingless bee. Proc. R. Soc. B Biol. Sci., 286.10.1098/rspb.2019.1071 ↗
30. South American native bumblebees (Hymenoptera: Apidae) infected by Nosema ceranae (Microsporidia), an emerging pathogen of honeybees (Apis mellifera)10.1111/j.1758-2229.2009.00018.x ↗
31. Gisder, S., Horchler, L., Pieper, F., Schüler, V., Šima, P., and Genersch, E. (2020). Rapid gastrointestinal passage may protect Bombus terrestris from becoming a true host for Nosema ceranae. Appl. Environ. Microbiol., 86.10.1128/AEM.00629-20 ↗
32. Bramke, K., Müller, U., McMahon, D.P., and Rolff, J. (2019). Exposure of larvae of the solitary bee Osmia bicornis to the honey bee pathogen Nosema ceranae affects life history. Insects, 10.10.3390/insects10110380 ↗
33. Yañez, O., Piot, N., Dalmon, A., de Miranda, J.R., Chantawannakul, P., Panziera, D., Amiri, E., Smagghe, G., Schroeder, D., and Chejanovsky, N. (2020). Bee Viruses: Routes of Infection in Hymenoptera. Front. Microbiol., 11.10.3389/fmicb.2020.00943 ↗
34. Tiritelli, R., Flaminio, S., Zavatta, L., Ranalli, R., Giovanetti, M., Grasso, D.A., Leonardi, S., Bonforte, M., Boni, C.B., and Cargnus, E. (2024). Ecological and social factors influence interspecific pathogens occurrence among bees. Sci. Rep., 14.10.1038/s41598-024-55718-x ↗
35. A scoping review on the effects of Varroa mite (Varroa destructor) on global honey bee decline10.1016/j.scitotenv.2023.167492 ↗
36. Varroa destructor: A complex parasite, crippling honey bees worldwide10.1016/j.pt.2020.04.004 ↗
37. Varroa mites and honey bee health: Can Varroa explain part of the colony losses?10.1051/apido/2010017 ↗
38. Spread of infectious chronic bee paralysis virus by honeybee (Apis mellifera L.) feces10.1128/AEM.01053-07 ↗
39. Dolezal, A.G., Hendrix, S.D., Scavo, N.A., Carrillo-Tripp, J., Harris, M.A., Wheelock, M.J., and Toth, A.L. (2016). Honey bee viruses in wild bees: Viral prevalence, loads, and experimental inoculation. PLoS ONE, 11.10.1371/journal.pone.0166190 ↗
40. Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites10.1126/science.aac9976 ↗
41. The role of varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees10.1016/j.virol.2005.07.012 ↗
42. Singh, R., Levitt, A.L., Rajotte, E.G., Holmes, E.C., Ostiguy, N., van Engelsdorp, D., Lipkin, W.I., de Pamphilis, C.W., Toth, A.L., and Cox-Foster, D.L. (2010). RNA Viruses in Hymenopteran Pollinators: Evidence of Inter-Taxa Virus Transmission via Pollen and Potential Impact on Non-Apis Hymenopteran Species. PLoS ONE, 5.10.1371/journal.pone.0014357 ↗
43. Floral resources shape parasite and pathogen dynamics in bees facing urbanization10.1111/mec.16374 ↗
44. Alger, S.A., Burnham, P.A., Boncristiani, H.F., and Brody, A.K. (2019). RNA virus spillover from managed honeybees (Apis mellifera) to wild bumblebees (Bombus sp.). PLoS ONE, 14.10.1371/journal.pone.0217822 ↗
45. Balkanska, R., Shumkova, R., Atsenova, N., Salkova, D., Dundarova, H., Radoslavov, G., and Hristov, P. (2023). Molecular Detection and Phylogenetic Analysis of Deformed Wing Virus and Sacbrood Virus Isolated from Pollen. Vet. Sci., 10.10.3390/vetsci10020140 ↗
46. Power, K., Altamura, G., Martano, M., and Maiolino, P. (2022). Detection of honeybee viruses in Vespa orientalis. Front. Cell. Infect. Microbiol., 12.10.3389/fcimb.2022.896932 ↗
47. Evison, S.E.F., Roberts, K.E., Laurenson, L., Pietravalle, S., Hui, J., Biesmeijer, J.C., Smith, J.E., Budge, G., and Hughes, W.O.H. (2012). Pervasiveness of parasites in pollinators. PLoS ONE, 7.10.1371/journal.pone.0030641 ↗
48. (2024, December 13). Comune di Milano, 2.21 Contesto Geografico. Available online: https://www.pgt.comune.milano.it/vasraall2-quadro-di-riferimento-territoriale-e-ambientale/2-analisi-dei-fattori-determinanti/22-contesto-urbano-demografico-e-socio-economico/221-contesto-geografico.
49. (2024, December 13). Milano Geoportale. Available online: https://geoportale.comune.milano.it/sit/dettagli/?uuid=C_F205%3ASIT_CENTRALE_M201280017%3A20160427.
50. Connected urban green spaces for pluvial flood risk reduction in the Metropolitan area of Milan10.1016/j.scs.2024.105288 ↗
51. (2024, December 13). Collezione Botanica—Bam. Available online: https://bam.milano.it/collezione-botanica/.
52. Foraging behaviour and pollinating efficiency of Osmia cornuta and Apis mellifera on almond (Hymenoptera, Megachilidae and Apidae)10.1303/aez.29.1 ↗
53. Weather-dependent pollinator activity in an apple orchard, with special reference to Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae and Apidae)10.1603/0046-225X-29.3.413 ↗
54. Population dynamics of Varroa mite and honeybee: Effects of parasitism with age structure and seasonality10.1016/j.ecolmodel.2020.109359 ↗
55. Standard methods for Nosema research10.3896/IBRA.1.52.1.14 ↗
56. Lavazza, A., Botti, G., Milani, N., Gamba, D., Ball, B.V., and Capucci, L. (2003, January 24–29). The identification and characterization of deformed wing virus in Italian Honey bees as a preliminary step for the production of specific reagents and the establishment of diagnostic methods. Proceedings of the Abstracts 38th International Congress of Apimondia, Ljubljana, Slovenia.
57. Seasonal trends of the ABPV, KBV, and IAPV complex in Italian managed honey bee (Apis mellifera L.) colonies10.1007/s00705-024-05967-y ↗
58. Rod-shaped virus-like particles in intestinal contents of three avian species
59. Carpana, E., Vecchi, M.A., Lavazza, A., Bassi, S., and Dottori, M. (1990, January 5–7). Prevalence of acute paralysis virus and other viral infections in honeybees in Italy. Proceedings of the International Symposium on Recent Research on Bee Pathology, Gent, Belgium.
60. The Use of Convalescent Sera in Immune-Electron Microscopy to Detect Non-Suspected/New Viral Agents10.3390/v7052683 ↗
61. Spring mortality in honey bees in northeastern Italy: Detection of pesticides and viruses in dead honey bees and other matrices10.1080/00218839.2017.1304878 ↗
62. 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 colony10.1016/j.jviromet.2006.11.021 ↗
63. Occurrence of six honeybee viruses in diseased Austrian apiaries10.1128/AEM.72.4.2414-2420.2006 ↗
64. The German bee monitoring project: A long term study to understand periodically high winter losses of honey bee colonies10.1051/apido/2010014 ↗
65. Nosema apis infection in worker and queen Apis mellifera10.1051/apido:2003063 ↗
66. Outcome of colonization of Apis mellifera by Nosema ceranae10.1128/AEM.00270-07 ↗
67. RStudio Team (2025, January 10). RStudio: Integrated Development for R. Available online: http://www.rstudio.com/.
68. Introducing the bipartite Package: Analysing Ecological Networks
69. The modularity of pollination networks10.1073/pnas.0706375104 ↗
70. Dormann, C.F. (2025, January 10). Using Bipartite to Describe and Plot Two-Mode Networks in R. Available online: https://cloud.r-project.org/web/packages/bipartite/vignettes/Intro2bipartite.pdf.
71. Co-flowering modularity and floral trait similarity help explain temporal changes in plant–pollinator network structure10.1007/s11258-022-01275-0 ↗
72. The potential for indirect effects between co-flowering plants via shared pollinators depends on resource abundance, accessibility and relatedness10.1111/ele.12342 ↗
73. Zakardjian, M., Geslin, B., Mitran, V., Franquet, E., and Jourdan, H. (2020). Effects of urbanization on plant–pollinator interactions in the tropics: An experimental approach using exotic plants. Insects, 11.10.3390/insects11110773 ↗
74. Seasonal dynamics of competition between honey bees and wild bees in a protected Mediterranean scrubland10.1111/oik.08915 ↗
75. Validation of quantitative real-time RT-PCR assays for the detection of six honeybee viruses10.1016/j.jviromet.2019.04.020 ↗
76. Ayers, A.C., and Rehan, S.M. (2021). Supporting bees in cities: How bees are influenced by local and landscape features. Insects, 12.10.3390/insects12020128 ↗
77. Urbanization as a driver of changes in mutualistic networks between bees and plants10.1007/s11252-024-01639-6 ↗
78. Importance of urban green areas’ connectivity for the conservation of pollinators10.1007/s11252-023-01457-2 ↗
79. The conservation value of urban green space habitats for Australian native bee communities10.1016/j.biocon.2015.05.003 ↗
80. Features of urban green space favourable for large and diverse bee populations (Hymenoptera: Apoidea: Apiformes)10.1016/j.ufug.2016.10.015 ↗
81. Temperature-driven changes in viral loads in the honey bee Apis mellifera10.1016/j.jip.2018.12.005 ↗
82. Chen, G., Wu, Y., Deng, J., Wen, Z., Wang, S., Chen, Y., and Zheng, H. (2021). Seasonal variation of viral infections between the eastern honey bee (Apis cerana) and the western honey bee (Apis mellifera). Microbiologyopen, 10.10.1002/mbo3.1162 ↗
83. Piot, N., Schweiger, O., Meeus, I., Yañez, O., Straub, L., Villamar-Bouza, L., and De Miranda, J.R. (2022). Honey bees and climate explain viral prevalence in wild bee communities on a continental scale. Sci. Rep., 12.10.1038/s41598-022-05603-2 ↗
84. Viruses of commercialized insect pollinators10.1016/j.jip.2016.07.010 ↗
85. A sting in the spit: Widespread cross-infection of multiple RNA viruses across wild and managed bees10.1111/1365-2656.12345 ↗
86. Acute infection of bees with paralysis virus
87. Acute paralysis virus isolates from honeybee colonies infested with Varroa jacobsoni10.1080/00218839.1985.11100658 ↗
88. The acute bee paralysis virus—Kashmir bee virus—Israeli acute paralysis virus complex10.1016/j.jip.2009.06.014 ↗
89. Commercial Bombus impatiens as reservoirs of emerging infectious diseases in central Mexico10.1007/s10530-015-0859-6 ↗
90. First detection of honey bee viruses in stingless bees in North America10.1080/00218839.2015.1100154 ↗
91. Bee pathogens found in Bombus atratus from Colombia: A case study10.1016/j.jip.2015.05.013 ↗
92. Gusachenko, O.N., Woodford, L., Balbirnie-Cumming, K., Kyabov, E.V., and Evans, D.J. (2020). Evidence for and against deformed wing virus spillover from honey bees to bumble bees: A reverse genetic analysis. Sci. Rep., 10.10.1038/s41598-020-73809-3 ↗
93. Cilia, G., Flaminio, S., Zavatta, L., Ranalli, R., Quaranta, M., Bortolotti, L., and Nanetti, A. (2022). Occurrence of honey bee (Apis mellifera L.) pathogens in wild pollinators in northern Italy. Front. Cell. Infect. Microbiol., 12.10.3389/fcimb.2022.907489 ↗
94. Occurrence of deformed wing virus variants in the stingless bee Melipona subnitida and honey bee Apis mellifera populations in Brazil10.1099/jgv.0.001206 ↗
95. Cross-species transmission of honey bee viruses in associated arthropods10.1016/j.virusres.2013.06.013 ↗
96. Host range expansion of honey bee black queen cell virus in the bumble bee, Bombus huntii10.1007/s13592-011-0061-5 ↗
97. Evidence of presence and replication of honey bee viruses among wild bee pollinators in subtropical environments10.1016/j.jip.2019.107256 ↗
98. Two viruses from adult honey bees (Apis mellifera Linnaeus)10.1016/0042-6822(63)90200-9 ↗
99. Chronic bee paralysis virus: A disease and a virus like no other?10.1016/j.jip.2009.06.013 ↗
100. Occurrence and distribution of seven bee viruses in Apis mellifera and Apis cerana in Anhui Province, China