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Vairimorpha apis Versus Vairimorpha ceranae, Replacement or Dynamic Prevalence?


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1. Al Naggar, Y., Baer, B., 2019: Consequences of a short time exposure to a sublethal dose of flupyradifurone (Sivanto) pesticide early in life on survival and immunity in the honeybee (Apis mellifera). Sci. Rep., 9, 19753. DOI: 10.1038/ s41598-019-56224-1. Search in Google Scholar

2. Alaux, C., Brunet, J.-L., Dussaubat, C., Mondet, F., Tchamitchan, S., Cousin, M., et al., 2010: Interactions between Nosema microspores and a neonicotinoid (imidacloprid) weaken honeybees (Apis mellifera). Environ. Microbiol., 12, 3, 774–782. DOI: 10.1111/j.1462-2920.2009.02123.x. Search in Google Scholar

3. Amdam, G. V., Omholt, W., 2003: The hive bee to forager transition in honeybee colonies: The double repressor hypothesis. J. Theor. Biol., 223, 4, 451–464. DOI: 10.1016/ s0022-5193(03)00121-8. Search in Google Scholar

4. Anderson, D., East, I. J., 2008: The latest buzz about colony collapse disorder. Science, 319 (5864), 724–725, DOI: 10.1126/science.319.5864.724c. Search in Google Scholar

5. Antúnez, K., Martín-Hernández, R., Prieto, L., Meana, A., Zunino, P., Higes, M., 2009: Immune-suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environ. Microbiol., 11, 9, 2284–2290. DOI: 10.1111/j.1462-2920.2009.01953.x. Search in Google Scholar

6. Applegate, J. R., Petritz, O. A, 2020: Common and emerging infectious diseases of honey bees (Apis mellifera). Vet. Clin. N. Am. Exot. Anim. Pract., 23, 285–297, DOI: 10.1016/j.cvex.2020.01.001. Search in Google Scholar

7. Ares, A. M., Nozal, M. J., Bernal, J. L., Martín-Hernández, R., Higes, M., Bernal, J., 2012: Liquid chromatography coupled to ion trap-tandem mass spectrometry to evaluate juvenile hormone III levels in bee hemolymph from Nosema spp. infected colonies. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 899, 146–153, DOI: 10.1016/j. jchromb.2012.05.016 10.1016/j.jchromb.2012.05.016. Search in Google Scholar

8. Bojko, J., Reinke, A. W., Stentiford, G. D., Williams, B., Rogers, M. S. J., Bass, D., 2022: Microsporidia: A new taxonomic, evolutionary, and ecological synthesis. Trends Parasitol., 38, 8, 642‒659. DOI: 10.1016/j.pt.2022.05.007. Search in Google Scholar

9. Botías, C., Martín-Hernández, R., Meana, A., Higes, M., 2010: Negative effects of nosema infection in honey pro duction and vitality of honey bee (Apis mellifera) colonies in Spain. EURBEE, 4th European Conference of Apidology. M. Kence, Ed., Ankara, Turkey. DOI: 10.1186/1297-9716-44-25. Search in Google Scholar

10. Brodschneider, R., Gray, A., Adjlane, N., Ballis, A., Brusbardis, V., Charrière, J. D., et al., 2018: Multi-country loss rates of honey bee colonies during winter 2016/2017 from the COLOSS survey. J. Apic. Res., 57, 452–457. DOI: 10.1080/00218839.2018.1460911. Search in Google Scholar

11. Castelli, L., Branchiccela, B., Garrido, M., Invernizzi, C., Porrini, M., Romero, H., et al., 2020: Impact of nutritional stress on honeybee gut microbiota, immunity and Nose-ma ceranae infection. Microb. Ecol., 80, 908–919. DOI: 10.1038/s41598-019-46453-9. Search in Google Scholar

12. Chemurot, M., De Smet, L., Brunain, M., De Rycke, R., de Graaf, D. C., 2017: Nosema neumanni n. sp. (Micro-sporidia, Nosematidae), a new microsporidian parasite of honeybees Apis mellifera in Uganda. Eur. J. Protistol., 61, 13–19. DOI: 10.1016/j.ejop.2017.07.002. Search in Google Scholar

13. Chen, Y. P., Huang, Z., 2010: Nosema ceranae a newly identified pathogen of Apis mellifera in the USA and Asia. Apidologie, 41, 364–374. DOI: 10.1051/apido/2010021. Search in Google Scholar

14. Chen, Y., Evans, J. D., Smith, I. B., Pettis, J. S., 2008: Nosema ceranae is a long-present and wide-spread micro-sporidian infection of the European honey bee (Apis mellifera) in the United States. J. Invert. Pathol., 97, 186–188. DOI: 10.1016/j.jip.2007.07.010. Search in Google Scholar

15. Chen, Y., Evans, J. D., Zhou, L., Boncristiani, H., Kimura, K., Xiao, T., et al., 2009: Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees. J. Invertebr. Pathol., 101, 204–209. DOI: 10.1016/j.jip.2009.05.012. Search in Google Scholar

16. Cilia, G., Cardaio, I., dos Santos, P. E. J., Ellis, J. D., Nanetti, A., 2018: The first detection of Nosema ceranae (Microsporidia) in the Small Hive beetle, Aethina tumida Murray (Coleoptera: Nitidulidae). Apidologie, 49, 619–624, DOI: 10.1007/s13592-018-0589-8. Search in Google Scholar

17. FAO – Food and Agriculture Organization of the United Nations, 2023: Available online at https://www.destatis.de/EN/Themes/Countries-Regions/International-Statistics/Data-Topic/AgricultureForestryFisheries/Bees.html. Accessed on 02.03.2023. Search in Google Scholar

18. de Figueiró Santos, J., Coelho, F. C., Bliman, P. A., 2016: Behavioral modulation of infestation by Varroa destructor in bee colonies. Implications for colony stability. PLOS ONE, 11, e0160465. DOI: 10.1371/journal.pone.0160465. Search in Google Scholar

19. Deplazes, P. J., Eckert, G., von Samson-Himmelstjerna, H., 2013: Lehrbuch der Parasitologie für die Tiermedizin, Stuttgart, Enke Verlag, 147‒148. Search in Google Scholar

20. Dittes, J., Schäfer, M. O., Aupperle-Lellbach, H., Mülling, C. K. W., Emmerich, I. U., 2020: Overt infection with chronic bee paralysis virus (CBPV) in two honey hee colonies. Vet. Sci., 7, 142. DOI: 10.3390/vetsci7030142. Search in Google Scholar

21. Down, R. E., Bell, H. A., Bryning, G., Kirkbride-Smith, A. E., Edwards, J. P., Weaver, R. J., 2008: Infection by the microsporidium Vairimorpha necatrix (Microspora: Microsporidia) elevates juvenile hormone titres in larvae of the tomato moth, Lacanobia oleracea (Lepidoptera: Noctuidae). J. Invertebr. Pathol., 97, 223–229. DOI: 10.1016/J.JIP.2007.10.003. Search in Google Scholar

22. Dussaubat, C., Maisonnasse, A., Alaux, C., Tchamitchan, S., Brunet, J. L., Plettener, E., et al., 2010: Nosema spp. infectation alters pheromone production in honey bee (Apis mellifera). J. Chem. Ecol., 36, 522–525. DOI: 10.1007/ s10886-010-9786-2. Search in Google Scholar

23. Emsen, B., Guzman-Novoa, E., Hamiduzzaman, M. M., Eccles, L., Lacey, B., Ruiz-Pérez, R. A., 2016: Higher prevalence and levels of Nosema ceranae than Nosema apis infections in Canadian honey bee colonies. Parasitol. Res., 115, 175–181. DOI: 10.1007/s00436-015-4733-3. Search in Google Scholar

24. Emsen, B., De la Mora, A., Lacey, B., Eccles, L., Kelly, P. G., Medina-Flores, C. A., et al., 2020: Seasonality of Nose-ma ceranae infections and their relationship with honey bee populations, food stores, and survivorship in a North American region. Vet. Sci., 7, 131, DOI: 10.3390/vetsci7030131. Search in Google Scholar

25. Erler, S., Lommatzsch, S., Lattorff, H. M. G., 2012: Comparative analysis of detection limits and specificity of molecular diagnostic markers for three pathogens (Microsporidia, Nosema spp.) in the key pollinators Apis mellifera and Bombus terrestris. Parasitol. Res., 110, 1403–1410. DOI: 10.1007/s00436-011-2640-9. Search in Google Scholar

26. FAOSTAT, 2021: Available online at https://www.fao.org/faostat/en/home. Accessed on Dec. 20, 2021. Search in Google Scholar

27. Ferroglio, E., Zanet, S., Peraldo, N., Tachis, E., Trisciuoglio, A., Laurino, D., 2013: Nosema ceranae has been infecting honey bees Apis mellifera in Italy since at least 1993. J. Apic. Res., 52, 60–61. DOI: 10.3896/IBRA.1.52.2.11. Search in Google Scholar

28. Flores, J. M., Gil-Lebrero, S., Gámiz, V., Rodríguez, M. I., Ortiz, M. A., Quiles, F. J., 2019: Effect of the climate change on honey bee colonies in a temperate mediterranean zone assessed through remote hive weight monitoring system in conjunction with exhaustive colonies assessment. Sci. Total Environ., 653, 1111–1119. DOI: 10.1016/j.scitotenv.2018.11.004. Search in Google Scholar

29. Forsgren, E., Fries, I., 2010: Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Vet. Parasitol., 170, 212–217. DOI: 10.1016/j. vetpar.2010.02.010. Search in Google Scholar

30. Fries, I., 2010: Nosema ceranae in European honey bees (Apis mellifera). J. Invertebr. Pathol., 103, S73–S79. DOI: 10.1016/j.jip.2009.06.017. Search in Google Scholar

31. Fries, I., 1993: Nosema apis a parasite in the honey-bee colony. Bee World, 74, 5‒19. DOI: 10.1080/0005772x.1993.11099149. Search in Google Scholar

32. Fries, I., Feng, F., da Silva, A., Slemenda, S. B., Pieniazek, N. J., 1996: Nosema ceranae n. sp. 386 (microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis ceranae (hymenoptera, Apidae). Eur. J. Protistol., 32, 356–365. DOI: 10.1016/S0932-4739(96)80059-9. Search in Google Scholar

33. Fries, I., Chauzat, M.-P., Chen, Y.-P., Doublet, V., Genersch, E., Gisder, S., et al., 2013: Standard methods for nosema research. J. Apic. Res., 52, 1–28. Search in Google Scholar

34. Galajda, R., Valenčáková, A., Sučik, M., Kandráčová, P., 2021: Nosema disease of European honey bees. J. Fungi, 7, 714. DOI: 10.3390/jof7090714. Search in Google Scholar

35. Gisder, S., Hedtke, K., Möckel, N., Frielitz, M. C., Linde, A., Genersch, E., 2010: Five-year cohort study of Nosema spp. in Germany: Does climate shape virulence and assertiveness of Nosema ceranae? Appl. Environ. Microbiol., 76, 3032–3038. DOI: 10.1128/AEM.03097-09. Search in Google Scholar

36. Gisder, S., Möckel, N., Linde, A., Genersch, E., 2011: A cell culture model for Nosema ceranae and Nosema apis allows new insights into the life cycle of these important honey bee-pathogenic microsporidia: Nosema spp. infection in cell culture. Environ. Microbiol., 13, 404–413. DOI: 10.1111/j.1462-2920.2010.02346.x. Search in Google Scholar

37. Gisder, S., Schüler, V., Horchler, L. L., Groth, D., Genersch, E., 2017: Long-term temporal trends of Nosema spp. infection prevalence in northeast Germany: Continuous spread of Nose-ma ceranae, an emerging pathogen of honey bees (Apis mellifera), but no general replacement of Nosema apis. Front. Cell. Infect. Microbiol., 7, 301. DOI: 10.3389/fcimb.2017.00301. Search in Google Scholar

38. Goblirsch, M., 2018: Nosema ceranae disease of the honey bee (Apis mellifera). Apidologie, 49, 131–150, DOI: 10.1007/s13592-017-0535-1. Search in Google Scholar

39. Higes, M., Meana, A., Bartolome, C., Botias, R., Martin-Hernandez, R., 2013: Nosema ceranae (microsporidia), a controversial 21st century honey bee pathogen. Env. Micro-biol. Rep., 5, 17–29. DOI: 10.1111/1758-2229.12024. Search in Google Scholar

40. Higes, M., García-Palencia, P., Martín-Hernández, R., Meana, A., 2007: Experimental infection of Apis mellifera honeybees with the microsporidia Nosema ceranae. J. Invertebr. Pathol., 94, 211–217. DOI: 10.1016/j.jip.2006.11.001. Search in Google Scholar

41. Higes, M., Martín, R., Meana, A., 2006: Nosema ceranae, a new microsporidian parasite in honey bees in Europe. J. Invert. Pathol., 92, 93–95. DOI: 10.1016/j.jip.2006.02.005. Search in Google Scholar

42. Higes, M., Martín-Hernández, R., Botías, C., Bailón, E. G., González-Porto, A. V., Barrios, L., et al., 2008: How natural infection by Nosema ceranae causes honey bee colony collapse. Environ. Microbiol., 10, 2659–2669. DOI: 10.1111/j.1462-2920.2008.01687.x. Search in Google Scholar

43. Higes, M., Martín-Hernández, R., Martínez-Salvador, A., Garrido-Bailón, E., González-Porto, A. V., et al., 2010: Preliminary study of the epidemiological factors related to honey bee colony loss in Spain. Environ. Microbiol. Rep., 2, 243–250. DOI: 10.1111/j.1758-2229.2009.00099.x. Search in Google Scholar

44. Huang, W. F., Jiang, J. H., Chen, Y. W., Wang, C. H. A., 2007: Nosema ceranae isolate from the honey bee Apis mellifera. Apidologie, 38, 30–37. Search in Google Scholar

45. Hurná, B., Valenčáková, A., Sučik, M., Staroň, M., Maková, Z., Galajda, R., 2022: The incidence of Nosema spp. in the honey bee colonies in Slovakia during 2021. 15th Int. Congress of Parasitology ‒ ICOPA 2022, Copenhagen, Denmark. Available at https://icopa2022.org/. Search in Google Scholar

46. Khoury, D. S., Myerscough, M. R., Barron, A. B., 2011: A quantitative model of honey bee colony population dynamics. PLOS ONE, 6, e18491. DOI: 10.1371/journal.pone.0018491. Search in Google Scholar

47. Klee, J., Besana, A. M., Genersch, E., Gisder, S., Nanetti, A., Tam, D. Q., et al., 2007: Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J. Invertebr. Pathol., 96, 1–10. DOI: 10.1016/j.jip.2007.02.014. Search in Google Scholar

48. Klein, A. M., Vaissière, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C., et al., 2007: Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B Biol. Sci., 274, 303–313. DOI: 10.1098/rspb.2006.3721. Search in Google Scholar

49. Wadi, L., Reinke, A. W., 2020: Evolution of microsporidia: An extremely successful group of eukaryotic intracellular parasites. PLOS Pathog., 16, e1008276, DOI: 10.1371/journal.ppat.1008276. Search in Google Scholar

50. Lannutti, L., Gonzales, F. N., Dus Santos, M. J., Florin-Christensen, M., Schnittger, L., 2022: Molecular detection and differentiation of arthropod, fungal, protozoan, bacterial and viral pathogens of honey bees. Vet. Sci., 9, 221. DOI: 10.3390/vetsci9050221. Search in Google Scholar

51. Lannutti, L., Mira, A., Basualdo, M., Rodriguez, G., Erler, S., Silva, V., et al., 2020: Development of a loop-mediated isothermal amplification (LAMP) and a direct LAMP for the specific detection of Nosema ceranae, a parasite of honey bees. Parasitol. Res., 119, 3947–3956. DOI: 10.1007/ s00436-020-06915-w. Search in Google Scholar

52. Marín-García, P. J., Peyre, Y., Ahuir-Baraja, A. E., Garijo, M. M., Llobat, L., 2022: The role of Nosema ceranae (microsporidia: Nosematidae) in honey bee colony losses and current insights on treatment. Vet. Sci., 9, 130. DOI: 10.3390/vetsci9030130. Search in Google Scholar

53. Martin-Hernandez, R., Botias, C., Bailon, E. G., Martinez-Salvador, A., Prieto, L., Meana, A., et al., 2012: Microsporidia infecting Apis mellifera: Coexistence or competition. Is Nosema ceranae replacing Nosema apis? Environ. Microbiol., 14, 2127–2138. DOI: 10.1111/j.1462-2920.2011.02645.x Search in Google Scholar

54. Martin-Hernandez, R., Meana, A., Garcia-Palencia, P., Marin, P., Botias, C., Garrido-Bailon, E., et al., 2009: Effect of temperature on the biotic potential of honeybee microsporidia. Appl. Environ. Microbiol., 75, 2554–2557. DOI: 10.1128/AEM.02908-08. Search in Google Scholar

55. Martín-Hernández, R., Meana, A., Prieto, L., Salvador, A. M., Garrido-Bailón, E., Higes, M., 2007: Outcome of colonization of Apis mellifera by Nosema ceranae. Appl. Environ. Microbiol., 73, 6331–6338. DOI: 10.1128/AEM.00270-07. Search in Google Scholar

56. Mehlhorn, H., 2008: Nosema apis. Encyclopedia of Parasitology. Springer Verlag, Berlin, Heidelberg, 1021‒1021. Search in Google Scholar

57. Milbrath, M. O., Van Tran, T., Huang, W. F., Solter, L. F., Tarpy, D. R., Lawrence, F., et al., 2015: Comparative virulence and competition between Nosema apis and Nosema ceranae in honey bees (Apis mellifera). J. Invertebr. Pathol., 125, 9–15. DOI: 10.1016/j.jip.2014.12.006. Search in Google Scholar

58. Natsopoulou, M. E., McMahon, D. P., Doublet, V., Bryden, J., Paxton, R. J., 2015: Interspecific competition in honey bee intracellular gut parasites is asymmetric and favours the spread of an emerging infectious disease. Proc. R. Soc. B, 282, 20141896. DOI: 10.1098/rspb.2014.1896. Search in Google Scholar

59. Özkırım, A., Schiesser, A., Keskin, N., 2019: Dynamics of Nosema apis and Nosema ceranae co-infection seasonally in honey bee (Apis mellifera L.) colonies, J. Apic. Sci., 63, 1. DOI: 10.2478/JAS-2019-0001. Search in Google Scholar

60. Paxton, R. J., Klee, J., Korpela, S., Fries, I., 2007: Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie, 38, 558‒565. DOI: 10.1051/apido:2007037. Search in Google Scholar

61. Retschnig, G., Williams, G. R., Schneeberger, A., Neumann, P., 2017: Cold ambient temperature promotes Nosema spp. intensity in honey bees (Apis mellifera). Insects, 8, 20. DOI: 10.3390/insects8010020. Search in Google Scholar

62. Roberts, K. E., Evison, S. E. F., Baer, B., Hughes, W.O. H., 2015: The cost of promiscuity: sexual transmission of nosema microsporidian parasites in polyandrous honey bees. Sci. Rep., 5, 10982. DOI: 10.1038/srep36649. Search in Google Scholar

63. Schmid-Hempel, P., Wolf, R. J., 1988: Foraging effort and life span in workers of social insects. J. Anim. Ecol., 57, 509–522. DOI: 10.2307/4921. Search in Google Scholar

64. Seeley, T. D., 2016: Honeybee Ecology: A study of Adaptation in Social Life. Princeton, USA, Princeton Legacy Library, 214 pp. Search in Google Scholar

65. Snow, J. W., 2022: Nosema apis and N. ceranae infection in honey bees: A model for host-pathogen interactions in insects. Weis, L. M., Reinke, A. W.: Microsporidia, Experientia Supplementum, 114. DOI: 10.1007/978-3-030-93306-7_7. Search in Google Scholar

66. Snow, J. W., Ceylan Koydemir, H., Karinca, D. K., Liang, K., Tseng, D., Ozcan, A., 2019: Rapid imaging, detection, and quantification of Nosema ceranae spores in honey bees using mobile phone-based fluorescence microscopy. Lab on a Chip, 19, 789–797. DOI: 10.1039/c8lc01342j. Search in Google Scholar

67. Staroň, M., Jurovčíková, J., Čermáková, T., Staroňová, D., 2012: Scientific note on incidence of Nosema apis and Nosema ceranae in Slovakia during the years 2009 and 2010. Slovak J. Anim. Sci., 45, 1, 36‒38. Search in Google Scholar

68. Staroň, M., 2009: Nosematosis, IInd part, Nosema apis vs. Nosema ceranae (In Slovak). Včelár, 83, 11, 162‒163. Search in Google Scholar

69. Stentiford, G. G. D., Becnel, J. J., Weiss, L. M., Keeling, P. J., Didier, E. S., Williams, B. A. P., et al., 2016: Microsporidia – emergent pathogens in the global food chain. Trends Parasitol., 32, 336‒348. DOI: 10.1016/j. pt.2015.12.004. Search in Google Scholar

70. Terrestrial Manual of the OIE, 2018: Chapter 3.02.04, Nosemosis 2018, Terrestrial Animal Health Code ‒ Contents (oie.int), 745‒746. Search in Google Scholar

71. Tokarev, Y. S., Zinatullina, Z. Y., Ignatieva, A. N., Zhigileva, O. N., Malysh, J. M., Sokolova, Y. Y., 2018: Detection of two microsporidia pathogens of the European honey bee Apis mellifera (Insecta: Apidae) in western Siberia. Acta Parasitol., 63, 4, 728–732. 10.1515/ap-2018-0086. Search in Google Scholar

72. Tokarev, Y. S., Huang, W.-F., Solter, L. F., Malysh, J. M., Becnel, J. J., Vossbrinck, C. R., 2020: A formal redefinition of the genera Nosema and Vairimorpha (microsporidia: Nosematidae) and reassignment of species based on molecular phylogenetics. J. Invert. Pathol., 169, 107279, DOI: 10.1016/j.jip.2019.107279. Search in Google Scholar

73. Wang, D. I., Moeller, F. E., 1970: The division of labor and queen attendance behaviour of nosema infected worker honey bees. J. Econ. Entomol., 63, 1539–1541, DOI: 10.1093/ JEE/63.5.1539. Search in Google Scholar

74. Williams, G. R., Shafer, A. B. A., Rogers, R. E. L., Shutler, D., Stewart, D. T., 2008: First detection of Nosema ceranae, a microsporidian parasite of European honey bees (Apis mellifera), in Canada and central USA. J. Invertebr. Pathol., 97, 189–192. DOI: 10.1016/j.jip.2007.08.005. Search in Google Scholar

75. Williams, G. R., Shutler, D., Burgher-Maclellan, K. L., Rogers, R. E. L., 2014: Infra-population and community dynamics of the parasites Nosema apis and Nosema ceranae, and consequences for honey bee (Apis mellifera) hosts. PLOS ONE, 9, e99465. DOI: 10.1371/journal.pone.00 99465. Search in Google Scholar

76. Zander, E., 1909: Tierische Parasiten als Krankenheitserreger bei der Biene. Leipz. Bienenztg., 24, 147–150, 164–166. Search in Google Scholar

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