[en] The interspecific transmission of pathogens can occur frequently in the environment. Among wild bees, the main spillover cases are caused by pathogens associated with Apis mellifera, whose colonies can act as reservoirs. Due to the limited availability of data in Italy, it is challenging to accurately assess the impact and implications of this phenomenon on the wild bee populations. In this study, a total of 3372 bees were sampled from 11 Italian regions within the BeeNet project, evaluating the prevalence and the abundance of the major honey bee pathogens (DWV, BQCV, ABPV, CBPV, KBV, Nosema ceranae, Ascosphaera apis, Crithidia mellificae, Lotmaria passim, Crithidia bombi). The 68.4% of samples were positive for at least one pathogen. DWV, BQCV, N. ceranae and CBPV showed the highest prevalence and abundance values, confirming them as the most prevalent pathogens spread in the environment. For these pathogens, Andrena, Bombus, Eucera and Seladonia showed the highest mean prevalence and abundance values. Generally, time trends showed a prevalence and abundance decrease from April to July. In order to predict the risk of infection among wild bees, statistical models were developed. A low influence of apiary density on pathogen occurrence was observed, while meteorological conditions and agricultural management showed a greater impact on pathogen persistence in the environment. Social and biological traits of wild bees also contributed to defining a higher risk of infection for bivoltine, communal, mining and oligolectic bees. Out of all the samples tested, 40.5% were co-infected with two or more pathogens. In some cases, individuals were simultaneously infected with up to five different pathogens. It is essential to increase knowledge about the transmission of pathogens among wild bees to understand dynamics, impact and effects on pollinator populations. Implementing concrete plans for the conservation of wild bee species is important to ensure the health of wild and human-managed bees within a One-Health perspective.
Disciplines :
Zoology
Author, co-author :
Tiritelli, Rossella ✱; CREA Research Centre for Agriculture and Environment (CREA-AA), Bologna, Italy ; Life Sciences and Environmental Sustainability, Department of Chemistry, University of Parma, Parma, Italy
Flaminio, Simone ✱; Université de Mons - UMONS > Faculté des Sciences > Service de Zoologie ; CREA Research Centre for Agriculture and Environment (CREA-AA), Bologna, Italy
Zavatta, Laura; CREA Research Centre for Agriculture and Environment (CREA-AA), Bologna, Italy ; Departement of Agriculture and Food Sciences, University of Bologna, Bologna, Italy
Ranalli, Rosa; CREA Research Centre for Agriculture and Environment (CREA-AA), Bologna, Italy ; ZooPlantLab, Department of Biotecnology and Biosciences, University of Milano-Bicocca, Milan, Italy
Giovanetti, Manuela; CREA Research Centre for Agriculture and Environment (CREA-AA), Bologna, Italy
Grasso, Donato; Life Sciences and Environmental Sustainability, Department of Chemistry, University of Parma, Parma, Italy
Leonardi, Stefano; Life Sciences and Environmental Sustainability, Department of Chemistry, University of Parma, Parma, Italy
Bonforte, Marta; Department of Agriculture, Food and Environment, University of Catania, Catania, Italy
Chiara, Benedetta
Boni; Department of Veterinary Sciences, University of Pisa, Pisa, Italy
Cargnus, Elena; CREA Research Centre for Agriculture and Environment (CREA-AA), Bologna, Italy ; Department of Agricultural, Environmental and Animal Sciences, University of Udine, Food, Udine, Italy
Catania, Roberto; Department of Agriculture, Food and Environment, University of Catania, Catania, Italy
Coppola, Francesca; Department of Veterinary Sciences, University of Pisa, Pisa, Italy
Santo, Marco; Maiella National Park, Sulmona, Italy
Pusceddu, Michelina; Department of Agricultural Sciences, University of Sassari, Sassari, Italy ; National Biodiversity Future Center (NBFC), Palermo, Italy
Marino Quaranta; CREA Research Centre for Agriculture and Environment (CREA-AA), Bologna, Italy
Bortolotti, Laura; CREA Research Centre for Agriculture and Environment (CREA-AA), Bologna, Italy
Nanetti, Antonio; CREA Research Centre for Agriculture and Environment (CREA-AA), Bologna, Italy
Cilia, Giovanni; CREA Research Centre for Agriculture and Environment (CREA-AA), Bologna, Italy
M. Drossart M. Gérard Beyond the decline of wild bees: Optimizing conservation measures and bringing together the actors Insects 2020 11 1 23
S.G. Potts et al. Global pollinator declines: Trends, impacts and drivers Trends Ecol. Evol. 2010 25 345 353 20188434
S.G. Potts et al. Safeguarding pollinators and their values to human well-being Nature 2016 540 220 229 2016Natur.540.220P 1:CAS:528:DC%2BC28XhvFGgurjL 27894123
A.M. Klein V. Boreux F. Fornoff A.C. Mupepele G. Pufal Relevance of wild and managed bees for human well-being Curr. Opin. Insect Sci. 2018 26 82 88 29764666
M.A. Aizen L.D. Harder The global stock of domesticated honey bees is growing slower than agricultural demand for pollination Curr. Biol. 2009 19 915 918 1:CAS:528:DC%2BD1MXntVGjurk%3D 19427214
D. Panziera F. Requier P. Chantawannakul C.W.W. Pirk T. Blacquière The diversity decline in wild and managed honey bee populations urges for an integrated conservation approach Front. Ecol. Evol. 2022 10 93
F. Sánchez-Bayo K.A.G. Wyckhuys Worldwide decline of the entomofauna: A review of its drivers Biol. Conserv. 2019 232 8 27
E.E. Zattara M.A. Aizen Worldwide occurrence records suggest a global decline in bee species richness One Earth 2021 4 114 123 2021OEart..4.114Z
L.G. Carvalheiro et al. Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants Ecol. Lett. 2013 16 870 878 23692632 3738924
J.T. Kerr et al. Climate change impacts on bumblebees converge across continents Science (80-) 2015 349 177 180 2015Sci..349.177K 1:CAS:528:DC%2BC2MXhtFWqtr%2FP
I. Bartomeus et al. Historical changes in northeastern US bee pollinators related to shared ecological traits Proc. Natl. Acad. Sci. USA 2013 110 4656 4660 2013PNAS.110.4656B 1:CAS:528:DC%2BC3sXmslCjsr4%3D 23487768 3606985
D.P. Cariveau R. Winfree Causes of variation in wild bee responses to anthropogenic drivers Curr. Opin. Insect. Sci. 2015 1 104 109 10.1016/j.cois.2015.05.004
L.V. Dicks et al. A global-scale expert assessment of drivers and risks associated with pollinator decline Nat. Ecol. Evol. 2021 5 1453 1461 34400826
D. Goulson E. Nicholls C. Botías E.L. Rotheray Bee declines driven by combined Stress from parasites, pesticides, and lack of flowers Science (80-) 2015 347 1255957
R.F.A. Moritz S. Härtel P. Neumann Global invasions of the western honeybee (Apis mellifera) and the consequences for biodiversity Ecoscience 2016 12 289 301
A.J. Vanbergen et al. Threats to an ecosystem service: pressures on pollinators Front. Ecol. Environ. 2013 11 251 259
L.J. Jones R.P. Ford R.J. Schilder M.M. López-Uribe Honey bee viruses are highly prevalent but at low intensities in wild pollinators of cucurbit agroecosystems J. Invertebr. Pathol. 2021 185 1:CAS:528:DC%2BB38XjsVektLc%3D 34560106
A. Nanetti L. Bortolotti G. Cilia Pathogens spillover from honey bees to other arthropods Pathogens 2021 10 1044 1:CAS:528:DC%2BB3MXis1Snur7E 34451508 8400633
M.P. Ocepek I. Toplak U. Zajc D. Bevk The pathogens spillover and incidence correlation in bumblebees and honeybees in Slovenia Pathogens 2021 10 884
N. Piot et al. Honey bees and climate explain viral prevalence in wild bee communities on a continental scale Sci. Rep. 2022 12 1904 2022NatSR.12.1904P 1:CAS:528:DC%2BB38XislKnu7o%3D 35115568 8814194
G. Cilia et al. Occurrence of Honey Bee (Apis mellifera L.) Pathogens in Wild Pollinators in Northern Italy Front. Cell. Infect. Microbiol. 2022 12 7489
Z.A. Pritchard et al. Do viruses from managed honey bees (Hymenoptera: Apidae) endanger wild bees in native prairies? Environ. Entomol. 2021 50 455 466 1:CAS:528:DC%2BB3MXislGlsr%2FF 33492382 8064301
O. Yañez et al. Bee viruses: Routes of infection in hymenoptera Front. Microbiol. 2020 11 943 32547504 7270585
R. Manley M. Boots L. Wilfert Emerging viral disease risk to pollinating insects: Ecological, evolutionary and anthropogenic factors J. Appl. Ecol. 2015 52 331 340 1:CAS:528:DC%2BC2MXpvFahtLc%3D 25954053 4415536
S.A. Alger P.A. Burnham A.K. Brody Flowers as viral hot spots: Honey bees (Apis mellifera) unevenly deposit viruses across plant species PLoS One 2019 14 1:CAS:528:DC%2BC1MXitl2rsbnN 31532764 6750573
P.A. Burnham et al. Flowers as dirty doorknobs: Deformed wing virus transmitted between Apis mellifera and Bombus impatiens through shared flowers J. Appl. Ecol. 2021 58 2065 2074
P. Graystock D. Goulson W.O.H. Hughes Parasites in bloom: Flowers aid dispersal and transmission of pollinator parasites within and between bee species Proc. R. Soc. B Biol. Sci. 2015 282 1371
M. Mazzei et al. Infectivity of DWV associated to flower pollen: Experimental evidence of a horizontal transmission route PLoS One 2014 9 2014PLoSO..9k3448M 25419704 4242645
N. Piot G. Smagghe I. Meeus Network centrality as an indicator for pollinator parasite transmission via flowers Insects 2020 11 872 33302397 7762566
N. Piot et al. More is less: Mass-flowering fruit tree crops dilute parasite transmission between bees Int. J. Parasitol. 2021 51 777 785 33811913
O. Yañez et al. Deformed wing virus and drone mating flights in the honey bee (Apis mellifera): Implications for sexual transmission of a major honey bee virus Apidologie 2012 43 17 30
S. Gisder E. Genersch Viruses of commercialized insect pollinators J. Invertebr. Pathol. 2017 147 51 59 27498219
S. Gisder P. Aumeier E. Genersch Deformed wing virus: Replication and viral load in mites (Varroa destructor) J. Gen. Virol. 2009 90 463 467 1:CAS:528:DC%2BD1MXhslejtLs%3D 19141457
M. Mazzei et al. First detection of replicative deformed wing virus (DWV) in Vespa velutina nigrithorax Bull. Insectology 2018 71 211 216
M. Mazzei et al. Detection of replicative Kashmir Bee Virus and Black Queen Cell Virus in Asian hornet Vespa velutina (Lepelieter 1836) in Italy Sci. Rep. 2019 9 10091 2019NatSR..910091M 31300700 6626046
M. Forzan A. Felicioli S. Sagona P. Bandecchi M. Mazzei Complete genome sequence of deformed wing virus isolated from Vespa crabro in Italy Genome Announc. 2017 5 1
W. Proesmans et al. Pathways for novel epidemiology: Plant–pollinator–pathogen networks and global change Trends Ecol. Evol. 2021 36 623 636 1:CAS:528:DC%2BB38XitVaqs7zK 33865639
L.L. Figueroa et al. Landscape simplification shapes pathogen prevalence in plant-pollinator networks Ecol. Lett. 2020 23 1212 1222 32347001 7340580
H. Cohen et al. Mass-flowering monoculture attracts bees, amplifying parasite prevalence Proc. R. Soc. B 2021 288 1
C.D. Lytle J.-L. Sagripanti Predicted inactivation of viruses of relevance to biodefense by solar radiation J. Virol. 2005 79 14244 14252 1:CAS:528:DC%2BD2MXht1ShsLjL 16254359 1280232
D.J. Pascall M.C. Tinsley B.L. Clark D.J. Obbard L. Wilfert Virus prevalence and genetic diversity across a wild Bumblebee Community Front. Microbiol. 2021 12 856
L.L. Figueroa S. Compton H. Grab S.H.S.S.H. Mcart Functional traits linked to pathogen prevalence in wild bee communities Sci. Rep. 2021 11 7529 2021NatSR.11.7529F 1:CAS:528:DC%2BB3MXosVCisro%3D 33824396 8024325
P. Graystock et al. Dominant bee species and floral abundance drive parasite temporal dynamics in plant-pollinator communities Nat. Ecol. Evol. 2020 4 1358 1367 32690902 7529964
M.S. Pinilla-Gallego et al. Within-colony transmission of microsporidian and trypanosomatid parasites in honey bee and bumble bee colonies Environ. Entomol. 2020 49 1393 1401 1:CAS:528:DC%2BB3MXitFehu7zK 32960211 7734961
Kappeler, P. M., Cremer, S. & Nunn, C. L. (2015) Sociality and health: Impacts of sociality on disease susceptibility and transmission in animal and human societies. Philos. Trans. R. Soc. B Biol. Sci. 370, 20140116.
R.J. Leonard A.N. Harmon-Threatt Methods for rearing ground-nesting bees under laboratory conditions Apidologie 2019 50 689 703 1:CAS:528:DC%2BC1MXhsF2murrE
C.T. Wuellner Nest site preference and success in a gregarious, ground-nesting bee Dieunomia triangulifera Ecol. Entomol. 1999 24 471 479
S.P. Ellner W. Hao Ng C.R. Myers Specialization and multihost epidemics: Disease spread in plant-pollinator networks Am. Nat. 2020 195 E118 E131 32364778
D.J. Becker D.G. Streicker S. Altizer Using host species traits to understand the consequences of resource provisioning for host–parasite interactions J. Anim. Ecol. 2018 87 511 525 29023699
L. Wilfert M.J.F. Brown V. Doublet OneHealth implications of infectious diseases of wild and managed bees J. Invertebr. Pathol. 2021 186 33249062
P. Donkersley L. Ashton G.P.A. Lamarre S. Segar Global insect decline is the result of wilful political failure: A battle plan for entomology Ecol. Evol. 2022 12 9417
E.P.J. Gibbs The evolution of One Health: A decade of progress and challenges for the future Vet. Rec. 2014 174 85 91 24464377
M. Giovanetti L. Bortolotti Report on a project: BeeNet at the start Bull. Insectology 2021 284 1
G. Cilia et al. Nosema ceranae infection in honeybee samples from Tuscanian Archipelago (Central Italy) investigated by two qPCR methods Saudi J. Biol. Sci. 2019 26 1553 1556 1:CAS:528:DC%2BC1cXisVSgt7bK 31762625
A. Nanetti J.D. Ellis I. Cardaio G. Cilia 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 2021 10 372 1:CAS:528:DC%2BB3MXhs1KntL7I 33808848 8003614
A. Nanetti et al. Seed Meals from Brassica nigra and Eruca sativa Control Artificial Nosema ceranae Infections in Apis mellifera Microorganisms 2021 9 949 1:CAS:528:DC%2BB3MXis1Ghs7bF 33924845 8146933
G. Cilia L. Zavatta R. Ranalli A. Nanetti L. Bortolotti Replicative Deformed Wing Virus found in the head of adults from symptomatic commercial bumblebee (Bombus terrestris) colonies Vet. Sci. 2021 8 117 34201628 8310072
G. Cilia et al. A novel TaqMan ® assay for Nosema ceranae quantification in honey bee, based on the protein coding gene Hsp70 Eur. J. Protistol. 2018 63 44 50 29459253
G. Xu et al. Triplex real-time PCR for detection of Crithidia mellificae and Lotmaria passim in honey bees Parasitol. Res. 2018 117 623 628 29282526
P. Chantawannakul L. Ward N. Boonham M. Brown 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. 2006 91 69 73 1:CAS:528:DC%2BD28XkvFal 16376930
R.R. James J.S. Skinner PCR diagnostic methods for Ascosphaera infections in bees J. Invertebr. Pathol. 2005 90 98 103 1:CAS:528:DC%2BD2MXhtFKms7jI 16214164
W.F. Huang K. Skyrm R. Ruiter L. Solter Disease management in commercial bumble bee mass rearing, using production methods, multiplex PCR detection techniques, and regulatory assessment J. Apic. Res. 2015 54 516 524
N. Arismendi A. Bruna N. Zapata M. Vargas PCR-specific detection of recently described Lotmaria passim (Trypanosomatidae) in Chilean apiaries J. Invertebr. Pathol. 2016 134 1 5 1:CAS:528:DC%2BC28XitVOksQ%3D%3D 26721451
G. Cilia I. Cardaio P.E.J. dos Santos J.D. Ellis A. Nanetti The first detection of Nosema ceranae (Microsporidia) in the small hive beetle, Aethina tumida Murray (Coleoptera: Nitidulidae) Apidologie 2018 49 619 624 1:CAS:528:DC%2BC1cXhsFahsbzM
S.S. Greenleaf N.M. Williams R. Winfree C. Kremen Bee foraging ranges and their relationship to body size Oecologia 2007 153 589 596 2007Oecol.153.589G 17483965
Kuhn, M. caret: Classification and Regression Training. (2022).
Fox, J. car: Companion to Applied Regression. (2022).
Wickham, H. dplyr: A Grammar of Data Manipulation. (2023).
Lüdecke, D. sjPlot: Data Visualization for Statistics in Social Science. (2022).
Wickham, H. ggplot2: Elegant Graphics for Data Analysis. ggplot2 (Springer New York, 2009). https://doi.org/10.1007/978-0-387-98141-3.
de Mendiburu, F. agricolae: Statistical Procedures for Agricultural Research. https://cran.r-project.org/web/packages/agricolae/index.html (2021).
Z. Gu L. Gu R. Eils M. Schlesner B. Brors circlize Implements and enhances circular visualization in R Bioinformatics 2014 30 2811 2812 1:CAS:528:DC%2BC28XhtFOrtL7I 24930139
Wright, K. corrgram: plota a Correlogram. https://CRAN.R-project.org/package=corrgram (2021).
Wei, T. & Simko, V. corrplot: Visualization of a Correlation. https://cran.r-project.org/web/packages/corrplot/citation.html (2021).
Kassambara, A. rstatix: Pipe-Friendly Framework for Basic Statistical Tests [R package rstatix version 0.7.2]. https://cran.r-project.org/web/packages/rstatix/index.html (2023).
M. Forzan S. Sagona M. Mazzei A. Felicioli Detection of deformed wing virus in Vespa crabro Bull. Insectol. 2017 70 261 265
K. Power G. Altamura M. Martano P. Maiolino Detection of honeybee viruses in Vespa orientalis Front. Cell. Infect. Microbiol. 2022 12 35601108 9114811
A.G. Dolezal et al. Honey bee viruses in wild bees: Viral prevalence, loads, and experimental inoculation PLoS One 2016 11 27832169 5104440
L. Zhang Y. Deng H. Zhao M. Zhang C. Hou Occurrence and phylogenetic analysis of DWV in Stingless Bee (Apidae sp.) in China: A case report Front. Insect Sci. 2021 1
A. Tehel T. Streicher S. Tragust R.J. Paxton Experimental infection of bumblebees with honeybee-associated viruses: No direct fitness costs but potential future threats to novel wild bee hosts R. Soc. Open Sci. 2020 7 20212255
T. Gómez-Moracho T. Durand C. Pasquaretta P. Heeb M. Lihoreau Artificial diets modulate infection rates by Nosema ceranae in bumblebees Microorganisms 2021 9 158 33445614 7827189
A. Dalmon et al. Possible spillover of pathogens between bee communities foraging on the same floral resource Insects 2021 12 122 33573084 7911050
A.L. Levitt et al. Cross-species transmission of honey bee viruses in associated arthropods Virus Res. 2013 176 232 240 1:CAS:528:DC%2BC3sXhtFCksb7F 23845302
S.J. Martin L.E. Brettell Deformed wing virus in honeybees and other insects Annu. Rev. Virol. 2019 6 49 69 1:CAS:528:DC%2BC1MXhtFGiurzI 31185188
E. Genersch C. Yue I. Fries J.R. de Miranda Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities J. Invertebr. Pathol. 2006 91 61 63 16300785
A. Beaurepaire et al. Diversity and global distribution of viruses of the Western Honey Bee, Apis mellifera Insects 2020 11 239 32290327 7240362
C. Porrini et al. The status of honey bee health in Italy: Results from the nationwide bee monitoring network PLoS One 2016 11 27182604 4868308
I.T. Gajger L. Šimenc I. Toplak The first detection and genetic characterization of four different honeybee viruses in wild bumblebees from Croatia Pathogens 2021 10 808
M.P. Porrini et al. Nosema ceranae in South American native stingless bees and social Wasp Microb. Ecol. 2017 74 761 764 2017MicEc.74.761P 28389730
T. Purkiss L. Lach Pathogen spillover from Apis mellifera to a stingless bee Proc. R. Soc. B Biol. Sci. 2019 286 1
V. Martínez-López et al. Detection of microsporidia in pollinator communities of a mediterranean biodiversity hotspot for wild bees Microb. Ecol. 2021 84 638 642 2022MicEc.84.638M 34585291
G.E. Budge et al. Chronic bee paralysis as a serious emerging threat to honey bees Nat. Commun. 2020 11 1 9 1976CoPhC.11..1B
L. Bailey B.V. Ball J.N. Perry Honeybee paralysis: Its natural spread and its diminished incidence in England and Wales J. Apic. Res. 1983 22 191 195
K.S. Traynor et al. Multiyear survey targeting disease incidence in US honey bees Apidologie 2016 47 325 347
A. Cersini V. Antognetti R. Conti F. Velletrani G. Formato First PCR isolation of Crithidia mellificae (Euglenozoa: Trypanosomatidae) in Apis mellifera (Hymenoptera: Apidae) in Italy Fragm. Entomol. 2015 47 45 49
F. Bordin et al. Presence of Known and Emerging Honey Bee Pathogens in Apiaries of Veneto Region (Northeast of Italy) during Spring 2020 and 2021 Appl. Sci. 2022 12 2134 1:CAS:528:DC%2BB38XltVakt7w%3D
G. Cilia E. Tafi L. Zavatta V. Caringi A. Nanetti The epidemiological situation of the managed honey bee (Apis mellifera) colonies in the Italian Region Emilia-Romagna Vet. Sci. 2022 9 437 36006352 9412502
A. Cersini et al. First isolation of Kashmir bee virus (KBV) in Italy J. Apic. Res. 2013 52 54 55
G. Chen et al. Seasonal variation of viral infections between the eastern honey bee (Apis cerana) and the western honey bee (Apis mellifera) Microbiologyopen 2021 10 33650796 7862873
R. Martín-Hernández et al. Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honeybees (Apis mellifera) Parasitol. Res. 2011 109 605 612 21360094
G. Cilia C. Garrido M. Bonetto D. Tesoriero A. Nanetti Effect of Api-Bioxal ® and ApiHerb ® Treatments against Nosema ceranae Infection in Apis mellifera Investigated by Two qPCR Methods Vet. Sci. 2020 7 125 32899611 7558000
D.P. McMahon et al. A sting in the spit: Widespread cross-infection of multiple RNA viruses across wild and managed bees J. Anim. Ecol. 2015 84 615 624 25646973 4832299
R. Radzevičiūtė et al. Replication of honey bee-associated RNA viruses across multiple bee species in apple orchards of Georgia, Germany and Kyrgyzstan J. Invertebr. Pathol. 2017 146 14 23 28392285
E.A. Murray et al. Viral transmission in honey bees and native bees, supported by a global black queen cell virus phylogeny Environ. Microbiol. 2019 21 972 983 30537211
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 One14, e0217822 (2019).
P. D’Alvise V. Seeburger K. Gihring M. Kieboom M. Hasselmann Seasonal dynamics and co-occurrence patterns of honey bee pathogens revealed by high-throughput RT-qPCR analysis Ecol. Evol. 2019 9 10241 10252 31624548 6787843
F. Mondet et al. Transcriptome profiling of the honeybee parasite Varroa destructor provides new biological insights into the mite adult life cycle BMC Genomics 2018 19 1 19
S. Smoliński A. Langowska A. Glazaczow Raised seasonal temperatures reinforce autumn Varroa destructor infestation in honey bee colonies Sci. Rep. 2021 11 22256 2021NatSR.1122256S 34782664 8593171
B.V. Ball M.F. Allen The prevalence of pathogens in honey bee (Apis mellifera) colonies infested with the parasitic mite Varroa jacobsoni Ann. Appl. Biol. 1988 113 237 244
M.L. Fearon E.A. Tibbetts Pollinator community species richness dilutes prevalence of multiple viruses within multiple host species Ecology 2021 102 33571384
H. Cohen L.C. Ponisio K.A. Russell S.M. Philpott Q.S. McFrederick Floral resources shape parasite and pathogen dynamics in bees facing urbanization Mol. Ecol. 2022 31 2157 2171 35114032
L. Figueroa et al. Bee pathogen transmission dynamics: Deposition, persistence and acquisition on flowers Proc. R. Soc. B 2019 286 20190603 31138075 6545085
M.S. Pinilla-Gallego W.H. Ng V.E. Amaral R.E. Irwin Floral shape predicts bee-parasite transmission potential Ecology 2022 103 35416294
S.V.K. Jagadish et al. Implications of high temperature and elevated CO2on flowering time in plants Front. Plant Sci. 2016 7 913 27446143 4921480
L.S. Dudley M.T.K. Arroyo M.P. Fernández-Murillo Physiological and fitness response of flowers to temperature and water augmentation in a high Andean geophyte Environ. Exp. Bot. 2018 150 1 8
X. Li et al. Tolerance and response of two honeybee species Apis cerana and Apis mellifera to high temperature and relative humidity PLoS One 2019 14 1:CAS:528:DC%2BC1MXhsVOit77M 31170259 6553758
J. Peat D. Goulson Effects of experience and weather on foraging rate and pollen versus nectar collection in the bumblebee, Bombus terrestris Behav. Ecol. Sociobiol. 2005 58 152 156
B. Locke et al. Adapted tolerance to virus infections in four geographically distinct Varroa destructor-resistant honeybee populations Sci. Rep. 2021 11 1 12
D.P. McMahon L. Wilfert R.J. Paxton M.J.F. Brown Emerging viruses in bees: From molecules to ecology Adv. Virus Res. 2018 101 251 291 29908591
N.R. Choi C. Jung D.-W.W. Lee Optimization of detection of black queen cell virus from Bombus terrestris via real-time PCR J. Asia. Pac. Entomol. 2015 18 9 12 1:CAS:528:DC%2BC2cXhvFSht7fN
W. Peng et al. Host range expansion of honey bee Black Queen Cell Virus in the bumble bee Bombus huntii. Apidologie 2011 42 650 658
M. Higes et al. The stability and effectiveness of fumagillin in controlling Nosema ceranae (Microsporidia) infection in honey bees (Apis mellifera) under laboratory and field conditions Apidologie 2011 42 364 377 1:CAS:528:DC%2BC3MXht1GhsbzJ
M. Goblirsch Nosema ceranae disease of the honey bee (Apis mellifera) Apidologie 2018 49 131 150
Fratianni, S. & Acquaotta, F. The Climate of Italy. World Geomorphol. Landscapes 29–38 (2017). https://doi.org/10.1007/978-3-319-26194-2_4/COVER.
L.L. Figueroa C. Grincavitch S.H. McArt Crithidia bombi can infect two solitary bee species while host survivorship depends on diet Parasitology 2021 148 435 442 33256872
Danforth, B. N., Minckley, R. L., Neff, J. L. & Fawcett, F. The Solitary Bees: biology, evolution and conservation. (Princeton University Press, 2019). https://doi.org/10.1515/9780691189321-004/HTML.
S. Cremer S. Armitage P. Schmid-Hempel Social immunity Curr. Biol. 2007 17 R693 R702 1:CAS:528:DC%2BD2sXpt1Knt7w%3D 17714663
Meunier, J. Social immunity and the evolution of group living in insects. Philos. Trans. R. Soc. B Biol. Sci.370, 20140102 (2015).
X. Zhao Y. Liu Current knowledge on bee innate immunity based on genomics and transcriptomics Int. J. Mol. Sci. 2022 23 14278 1:CAS:528:DC%2BB38XjtVahu77N 36430757 9692672
H. Koch P. Schmid-Hempel Socially transmitted gut microbiota protect bumble bees against an intestinal parasite Proc. Natl. Acad. Sci. 2011 108 19288 19292 2011PNAS.10819288K 1:CAS:528:DC%2BC3MXhs1eitLfM 22084077 3228419
L. Straub et al. Do pesticide and pathogen interactions drive wild bee declines? Int. J. Parasitol. Parasites Wildl. 2022 18 232 243 35800107 9253050
A. Harmon-Threatt Influence of nesting characteristics on health of wild bee communities Annu. Rev. Entomol. 2020 65 39 56 1:CAS:528:DC%2BB3cXntFOrtw%3D%3D 31923377
A. Evans J. Llanos W. Kunin S. Evison Indirect effects of agricultural pesticide use on parasite prevalence in wild pollinators Agric. Ecosyst. Environ. 2018 258 40 48
V. Doublet M. Labarussias J.R. de Miranda R.F.A. Moritz R.J. Paxton Bees under stress: Sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle Environ. Microbiol. 2015 17 969 983 1:CAS:528:DC%2BC2MXlvV2ktLo%3D 25611325
D.B. Chagas et al. Black queen cell virus and Nosema ceranae coinfection in Africanized honey bees from southern Brazil Pesqui. Veterinária Bras. 2021 40 892 897
A.M. Gajda E.D. Mazur A.M. Bober M. Czopowicz Nosema Ceranae Interactions with Nosema apis and Black Queen Cell Virus Agriculture 2021 11 963 1:CAS:528:DC%2BB3MXislGjs7rL
Ryba, S., Titera, D., Schodelbauerova-Traxmandlova, I. & Kindlmann, P. Prevalence of honeybee viruses in the Czech Republic and coinfections with other honeybee disease. Biologia (Bratisl).67, 590–595 (2012).
H.Q. Zheng et al. Evidence of the synergistic interaction of honey bee pathogens Nosema ceranae and Deformed wing virus Vet. Microbiol. 2015 177 1 6 25752367
M. Benjeddou N. Leat M. Allsopp S. Davison Detection of acute bee paralysis virus and black queen cell virus from honeybees by reverse transcriptase PCR Appl. Environ. Microbiol. 2001 67 2384 2387 2001ApEnM.67.2384B 1:CAS:528:DC%2BD3MXjtlGmsb0%3D 11319129 92884
X. Zhang et al. New evidence that deformed wing virus and black queen cell virus are multi-host pathogens J. Invertebr. Pathol. 2012 109 156 159 1:STN:280:DC%2BC387gvVGltA%3D%3D 22001629
I. Meeus J.R. de Miranda D.C. de Graaf F. Wäckers G. Smagghe Effect of oral infection with Kashmir bee virus and Israeli acute paralysis virus on bumblebee (Bombus terrestris) reproductive success J. Invertebr. Pathol. 2014 121 64 69 25004171
R. Manley B. Temperton M. Boots L. Wilfert Contrasting impacts of a novel specialist vector on multihost viral pathogen epidemiology in wild and managed bees Mol. Ecol. 2020 29 380 393 1:CAS:528:DC%2BB3cXhvVaktbo%3D 31834965 7003859
H.T. Thu et al. Prevalence of bee viruses among Apis cerana populations in Vietnam J. Apic. Res. 2016 55 379 385
J.M.K.J. Roberts D.D.L. Anderson P.A.P. Durr Absence of deformed wing virus and Varroa destructor in Australia provides unique perspectives on honeybee viral landscapes and colony losses Sci. Rep. 2017 7 6925 2017NatSR..7.6925R 28761114 5537221
