Intestinal Microbiota of Honey Bees (Apis mellifera) Treated with Amitraz

Alberoni, D., Baffoni, L., Gaggìa, F., Ryan, P., Murphy, K., Ross, P, … Di Gioia, D. (2018). Impact of beneficial bacteria supplementation on the gut microbiota, colony development and productivity of Apis mellifera L. Beneficial Microbes, 9, 269–278. https://doi.org/10.3920/BM2017.0061 AlberoniD. BaffoniL. GaggìaF. RyanP. MurphyK. RossP Di GioiaD. 2018 Impact of beneficial bacteria supplementation on the gut microbiota, colony development and productivity of Apis mellifera L. Beneficial Microbes 9 269 278 https://doi.org/10.3920/BM2017.0061 10.3920/BM2017.006129380644 Search in Google Scholar

Anderson, K.E., Sheehan, T.H., Eckholm, B.J. (2011). An emerging paradigm of colony health: microbial balance of the honey bee and hive (Apis mellifera). Insectes Sociaux, 58, 431. https://doi.org/10.1007/s00040-011-0194-6 AndersonK.E. SheehanT.H. EckholmB.J. 2011 An emerging paradigm of colony health: microbial balance of the honey bee and hive (Apis mellifera) Insectes Sociaux 58 431 https://doi.org/10.1007/s00040-011-0194-6 10.1007/s00040-011-0194-6 Search in Google Scholar

Audisio, M.C. (2017). Gram-positive bacteria with probiotic potential for the Apis mellifera L. honey bee: The experience in the Northwest of Argentina. Probiotics Antimicrobial Proteins, 9, 22–31. https://doi.org/10.1007/s12602-016-9231-0 AudisioM.C. 2017 Gram-positive bacteria with probiotic potential for the Apis mellifera L. honey bee: The experience in the Northwest of Argentina Probiotics Antimicrobial Proteins 9 22 31 https://doi.org/10.1007/s12602-016-9231-0 10.1007/s12602-016-9231-027655068 Search in Google Scholar

Babendreier, D., Joller, D., Romeis, J., Bigler, F., Widmer, F. (2006). Bacterial community structures in honeybee intestines and their response to two insecticidal proteins. FEMS Microbiology Ecology, 59, 600–610. https://doi.org/10.1111/j.1574-6941.2006.00249.x BabendreierD. JollerD. RomeisJ. BiglerF. WidmerF. 2006 Bacterial community structures in honeybee intestines and their response to two insecticidal proteins FEMS Microbiology Ecology 59 600 610 https://doi.org/10.1111/j.1574-6941.2006.00249.x 10.1111/j.1574-6941.2006.00249.x17381517 Search in Google Scholar

Bahreini, R., & Currie R.W. (2015). Influence of honey bee genotype and wintering method on wintering performance of Varroa destructor (Parasitiformes: Varroidae) infected honey bee (Hymenoptera: Apidae) colonies in a Northern Climate. Journal of Economic Entomology, 108(4), 1495–505. https://doi.org/10.1093/jee/tov164 BahreiniR. CurrieR.W. 2015 Influence of honey bee genotype and wintering method on wintering performance of Varroa destructor (Parasitiformes: Varroidae) infected honey bee (Hymenoptera: Apidae) colonies in a Northern Climate Journal of Economic Entomology 108 4 1495 505 https://doi.org/10.1093/jee/tov164 10.1093/jee/tov16426470288 Search in Google Scholar

Blot, N., Veillat, L., Rouzé, R., Delatte, H. (2019). Glyphosate, but not its metabolite AMPA, alters the honeybee gut microbiota. PLoS One, 14:e0215466. https://doi.org/10.1371/journal.pone.0215466 BlotN. VeillatL. RouzéR. DelatteH. 2019 Glyphosate, but not its metabolite AMPA, alters the honeybee gut microbiota PLoS One 14 e0215466 https://doi.org/10.1371/journal.pone.0215466 10.1371/journal.pone.0215466646741630990837 Search in Google Scholar

Bober, A., Pohoreka, K., Skubida, M., Zdańska, D. (2016). Zdrowotność rodzin pszczelich w Polsce i Europie w świetle wyników programu EPILOBEE (2012–2014). In Proceedings of 53^rd Scientific Beekeeping Conference, Puławy. BoberA. PohorekaK. SkubidaM. ZdańskaD. 2016 Zdrowotność rodzin pszczelich w Polsce i Europie w świetle wyników programu EPILOBEE (2012–2014) In Proceedings of 53rd Scientific Beekeeping Conference Puławy Search in Google Scholar

Buczek, K. (2008). Pathogens of Apis mellifera. Annales Universitatis Mariae Curie-Skłodowska, section DD, 63(3), 1–10. BuczekK. 2008 Pathogens of Apis mellifera Annales Universitatis Mariae Curie-Skłodowska, section DD 63 3 1 10 10.2478/v10082-008-0008-8 Search in Google Scholar

Cox-Foster, D.L, Conlan, S., Holmes, E.C., Palacios, G., Evans, J.D., Moran, N.A. (2007). A metagenomic survey of microbes in honey bee colony collapse disorder. Science, 318, 283–287. https://doi.org/10.1126/science.1146498 Cox-FosterD.L ConlanS. HolmesE.C. PalaciosG. EvansJ.D. MoranN.A. 2007 A metagenomic survey of microbes in honey bee colony collapse disorder Science 318 283 287 https://doi.org/10.1126/science.1146498 10.1126/science.114649817823314 Search in Google Scholar

Cuesta-Maté, A., Renelies-Hamilton, J., Kryger, P., Jensen, A.B., Sinotte, V.M., Poulsen, M. (2021). Resistance and vulnerability of honeybee (Apis mellifera) gut bacteria to commonly used pesticides. Frontiers in Microbiology, 3(12), 717990. https://doi.org/10.3389/fmicb.2021.717990 Cuesta-MatéA. Renelies-HamiltonJ. KrygerP. JensenA.B. SinotteV.M. PoulsenM. 2021 Resistance and vulnerability of honeybee (Apis mellifera) gut bacteria to commonly used pesticides Frontiers in Microbiology 3 12 717990. https://doi.org/10.3389/fmicb.2021.717990 10.3389/fmicb.2021.717990844652634539609 Search in Google Scholar

Dai, P., Jack, C.J., Mortensen, A.N., Bustamante, T.A., Ellis, J.D. (2018). Chronic toxicity of amitraz, coumaphos and fluvalinate to Apis mellifera L. larvae reared in vitro. Scientific Reports, 8(1), 5635. https://doi.org/10.1038/s41598-018-24045-3 DaiP. JackC.J. MortensenA.N. BustamanteT.A. EllisJ.D. 2018 Chronic toxicity of amitraz, coumaphos and fluvalinate to Apis mellifera L. larvae reared in vitro Scientific Reports 8 1 5635 https://doi.org/10.1038/s41598-018-24045-3 10.1038/s41598-018-24045-3588478429618776 Search in Google Scholar

Di Noi, A., Casini, S., Campani, T., Cai, G., Caliani, I. (2021). Review on sublethal effects of environmental contaminants in honey bees (Apis mellifera), knowledge gaps and future perspectives. International Journal of Environmental Research and Public Health, 18, 1863. https://doi.org/10.3390/ijerph18041863 Di NoiA. CasiniS. CampaniT. CaiG. CalianiI. 2021 Review on sublethal effects of environmental contaminants in honey bees (Apis mellifera), knowledge gaps and future perspectives International Journal of Environmental Research and Public Health 18 1863 https://doi.org/10.3390/ijerph18041863 10.3390/ijerph18041863791879933672936 Search in Google Scholar

Dong, Z.X., Li, H.Y., Chen, Y.F., Wang, F., Deng, X.Y., Lin, L.B., … Guo, J. (2020). Colonization of the gut microbiota of honey bee (Apis mellifera) workers at different developmental stages. Microbiology Research, 231, 126370. https://doi.org/10.1016/j.micres.2019.126370 DongZ.X. LiH.Y. ChenY.F. WangF. DengX.Y. LinL.B. GuoJ. 2020 Colonization of the gut microbiota of honey bee (Apis mellifera) workers at different developmental stages Microbiology Research 231 126370. https://doi.org/10.1016/j.micres.2019.126370 10.1016/j.micres.2019.12637031739261 Search in Google Scholar

Dosch, C., Manigk, A., Streicher, T., Tehel, A., Paxton, R.J., Tragust, S. (2021). The gut microbiota can provide viral tolerance in the honey bee. Microorganisms, 9(4), 871. https://doi.org/10.3390/microorganisms9040871 DoschC. ManigkA. StreicherT. TehelA. PaxtonR.J. TragustS. 2021 The gut microbiota can provide viral tolerance in the honey bee Microorganisms 9 4 871 https://doi.org/10.3390/microorganisms9040871 10.3390/microorganisms9040871807260633920692 Search in Google Scholar

Gąbka, J., Kotlicki, W., Kamiński, Z., Zajdel, B. (2019). Effectiveness of Apiwarol applied by electric smoker for control of Varroa destructor in honey bee colonies. Medycyna Weterynaryjna, 75(4), 253–255. https://doi.org/10.21521/mw.6199 GąbkaJ. KotlickiW. KamińskiZ. ZajdelB. 2019 Effectiveness of Apiwarol applied by electric smoker for control of Varroa destructor in honey bee colonies Medycyna Weterynaryjna 75 4 253 255 https://doi.org/10.21521/mw.6199 10.21521/mw.6199 Search in Google Scholar

Gaggìa, F., Baffoni, L., Alberoni, D. (2018). Probiotics for honeybees’ health. In probiotics and prebiotics in animal health and food safety, Di Gioia, D., Biavati, B., Eds.; Springer International Publishing: Cham, Switzerland, pp. 219–245. GaggìaF. BaffoniL. AlberoniD. 2018 Probiotics for honeybees’ health. In probiotics and prebiotics in animal health and food safety Di GioiaD. BiavatiB. Eds.; Springer International Publishing Cham, Switzerland 219 245 10.1007/978-3-319-71950-4_9 Search in Google Scholar

Gregorc, A., & Bowen, I.D. (2000). Histochemical characterization of cell death in honeybee larvae midgut after treatment with Paenibacillus larvae, amitraz and oxytetracycline. Cell Biology International, 24, 319–324. https://doi.org/10.1006/cbir.1999.0490 GregorcA. BowenI.D. 2000 Histochemical characterization of cell death in honeybee larvae midgut after treatment with Paenibacillus larvae, amitraz and oxytetracycline Cell Biology International 24 319 324 https://doi.org/10.1006/cbir.1999.0490 10.1006/cbir.1999.049010805966 Search in Google Scholar

Hotchkiss, M.Z., Poulain, A.J., Forrest, J.R.K. (2022). Pesticide-induced disturbances of bee gut microbiotas. FEMS Microbiology Reviews, 46(2), fuab056. https://doi.org/10.1093/femsre/fuab056 HotchkissM.Z. PoulainA.J. ForrestJ.R.K. 2022 Pesticide-induced disturbances of bee gut microbiotas FEMS Microbiology Reviews 46 2 fuab056 https://doi.org/10.1093/femsre/fuab056 10.1093/femsre/fuab05635107129 Search in Google Scholar

Iorizzo, M., Letizia, F., Ganassi, S., Testa, B., Petrarca, S., Albanese, G., … De Cristofaro, A. (2022). Functional properties and antimicrobial activity from lactic acid bacteria as resources to improve the health and welfare of honey bees. Insects, 13, 308. https://doi.org/10.3390/insects13030308 IorizzoM. LetiziaF. GanassiS. TestaB. PetrarcaS. AlbaneseG. De CristofaroA. 2022 Functional properties and antimicrobial activity from lactic acid bacteria as resources to improve the health and welfare of honey bees Insects 13 308 https://doi.org/10.3390/insects13030308 10.3390/insects13030308895398735323606 Search in Google Scholar

Iorizzo, M., Pannella, G., Lombardi, S.J., Ganassi, S., Testa, B., Succi, M., … Tremonte P. (2020). Inter- and intra-species diversity of lactic acid bacteria in Apis mellifera ligustica colonie. Microorganisms, 8, 1578. https://doi.org/10.3390/microorganisms8101578 IorizzoM. PannellaG. LombardiS.J. GanassiS. TestaB. SucciM. TremonteP. 2020 Inter- and intra-species diversity of lactic acid bacteria in Apis mellifera ligustica colonie Microorganisms 8 1578 https://doi.org/10.3390/microorganisms8101578 10.3390/microorganisms8101578760224833066358 Search in Google Scholar

Iorizzo, M., Testa, B., Lombardi, S.J, Ganassi, S., Ianiro, M., Letizia, F.,… De Cristofaro, A. (2020). Antimicrobial Activity against Paenibacillus larvae and functional properties of Lactiplantibacillus plantarum strains: Potential Benefits for Honeybee Health. Antibiotics (Basel), 9(8), 442. https://doi.org/10.3390/antibiotics9080442. PMID: 32722196; PMCID: PMC7460353 IorizzoM. TestaB. LombardiS.J GanassiS. IaniroM. LetiziaF. De CristofaroA. 2020 Antimicrobial Activity against Paenibacillus larvae and functional properties of Lactiplantibacillus plantarum strains: Potential Benefits for Honeybee Health Antibiotics (Basel) 9 8 442 https://doi.org/10.3390/antibiotics9080442. PMID: 32722196; PMCID: PMC7460353 10.3390/antibiotics9080442746035332722196 Search in Google Scholar

Keller, A., McFrederick, Q.S., Dharampal, P., Steffan, S., Danforth, B.N., Leonhardt, S.D. (2021). Hitchhikers through the network: The shared microbiome of bees and flowers. Current Opinion in Insect Science, 44, 8–15. https://doi.org/10.1016/j.cois.2020.09.007 KellerA. McFrederickQ.S. DharampalP. SteffanS. DanforthB.N. LeonhardtS.D. 2021 Hitchhikers through the network: The shared microbiome of bees and flowers Current Opinion in Insect Science 44 8 15 https://doi.org/10.1016/j.cois.2020.09.007 10.1016/j.cois.2020.09.00732992041 Search in Google Scholar

Motta, E.V.S., Raymann, K., Moran, N.A. (2018). Glyphosate perturbs the gut microbiota of honeybees. Proceedings of the National Academy of Sciences of the United States of America, 115(41), 10305–10310. https://doi.org/10.1073/pnas.1803880115 MottaE.V.S. RaymannK. MoranN.A. 2018 Glyphosate perturbs the gut microbiota of honeybees Proceedings of the National Academy of Sciences of the United States of America 115 41 10305 10310 https://doi.org/10.1073/pnas.1803880115 10.1073/pnas.1803880115618712530249635 Search in Google Scholar

Naree, S., Ellis, J.D., Benbow, M.E., Suwannapong, G. (2022). Experimental Nosema ceranae infection is associated with microbiome changes in the midguts of four species of Apis (honey bees). Journal of Apicultural Research, 61(3), 435–447. https://doi.org/10.1080/00218839.2021.1987086 NareeS. EllisJ.D. BenbowM.E. SuwannapongG. 2022 Experimental Nosema ceranae infection is associated with microbiome changes in the midguts of four species of Apis (honey bees) Journal of Apicultural Research 61 3 435 447 https://doi.org/10.1080/00218839.2021.1987086 10.1080/00218839.2021.1987086 Search in Google Scholar

Nowak, A., Szczuka, D., Górczyńska, A., Motyl, I., Kręgiel, D. (2021). Characterization of Apis mellifera gastrointestinal microbiota and lactic acid bacteria for honeybee protection-a review. Cells, 10(3),701, https://doi.org/10.3390/cells10030701 NowakA. SzczukaD. GórczyńskaA. MotylI. KręgielD. 2021 Characterization of Apis mellifera gastrointestinal microbiota and lactic acid bacteria for honeybee protection-a review Cells 10 3 701 https://doi.org/10.3390/cells10030701 10.3390/cells10030701800419433809924 Search in Google Scholar

Nowotnik, P. (2019). Niebezpieczne zmiany w biologii Varroa destructor. Pasieka, 1, 26–28. NowotnikP. 2019 Niebezpieczne zmiany w biologii Varroa destructor Pasieka 1 26 28 Search in Google Scholar

Peters, J.M., Peleg, O., Mahadevan, L. (2019). Collective ventilation in honeybee nests. The Journal of the Royal Society Interface, 16(150), 1–8. https://doi.org/10.1098/rsif.2018.0561 PetersJ.M. PelegO. MahadevanL. 2019 Collective ventilation in honeybee nests The Journal of the Royal Society Interface 16 150 1 8 https://doi.org/10.1098/rsif.2018.0561 10.1098/rsif.2018.0561636465530958168 Search in Google Scholar

Ramsey, S., Ochoa, R., Bauchan, G., Gulbronson, C., Mowery, J., Cohen, A., … Engelsdorp, D. (2019). Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proceedings of the National Academy of Sciences of the United States of America, 116(5),1792–1801. DOI: 10.1073/pnas.1818371116 RamseyS. OchoaR. BauchanG. GulbronsonC. MoweryJ. CohenA. EngelsdorpD. 2019 Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph Proceedings of the National Academy of Sciences of the United States of America 116 5 1792 1801 10.1073/pnas.1818371116 635871330647116 Open DOISearch in Google Scholar

Raymann, K., & Moran, N.A. (2018). The role of the gut microbiome in health and disease of adult honey bee workers. Current Opinion in Insect Science, 26, 97–104. https://doi.org/10.1016/j.cois.2018.02.012 RaymannK. MoranN.A. 2018 The role of the gut microbiome in health and disease of adult honey bee workers Current Opinion in Insect Science 26 97 104 https://doi.org/10.1016/j.cois.2018.02.012 10.1016/j.cois.2018.02.012601023029764668 Search in Google Scholar

Rinkevich, F.D. (2020). Detection of amitraz resistance and reduced treatment efficacy in the Varroa Mite, Varroa destructor, within commercial beekeeping operations. PLoS One, 15:e0227264. https://doi.org/10.1371/journal.pone.0227264 RinkevichF.D. 2020 Detection of amitraz resistance and reduced treatment efficacy in the Varroa Mite, Varroa destructor, within commercial beekeeping operations PLoS One 15 e0227264 https://doi.org/10.1371/journal.pone.0227264 10.1371/journal.pone.0227264696886331951619 Search in Google Scholar

Rosenkranz, P., Aumeier, P., Ziegelmann, B. (2010). Biology and control of Varroa destructor. Journal of Invertebrate Pathology, 103, S96–S119. https://doi.org/10.1016/j.jip.2009.07.016 RosenkranzP. AumeierP. ZiegelmannB. 2010 Biology and control of Varroa destructor Journal of Invertebrate Pathology 103 S96 S119 https://doi.org/10.1016/j.jip.2009.07.016 10.1016/j.jip.2009.07.01619909970 Search in Google Scholar

Rouzé, R., Moné, A., Delbac, F., Belzunces, L., Blot, N. (2019). The honeybee gut microbiota is altered after chronic exposure to different families of insecticides and infection by Nosema ceranae. Microbes Environment, 34, 226–233. https://doi.org/10.1264/jsme2.ME18169 RouzéR. MonéA. DelbacF. BelzuncesL. BlotN. 2019 The honeybee gut microbiota is altered after chronic exposure to different families of insecticides and infection by Nosema ceranae Microbes Environment 34 226 233 https://doi.org/10.1264/jsme2.ME18169 10.1264/jsme2.ME18169675934931378758 Search in Google Scholar

Santorelli, L.A., Wilkinson, T., Abdulmalik, R., Rai, Y., Creevey, C.J., Huws, S., Gutierrez-Merino, J. (2021). Beehives possess their own distinct microbiomes. bioRxiv, 2021.08.25.457643. https://doi.org/10.1101/2021.08.25.45764 SantorelliL.A. WilkinsonT. AbdulmalikR. RaiY. CreeveyC.J. HuwsS. Gutierrez-MerinoJ. 2021 Beehives possess their own distinct microbiomes bioRxiv 2021.08.25.457643. https://doi.org/10.1101/2021.08.25.45764 10.1101/2021.08.25.457643 Search in Google Scholar

Semkiw, P. (2020). Sektor pszczelarski w Polsce w 2020 roku. InHort. Puławy. SemkiwP. 2020 Sektor pszczelarski w Polsce w 2020 roku InHort Puławy Search in Google Scholar

Strachecka, A., Sawicki, M., Borsuk, G., Olszewski, K., Paleolog, J., Bajda, M., Chobotow, J. (2013). Akarycydy jako sposób walki z roztoczami Varroa destructor w rodzinach pszczelich - skuteczność i zagrożenia. Medycyna Weterynaryjna, 69(4), 219–224. StracheckaA. SawickiM. BorsukG. OlszewskiK. PaleologJ. BajdaM. ChobotowJ. 2013 Akarycydy jako sposób walki z roztoczami Varroa destructor w rodzinach pszczelich - skuteczność i zagrożenia Medycyna Weterynaryjna 69 4 219 224 Search in Google Scholar

Van Dooremalen, C., Cornelissen, B., Poleij-Hok-Ahin, C., Blacquière, T. (2018). Single and interactive effects of Varroa destructor, Nosema spp., and imidacloprid on honey bee colonies (Apis mellifera). Ecosphere, 9(8), e02378. https://doi.org/10.1002/ecs2.2378 Van DooremalenC. CornelissenB. Poleij-Hok-AhinC. BlacquièreT. 2018 Single and interactive effects of Varroa destructor, Nosema spp., and imidacloprid on honey bee colonies (Apis mellifera) Ecosphere 9 8 e02378 https://doi.org/10.1002/ecs2.2378 10.1002/ecs2.2378 Search in Google Scholar

Vasquez, A., Forsgren, E., Fries, I., Paxton, R.J., Flaberg, E., Szekely, L. (2012). Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS One, 7:e33188. https://doi.org/10.1371/journal.pone.0033188 VasquezA. ForsgrenE. FriesI. PaxtonR.J. FlabergE. SzekelyL. 2012 Symbionts as major modulators of insect health: lactic acid bacteria and honeybees PLoS One 7 e33188 https://doi.org/10.1371/journal.pone.0033188 10.1371/journal.pone.0033188329975522427985 Search in Google Scholar

Zhang, Y., Lu, X., Huang, S., Zhang, L., Huang, S. (2019). Nosema ceranae infection enhances Bifidobacterium spp. abundances in the honey bee hindgut. Apidologie, 50, 353–362. https://doi.org/10.1007/s13592-019-00644-5 ZhangY. LuX. HuangS. ZhangL. HuangS. 2019 Nosema ceranae infection enhances Bifidobacterium spp. abundances in the honey bee hindgut Apidologie 50 353 362 https://doi.org/10.1007/s13592-019-00644-5 10.1007/s13592-019-00644-5 Search in Google Scholar

Zheng, H., Steele, M., Leonard, S., Motta, E., Moran, N. (2018). Honey bees as models for gut microbiota research. Lab Animal, 47(11), 317–325. https://doi.org/10.1038/s41684-018-0173-x ZhengH. SteeleM. LeonardS. MottaE. MoranN. 2018 Honey bees as models for gut microbiota research Lab Animal 47 11 317 325 https://doi.org/10.1038/s41684-018-0173-x 10.1038/s41684-018-0173-x647802030353179 Search in Google Scholar