Screening of Honey Bee Pathogens in the Czech Republic and Their Prevalence in Various Habitats
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
PubMed
34940139
PubMed Central
PMC8706798
DOI
10.3390/insects12121051
PII: insects12121051
Knihovny.cz E-zdroje
- Klíčová slova
- Apis mellifera, deformed wing virus, screening, trypanosomatids,
- Publikační typ
- časopisecké články MeSH
Western honey bee (Apis mellifera) is one of the most important pollinators in the world. Thus, a recent honey bee health decline and frequent honey bee mass losses have drawn attention and concern. Honey bee fitness is primarily reduced by pathogens, parasites, and viral load, exposure to pesticides and their residues, and inadequate nutrition from both the quality and amount of food resources. This study evaluated the prevalence of the most common honey bee pathogens and viruses in different habitats across the Czech Republic. The agroecosystems, urban ecosystems, and national park were chosen for sampling from 250 colonies in 50 apiaries. Surprisingly, the most prevalent honey bee pathogens belong to the family Trypanosomatidae including Lotmaria passim and Crithidia mellificae. As expected, the most prevalent viruses were DWV, followed by ABPV. Additionally, the occurrence of DWV-B and DWV-C were correlated with honey bee colony mortality. From the habitat point of view, most pathogens occurred in the town habitat, less in the agroecosystem and least in the national park. The opposite trend was observed in the occurrence of viruses. However, the prevalence of viruses was not affected by habitat.
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Gallai N., Salles J.-M., Settele J., Vaissière B.E. Economic Valuation of the Vulnerability of World Agriculture Confronted with Pollinator Decline. Ecol. Econ. 2009;68:810–821. doi: 10.1016/j.ecolecon.2008.06.014. DOI
Stokstad E. The Case of the Empty Hives. Science. 2007;316:970–972. doi: 10.1126/science.316.5827.970. PubMed DOI
Cox-Foster D.L., Conlan S., Holmes E.C., Palacios G., Evans J.D., Moran N.A., Quan P.-L., Briese T., Hornig M., Geiser D.M. A Metagenomic Survey of Microbes in Honey Bee Colony Collapse Disorder. Science. 2007;318:283–287. doi: 10.1126/science.1146498. PubMed DOI
Higes M., Martín-Hernández R., Garrido-Bailón E., González-Porto A.V., García-Palencia P., Meana A., Del Nozal M.J., Mayo R., Bernal J.L. Honeybee Colony Collapse Due to Nosema ceranae in Professional Apiaries. Environ. Microbiol. Rep. 2009;1:110–113. doi: 10.1111/j.1758-2229.2009.00014.x. PubMed DOI
Alonso-Salces R.M., Cugnata N.M., Guaspari E., Pellegrini M.C., Aubone I., De Piano F.G., Antunez K., Fuselli S.R. Natural Strategies for the Control of Paenibacillus larvae, the Causative Agent of American Foulbrood in Honey Bees: A Review. Apidologie. 2017;48:387–400. doi: 10.1007/s13592-016-0483-1. DOI
Frazier M., Mullin C., Frazier J., Ashcraft S. What Have Pesticides Got to Do with It? Am. Bee J. 2008;148:521–524.
Mutinelli F., Granato A. La Sindrome Del Collasso Della Colonia (Colony Collapse Disorder) Negli USA. Aggiorn. Sulla Situaz. Attuale. Apoidea. 2007;4:175–185.
Sharpe R.J., Heyden L.C. Honey Bee Colony Collapse Disorder Is Possibly Caused by a Dietary Pyrethrum Deficiency. Biosci. Hypotheses. 2009;2:439–440. doi: 10.1016/j.bihy.2009.01.004. DOI
Alaux C., Ducloz F., Crauser D., Le Conte Y. Diet Effects on Honeybee Immunocompetence. Biol. Lett. 2010;6:562–565. doi: 10.1098/rsbl.2009.0986. PubMed DOI PMC
Genersch E., Von Der Ohe W., Kaatz H., Schroeder A., Otten C., Büchler R., Berg S., Ritter W., Mühlen W., Gisder S. The German Bee Monitoring Project: A Long Term Study to Understand Periodically High Winter Losses of Honey Bee Colonies. Apidologie. 2010;41:332–352. doi: 10.1051/apido/2010014. DOI
Lanzi G., De Miranda J.R., Boniotti M.B., Cameron C.E., Lavazza A., Capucci L., Camazine S.M., Rossi C. Molecular and Biological Characterization of Deformed Wing Virus of Honeybees (Apis mellifera L.) J. Virol. 2006;80:4998–5009. doi: 10.1128/JVI.80.10.4998-5009.2006. PubMed DOI PMC
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. 2016;10:1264–1273. doi: 10.1038/ismej.2015.178. PubMed DOI PMC
Dainat B., Evans J.D., Chen Y.P., Gauthier L., Neumann P. Dead or Alive: Deformed Wing Virus and Varroa destructor Reduce the Life Span of Winter Honeybees. Appl. Environ. Microbiol. 2012;78:981–987. doi: 10.1128/AEM.06537-11. PubMed DOI PMC
Martin S.J., Highfield A.C., Brettell L., Villalobos E.M., Budge G.E., Powell M., Nikaido S., Schroeder D.C. Global Honey Bee Viral Landscape Altered by a Parasitic Mite. Science. 2012;336:1304–1306. doi: 10.1126/science.1220941. PubMed DOI
Schroeder D.C., Martin S.J. Deformed Wing Virus: The Main Suspect in Unexplained Honeybee Deaths Worldwide. Virulence. 2012;3:589–591. doi: 10.4161/viru.22219. PubMed DOI PMC
Mordecai G.J., Brettell L.E., Martin S.J., Dixon D., Jones I.M., Schroeder D.C. Superinfection Exclusion and the Long-Term Survival of Honey Bees in Varroa-Infested Colonies. ISME J. 2016;10:1182–1191. doi: 10.1038/ismej.2015.186. PubMed DOI PMC
Natsopoulou M.E., McMahon D.P., Doublet V., Frey E., Rosenkranz P., Paxton R.J. The Virulent, Emerging Genotype B of Deformed Wing Virus Is Closely Linked to Overwinter Honeybee Worker Loss. Sci. Rep. 2017;7:5242. doi: 10.1038/s41598-017-05596-3. PubMed DOI PMC
Ongus J.R., Peters D., Bonmatin J.-M., Bengsch E., Vlak J.M., van Oers M.M. Complete Sequence of a Picorna-like Virus of the Genus Iflavirus Replicating in the Mite Varroa destructor. J. Gen. Virol. 2004;85:3747–3755. doi: 10.1099/vir.0.80470-0. PubMed DOI
McMahon D.P., Fürst M.A., Caspar J., Theodorou P., Brown M.J., Paxton R.J. A Sting in the Spit: Widespread Cross-infection of Multiple RNA Viruses across Wild and Managed Bees. J. Anim. Ecol. 2015;84:615–624. doi: 10.1111/1365-2656.12345. PubMed DOI PMC
Tehel A., Brown M.J., Paxton R.J. Impact of Managed Honey Bee Viruses on Wild Bees. Curr. Opin. Virol. 2016;19:16–22. doi: 10.1016/j.coviro.2016.06.006. PubMed DOI
Beims H., Bunk B., Erler S., Mohr K.I., Spröer C., Pradella S., Günther G., Rohde M., von der Ohe W., Steinert M. Discovery of Paenibacillus larvae ERIC V: Phenotypic and Genomic Comparison to Genotypes ERIC I-IV Reveal Different Inventories of Virulence Factors Which Correlate with Epidemiological Prevalences of American Foulbrood. Int. J. Med Microbiol. 2020;310:151394. doi: 10.1016/j.ijmm.2020.151394. PubMed DOI
Genersch E. American Foulbrood in Honeybees and Its Causative Agent, Paenibacillus larvae. J. Invertebr. Pathol. 2010;103:S10–S19. doi: 10.1016/j.jip.2009.06.015. PubMed DOI
Reybroeck W. Residues of Antibiotics and Chemotherapeutics in Honey. J. Apic. Res. 2018;57:97–112. doi: 10.1080/00218839.2017.1338129. DOI
Forsgren E. European Foulbrood in Honey Bees. J. Invertebr. Pathol. 2010;103:S5–S9. doi: 10.1016/j.jip.2009.06.016. PubMed DOI
Lewkowski O., Erler S. Virulence of Melissococcus plutonius and Secondary Invaders Associated with European Foulbrood Disease of the Honey Bee. MicrobiologyOpen. 2019;8:e00649. doi: 10.1002/mbo3.649. PubMed DOI PMC
Erban T., Ledvinka O., Kamler M., Hortova B., Nesvorna M., Tyl J., Titera D., Markovic M., Hubert J. Bacterial Community Associated with Worker Honeybees (Apis mellifera) Affected by European Foulbrood. PeerJ. 2017;5:e3816. doi: 10.7717/peerj.3816. PubMed DOI PMC
Martín-Hernández R., Bartolomé C., Chejanovsky N., Le Conte Y., Dalmon A., Dussaubat C., García-Palencia P., Meana A., Pinto M.A., Soroker V. Nosema ceranae in Apis mellifera: A 12 Years Postdetection Perspective. Environ. Microbiol. 2018;20:1302–1329. doi: 10.1111/1462-2920.14103. PubMed DOI
Spiltoir C.F. Life Cycle of Ascosphaera apis (Pericystis Apis) Am. J. Bot. 1955:501–508. doi: 10.1002/j.1537-2197.1955.tb11154.x. DOI
Mráz P., Hýbl M., Kopecký M., Bohatá A., Konopická J., Hoštičková I., Konvalina P., Šipoš J., Rost M., Čurn V. The Effect of Artificial Media and Temperature on the Growth and Development of the Honey Bee Brood Pathogen Ascosphaera apis. Biology. 2021;10:431. doi: 10.3390/biology10050431. PubMed DOI PMC
Chantawannakul P., Puchanichanthranon T., Wongsiri S. Inhibitory Effects of Some Medicinal Plant Extracts on the Growth of Ascosphaera apis; Proceedings of the III WOCMAP Congress on Medicinal and Aromatic Plants-Volume 4: Targeted Screening of Medicinal and Aromatic Plants, Economics 678; Chiang Mai, Thailand. 3–7 February 2003; pp. 183–189.
Ansari M.J., Al-Ghamdi A., Usmani S., Khan K.A., Alqarni A.S., Kaur M., Al-Waili N. In Vitro Evaluation of the Effects of Some Plant Essential Oils on Ascosphaera apis, the Causative Agent of Chalkbrood Disease. Saudi J. Biol. Sci. 2017;24:1001–1006. doi: 10.1016/j.sjbs.2016.04.016. PubMed DOI PMC
Aronstein K.A., Murray K.D. Chalkbrood Disease in Honey Bees. J. Invertebr. Pathol. 2010;103:S20–S29. doi: 10.1016/j.jip.2009.06.018. PubMed DOI
Schwarz R.S., Bauchan G.R., Murphy C.A., Ravoet J., de Graaf D.C., Evans J.D. Characterization of Two Species of Trypanosomatidae from the Honey Bee Apis mellifera: Crithidia mellificae Langridge and McGhee, and Lotmaria passim n. Gen., n. Sp. J. Eukaryot. Microbiol. 2015;62:567–583. doi: 10.1111/jeu.12209. PubMed DOI
Langridge D., McGhee R.B. Crithidia mellificae n. Sp. an Acidophilic Trypanosomatid of the Honey Bee Apis mellifera. J. Protozool. 1967;14:485–487. doi: 10.1111/j.1550-7408.1967.tb02033.x. PubMed DOI
Vejnovic B., Stevanovic J., Schwarz R.S., Aleksic N., Mirilovic M., Jovanovic N.M., Stanimirovic Z. Quantitative PCR Assessment of Lotmaria passim in Apis mellifera Colonies Co-Infected Naturally with Nosema ceranae. J. Invertebr. Pathol. 2018;151:76–81. doi: 10.1016/j.jip.2017.11.003. PubMed DOI
Ravoet J., Maharramov J., Meeus I., De Smet L., Wenseleers T., Smagghe G., De Graaf D.C. Comprehensive Bee Pathogen Screening in Belgium Reveals Crithidia mellificae as a New Contributory Factor to Winter Mortality. PLoS ONE. 2013;8:e72443. PubMed PMC
Arismendi N., Caro S., Castro M.P., Vargas M., Riveros G., Venegas T. Impact of Mixed Infections of Gut Parasites Lotmaria passim and Nosema ceranae on the Lifespan and Immune-Related Biomarkers in Apis mellifera. Insects. 2020;11:420. doi: 10.3390/insects11070420. PubMed DOI PMC
Castelli L., Branchiccela B., Invernizzi C., Tomasco I., Basualdo M., Rodriguez M., Zunino P., Antúnez K. Detection of Lotmaria passim in Africanized and European Honey Bees from Uruguay, Argentina and Chile. J. Invertebr. Pathol. 2019;160:95–97. doi: 10.1016/j.jip.2018.11.004. PubMed DOI
Raymann K., Moran N.A. The Role of the Gut Microbiome in Health and Disease of Adult Honey Bee Workers. Curr. Opin. Insect Sci. 2018;26:97–104. doi: 10.1016/j.cois.2018.02.012. PubMed DOI PMC
Hubert J., Bicianova M., Ledvinka O., Kamler M., Lester P.J., Nesvorna M., Kopecky J., Erban T. Changes in the Bacteriome of Honey Bees Associated with the Parasite Varroa destructor, and Pathogens Nosema and Lotmaria passim. Microb. Ecol. 2017;73:685–698. doi: 10.1007/s00248-016-0869-7. PubMed DOI
Hristov P., Shumkova R., Palova N., Neov B. Factors Associated with Honey Bee Colony Losses: A Mini-Review. Vet. Sci. 2020;7:166. doi: 10.3390/vetsci7040166. PubMed DOI PMC
Hýbl M., Mráz P., Šipoš J., Hoštičková I., Bohatá A., Čurn V., Kopec T. Polyphenols as Food Supplement Improved Food Consumption and Longevity of Honey Bees (Apis mellifera) Intoxicated by Pesticide Thiacloprid. Insects. 2021;12:572. doi: 10.3390/insects12070572. PubMed DOI PMC
Brodschneider R., Crailsheim K. Nutrition and Health in Honey Bees. Apidologie. 2010;41:278–294. doi: 10.1051/apido/2010012. DOI
Rutter L., Carrillo-Tripp J., Bonning B.C., Cook D., Toth A.L., Dolezal A.G. Transcriptomic Responses to Diet Quality and Viral Infection in Apis mellifera. BMC Genom. 2019;20:412. doi: 10.1186/s12864-019-5767-1. PubMed DOI PMC
Naug D. Nutritional Stress Due to Habitat Loss May Explain Recent Honeybee Colony Collapses. Biol. Conserv. 2009;142:2369–2372. doi: 10.1016/j.biocon.2009.04.007. DOI
Garbuzov M., Schürch R., Ratnieks F.L. Eating Locally: Dance Decoding Demonstrates That Urban Honey Bees in Brighton, UK, Forage Mainly in the Surrounding Urban Area. Urban Ecosyst. 2015;18:411–418. doi: 10.1007/s11252-014-0403-y. DOI
Hybl M., Mraz P., Sipos J. Diversity of Bees (Apoidea) and Their Pesticide Contamination in Two Different Types of Agricultural Management; Proceedings of the MendelNet; Brno, Czech Republic. 11–12 November 2020; pp. 216–221.
Ryba S., Titera D., Schodelbauerova-Traxmandlova I., Kindlmann P. Prevalence of Honeybee Viruses in the Czech Republic and Coinfections with Other Honeybee Disease. Biologia. 2012;67:590–595. doi: 10.2478/s11756-012-0038-5. DOI
Bakonyi T., Derakhshifar I., Grabensteiner E., Nowotny N. Development and Evaluation of PCR Assays for the Detection of Paenibacillus larvae in Honey Samples: Comparison with Isolation and Biochemical Characterization. Appl. Environ. Microbiol. 2003;69:1504–1510. doi: 10.1128/AEM.69.3.1504-1510.2003. PubMed DOI PMC
Govan V., Allsopp M., Davison S. A PCR Detection Method for Rapid Identification of Paenibacillus larvae. Appl. Environ. Microbiol. 1999;65:2243–2245. doi: 10.1128/AEM.65.5.2243-2245.1999. PubMed DOI PMC
Garrido-Bailón E., Higes M., Martínez-Salvador A., Antúnez K., Botías C., Meana A., Prieto L., Martín-Hernández R. The Prevalence of the Honeybee Brood Pathogens A Scosphaera apis, P Aenibacillus larvae and M Elissococcus plutonius in S Panish Apiaries Determined with a New Multiplex PCR Assay. Microb. Biotechnol. 2013;6:731–739. doi: 10.1111/1751-7915.12070. PubMed DOI PMC
Stevanovic J., Schwarz R.S., Vejnovic B., Evans J.D., Irwin R.E., Glavinic U., Stanimirovic Z. Species-Specific Diagnostics of Apis mellifera Trypanosomatids: A Nine-Year Survey (2007–2015) for Trypanosomatids and Microsporidians in Serbian Honey Bees. J. Invertebr. Pathol. 2016;139:6–11. doi: 10.1016/j.jip.2016.07.001. PubMed DOI
Arismendi N., Bruna A., Zapata N., Vargas M. PCR-Specific Detection of Recently Described Lotmaria passim (Trypanosomatidae) in Chilean Apiaries. J. Invertebr. Pathol. 2016;134:1–5. doi: 10.1016/j.jip.2015.12.008. PubMed DOI
Riveros G., Arismendi N., Zapata N., Evans D., Pérez I., Aldea P., Vargas M. Occurrence, Prevalence and Viral Load of Deformed Wing Virus Variants in Apis mellifera Colonies in Chile. J. Apic. Res. 2020;59:63–68. doi: 10.1080/00218839.2019.1670993. DOI
Sguazza G.H., Reynaldi F.J., Galosi C.M., Pecoraro M.R. Simultaneous Detection of Bee Viruses by Multiplex PCR. J. Virol. Methods. 2013;194:102–106. doi: 10.1016/j.jviromet.2013.08.003. PubMed DOI
Tentcheva D., Gauthier L., Zappulla N., Dainat B., Cousserans F., Colin M.E., Bergoin M. Prevalence and Seasonal Variations of Six Bee Viruses in Apis mellifera L. and Varroa destructor Mite Populations in France. Appl. Environ. Microbiol. 2004;70:7185–7191. doi: 10.1128/AEM.70.12.7185-7191.2004. PubMed DOI PMC
Iwanowicz D.D., Wu-Smart J.Y., Olgun T., Smart A.H., Otto C.R., Lopez D., Evans J.D., Cornman R. An Updated Genetic Marker for Detection of Lake Sinai Virus and Metagenetic Applications. PeerJ. 2020;8:e9424. doi: 10.7717/peerj.9424. PubMed DOI PMC
Gauthier L., Ravallec M., Tournaire M., Cousserans F., Bergoin M., Dainat B., de Miranda J.R. Viruses Associated with Ovarian Degeneration in Apis mellifera L. Queens. PLoS ONE. 2011;6:e16217. doi: 10.1371/journal.pone.0016217. PubMed DOI PMC
Bates D., Mächler M., Bolker B., Walker S. Fitting Linear Mixed-Effects Models Using Lme4. arXiv. 20141406.5823
ter Braak C.J., Smilauer P. Canoco Reference Manual and User’s Guide: Software for Ordination, Version 5.0. 2012. [(accessed on 22 September 2021)]. Available online: https://research.wur.nl/en/publications/canoco-reference-manual-and-users-guide-software-for-ordination-v.
Gómez-Moracho T., Buendía-Abad M., Benito M., García-Palencia P., Barrios L., Bartolomé C., Maside X., Meana A., Jiménez-Antón M.D., Olías-Molero A.I. Experimental Evidence of Harmful Effects of Crithidia mellificae and Lotmaria passim on Honey Bees. Int. J. Parasitol. 2020;50:1117–1124. doi: 10.1016/j.ijpara.2020.06.009. PubMed DOI
Michalczyk M., Bancerz-Kisiel A., Sokół R. Lotmaria passim as Third Parasite Gastrointestinal Tract of Honey Bees Living in Tree Trunk. J. Apic. Sci. 2020;64:143–151. doi: 10.2478/jas-2020-0012. DOI
Cepero A., Ravoet J., Gómez-Moracho T., Bernal J.L., Del Nozal M.J., Bartolomé C., Maside X., Meana A., González-Porto A.V., de Graaf D.C. Holistic Screening of Collapsing Honey Bee Colonies in Spain: A Case Study. BMC Res. Notes. 2014;7:649. doi: 10.1186/1756-0500-7-649. PubMed DOI PMC
Higes M., Martín-Hernández R., Botías C., Bailón E.G., González-Porto A.V., Barrios L., Del Nozal M.J., Bernal J.L., Jiménez J.J., Palencia P.G. How Natural Infection by Nosema ceranae Causes Honeybee Colony Collapse. Environ. Microbiol. 2008;10:2659–2669. doi: 10.1111/j.1462-2920.2008.01687.x. PubMed DOI
Gisder S., Hedtke K., Möckel N., Frielitz M.-C., Linde A., Genersch E. Five-Year Cohort Study of Nosema Spp. in Germany: Does Climate Shape Virulence and Assertiveness of Nosema ceranae? Appl. Environ. Microbiol. 2010;76:3032–3038. doi: 10.1128/AEM.03097-09. PubMed DOI PMC
Stevanovic J., Stanimirovic Z., Genersch E., Kovacevic S.R., Ljubenkovic J., Radakovic M., Aleksic N. Dominance of Nosema ceranae in Honey Bees in the Balkan Countries in the Absence of Symptoms of Colony Collapse Disorder. Apidologie. 2011;42:49–58. doi: 10.1051/apido/2010034. DOI
Higes M., Meana A., Bartolomé C., Botías C., Martín-Hernández R. Nosema ceranae (Microsporidia), a Controversial 21st Century Honey Bee Pathogen. Environ. Microbiol. Rep. 2013;5:17–29. doi: 10.1111/1758-2229.12024. PubMed DOI
Paxton R.J., Klee J., Korpela S., Fries I. Nosema ceranae Has Infected Apis mellifera in Europe since at Least 1998 and May Be More Virulent than Nosema apis. Apidologie. 2007;38:558–565. doi: 10.1051/apido:2007037. DOI
Gisder S., Schüler V., Horchler L.L., Groth D., Genersch E. Long-Term Temporal Trends of Nosema Spp. Infection Prevalence in Northeast Germany: Continuous Spread of Nosema ceranae, an Emerging Pathogen of Honey Bees (Apis mellifera), but No General Replacement of Nosema apis. Front. Cell. Infect. Microbiol. 2017;7:301. doi: 10.3389/fcimb.2017.00301. PubMed DOI PMC
Shumkova R., Georgieva A., Radoslavov G., Sirakova D., Dzhebir G., Neov B., Bouga M., Hristov P. The First Report of the Prevalence of Nosema ceranae in Bulgaria. PeerJ. 2018;6:e4252. doi: 10.7717/peerj.4252. PubMed DOI PMC
Ostroverkhova N.V., Konusova O.L., Kucher A.N., Kireeva T.N., Rosseykina S.A. Prevalence of the Microsporidian Nosema Spp. in Honey Bee Populations (Apis mellifera) in Some Ecological Regions of North Asia. Vet. Sci. 2020;7:111. doi: 10.3390/vetsci7030111. PubMed DOI PMC
Li Z., You X., Wang L., Yan Z., Zhou Z. Spore Morphology and Ultrastructure of an Ascosphaera apis Strain from the Honeybees (Apis mellifera) in Southwest China. Mycologia. 2018;110:325–338. doi: 10.1080/00275514.2018.1442084. PubMed DOI
Biová J., Bzdil J., Dostálková S., Petrivalsky M., Brus J., Carra E., Danihlík J. American Foulbrood in the Czech Republic: ERIC II Genotype of Paenibacillus larvae Is Prevalent. Front. Vet. Sci. 2021;8:698976. doi: 10.3389/fvets.2021.698976. PubMed DOI PMC
Erban T., Ledvinka O., Kamler M., Hortova B., Nesvorna M., Tyl J., Titera D., Markovic M., Hubert J. European Foulbrood in Czechia after 40 Years: Application of next-Generation Sequencing to Analyze Melissococcus plutonius Transmission and Influence on the Bacteriome of Apis mellifera. PeerJ Prepr. 2017;4:e2618v1.
Budge G.E., Barrett B., Jones B., Pietravalle S., Marris G., Chantawannakul P., Thwaites R., Hall J., Cuthbertson A.G., Brown M.A. The Occurrence of Melissococcus plutonius in Healthy Colonies of Apis mellifera and the Efficacy of European Foulbrood Control Measures. J. Invertebr. Pathol. 2010;105:164–170. doi: 10.1016/j.jip.2010.06.004. PubMed DOI
Roy C., Franco S. Investigation of an Atypical Case of European Foulbrood in France. Vet. Rec. Case Rep. 2021;9:e45. doi: 10.1002/vrc2.45. DOI
Grangier V., Belloy L., Charrière J.-D., Doherr M.G., Fritsche A., Waldvogel A.S. Real-Time PCR as a Decision Aid in the Control of European Foulbrood. J. Apic. Res. 2015;54:366–372. doi: 10.1080/00218839.2016.1169650. DOI
Kevill J.L., de Souza F.S., Sharples C., Oliver R., Schroeder D.C., Martin S.J. DWV-A Lethal to Honey Bees (Apis mellifera): A Colony Level Survey of DWV Variants (A, B, and C) in England, Wales, and 32 States across the US. Viruses. 2019;11:426. doi: 10.3390/v11050426. PubMed DOI PMC
Olgun T., Everhart S.E., Anderson T., Wu-Smart J. Comparative Analysis of Viruses in Four Bee Species Collected from Agricultural, Urban, and Natural Landscapes. PLoS ONE. 2020;15:e0234431. PubMed PMC
McMahon D.P., Natsopoulou M.E., Doublet V., Fürst M., Weging S., Brown M.J., Gogol-Döring A., Paxton R.J. Elevated Virulence of an Emerging Viral Genotype as a Driver of Honeybee Loss. Proc. R. Soc. B Biol. Sci. 2016;283:20160811. doi: 10.1098/rspb.2016.0811. PubMed DOI PMC
Tehel A., Vu Q., Bigot D., Gogol-Döring A., Koch P., Jenkins C., Doublet V., Theodorou P., Paxton R. The Two Prevalent Genotypes of an Emerging Infectious Disease, Deformed Wing Virus, Cause Equally Low Pupal Mortality and Equally High Wing Deformities in Host Honey Bees. Viruses. 2019;11:114. doi: 10.3390/v11020114. PubMed DOI PMC
Gisder S., Möckel N., Eisenhardt D., Genersch E. In Vivo Evolution of Viral Virulence: Switching of Deformed Wing Virus between Hosts Results in Virulence Changes and Sequence Shifts. Environ. Microbiol. 2018;20:4612–4628. doi: 10.1111/1462-2920.14481. PubMed DOI
Ryabov E.V., Childers A.K., Chen Y., Madella S., Nessa A., Evans J.D. Recent Spread of Varroa destructor Virus-1, a Honey Bee Pathogen, in the United States. Sci. Rep. 2017;7:17447. doi: 10.1038/s41598-017-17802-3. PubMed DOI PMC
Manley R., Temperton B., Doyle T., Gates D., Hedges S., Boots M., Wilfert L. Knock-on Community Impacts of a Novel Vector: Spillover of Emerging DWV-B from Varroa-infested Honeybees to Wild Bumblebees. Ecol. Lett. 2019;22:1306–1315. doi: 10.1111/ele.13323. PubMed DOI PMC
Kevill J.L., Highfield A., Mordecai G.J., Martin S.J., Schroeder D.C. ABC Assay: Method Development and Application to Quantify the Role of Three DWV Master Variants in Overwinter Colony Losses of European Honey Bees. Viruses. 2017;9:314. doi: 10.3390/v9110314. PubMed DOI PMC
Berthoud H., Imdorf A., Haueter M., Radloff S., Neumann P. Virus Infections and Winter Losses of Honey Bee Colonies (Apis mellifera) J. Apic. Res. 2010;49:60–65. doi: 10.3896/IBRA.1.49.1.08. DOI
Nguyen B.K., Ribière M., vanEngelsdorp D., Snoeck C., Saegerman C., Kalkstein A.L., Schurr F., Brostaux Y., Faucon J.-P., Haubruge E. 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. 2011;50:195–202. doi: 10.3896/IBRA.1.50.3.03. DOI
Faurot-Daniels C., Glenny W., Daughenbaugh K.F., McMenamin A.J., Burkle L.A., Flenniken M.L. Longitudinal Monitoring of Honey Bee Colonies Reveals Dynamic Nature of Virus Abundance and Indicates a Negative Impact of Lake Sinai Virus 2 on Colony Health. PLoS ONE. 2020;15:e0237544. doi: 10.1371/journal.pone.0237544. PubMed DOI PMC
De Miranda J.R., Cornman R.S., Evans J.D., Semberg E., Haddad N., Neumann P., Gauthier L. Genome Characterization, Prevalence and Distribution of a Macula-like Virus from Apis mellifera and Varroa destructor. Viruses. 2015;7:3586–3602. doi: 10.3390/v7072789. PubMed DOI PMC
McMenamin A.J., Flenniken M.L. Recently Identified Bee Viruses and Their Impact on Bee Pollinators. Curr. Opin. Insect Sci. 2018;26:120–129. doi: 10.1016/j.cois.2018.02.009. PubMed DOI
Abou Kubaa R., Molinatto G., Khaled B., Daher-Hjaij N., Heinoun K., Saponari M. First Detection of Black Queen Cell Virus, Varroa destructor Macula-like Virus, Apis mellifera Filamentous Virus and Nosema ceranae in Syrian Honey Bees Apis mellifera Syriaca. Bull. Insectol. 2018;71:217–224.
von Büren R.S., Oehen B., Kuhn N.J., Erler S. High-Resolution Maps of Swiss Apiaries and Their Applicability to Study Spatial Distribution of Bacterial Honey Bee Brood Diseases. PeerJ. 2019;7:e6393. doi: 10.7717/peerj.6393. PubMed DOI PMC
Brodschneider R., Brus J., Danihlík J. Comparison of Apiculture and Winter Mortality of Honey Bee Colonies (Apis mellifera) in Austria and Czechia. Agric. Ecosyst. Environ. 2019;274:24–32. doi: 10.1016/j.agee.2019.01.002. DOI
Taric E., Glavinic U., Vejnovic B., Stanojkovic A., Aleksic N., Dimitrijevic V., Stanimirovic Z. Oxidative Stress, Endoparasite Prevalence and Social Immunity in Bee Colonies Kept Traditionally vs. Those Kept for Commercial Purposes. Insects. 2020;11:266. doi: 10.3390/insects11050266. PubMed DOI PMC
Tehel A., Streicher T., Tragust S., Paxton R.J. 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;7:200480. doi: 10.1098/rsos.200480. PubMed DOI PMC
Simone-Finstrom M., Li-Byarlay H., Huang M.H., Strand M.K., Rueppell O., Tarpy D.R. Migratory Management and Environmental Conditions Affect Lifespan and Oxidative Stress in Honey Bees. Sci. Rep. 2016;6:32023. doi: 10.1038/srep32023. PubMed DOI PMC
Graystock P., Ng W.H., Parks K., Tripodi A.D., Muñiz P.A., Fersch A.A., Myers C.R., McFrederick Q.S., McArt S.H. Dominant Bee Species and Floral Abundance Drive Parasite Temporal Dynamics in Plant-Pollinator Communities. Nat. Ecol. Evol. 2020;4:1358–1367. doi: 10.1038/s41559-020-1247-x. PubMed DOI PMC