Nosema ceranae (Microsporidia: Nosematidae) Does Not Cause Collapse of Colonies of Africanized Apis mellifera (Hymenoptera: Apidae) in Tropical Climate


  • Lubiane Guimarães-Cestaro Federal University of Viçosa
  • T. S. Maia Universidade de Taubaté
  • Renata Martins Universidade de Taubaté
  • Maria Luísa Teles M. F. Alves Biological Institute/APTA/SAA
  • Ivani Pozar Otsuk Institute of Animal Science/APTA/SAA
  • Dejair Message Federal Rural University of the Semiarid
  • Erika Weinstein Teixeira Biological Institute/APTA/SAA



fungus, nosemosis, microsporidium.


Nosemosis is an important disease that affects honey bees (Apis mellifera Lineu), caused by obligate intracellular parasites, Nosema  apis  and/or  Nosema  ceranae. Since the initial detection of N. ceranae in A. mellifera coincided with recent large-scale losses of bee colonies worldwide, the impacts of this parasite under field conditions are of great interest. Here we test two hypotheses, the first one, whether the climatic variables (temperature, air humidity and precipitation) influence the intensity of infection of the microsporidium Nosema spp. in Africanized honey bees (Apis mellifera), and the second, whether the local of hive installation (outdoor or roofed) influences the intensity of infection of these spores in Africanized honey bees. Between August 2013 and August 2016, samples of Africanized bees were collected weekly from 20 colonies, of which ten were located in an open area (outdoor apiary) and ten under a roof on a concrete floor (roofed apiary). N.  ceranae was the only species present. The type of apiary did not influence (p > 0.05) the number of spores of N. ceranae in Africanized bees. However, the infection intensities of the roofed apiary colonies were lower in the autumn. Regarding the meteorological parameters, there was a negative correlation between the winter infection intensities and the minimum temperature in the roofed apiary and the humidity in the outdoor apiary. The highest infection intensities occurred in both apiaries in the spring and summer, which may be related to higher pollen production. On average, the infection intensity was 16.19 ± 15.81 x 105, ranging from zero to 100.5 x105, and there were no records of collapse during the three years.


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Alaux, C., Folschweiller, M., Mcdonnell, C., Beslay, D., Cousin, M., Dussaubat, C., Brunet, J. L. & Le Conte,Y. (2011). Pathological effects of the microsporidium Nosema ceranae on honey bee queen physiology (Apis mellifera). Journal of Invertebrate Pathology, 106: 380–385. doi: 10.1016/j.jip.2010.12.005

Antúnez K., Martín-Hernandez, R., Prieto, L., Meana, A., Zunino, P. & Higes, M. (2009). Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environmental Microbiology, 11: 2284–2290. doi: 10.1111/j.1462-2920.2009.01953.x

Botías, C., Martín-Hernández, R., Barrios, L., Meana, A. & Higes, M. (2013). Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Veterinary Research, 44: 1–14. doi: 10.1186/1297-9716-44-25

Cantwell, G. R. (1970). Standard methods for counting Nosema spores. American Bee Journal, 110: 222-223.

Chen, Y., Evans, J. D., Smith, I. B. & Pettis, J. S. (2008). Nosema ceranae is a long-present and wide-spread microsporidean infection of the European honey bee (Apis mellifera) in the United States. Journal of Invertebrate Pathology, 97: 186–188. doi: 10.1016/j.jip.2007.07.010

Chen, Y. W., Chung, W. P., Wang, C. H, Solter, L. F. & Huang W. F. (2012). Nosema ceranae infection intensity highly correlates with temperature. Journal of Invertebrate Pathology, 111: 264-267. doi 10.1016/j.jip.2012.08.014

Cilia, G., Sagona, S., Giusti, M., Santos, P. E. J., Nanetti, A. & Felicioli, A. (2018). Nosema ceranae infection in honeybee samples from Tuscanian Archipelago (Central Italy) investigated by two qPCR methods. Saudi Journal of Biological Sciences. doi: 10.1016/j.sjbs.2018.11.017

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., Martinson, V., Van Engelsdorp, D., Kalkstein, A. L., Drysdale, A., Hui, J., Zhai, J., Cui, L., Hutchison, S. K., Simons, J. F., Egholm, M., Pettis, J. S. & Lipkin, W. I. (2007). A metagenomic survey of microbes in honey bee colony collapse disorder. Science, 318: 283-287. doi: 10.1126/science.1146498

Dussaubat, C., Brunet, J. L., Higes, M., Colbourne, J. K. & Lopez J. (2012). Gut pathology and responses to the microsporidium Nosema ceranae in the Honey bee Apis mellifera. Plos One 7: e37017. doi: 10.1371/journal.pone.0037017

Eiri, D. M., Suwannapong, G., Endler, M. & Nieh, J. C. (2015). Nosema ceranae can infect honey bee larvae and reduces subsequent adult longevity. Plos One, 10:e0126330. doi: 10.1371/journal.pone.0126330

Emsen, B., Guzman-Novoa, E., Hamiduzzaman, M. M., Eccles, L., Lacey, B., Ruiz-Pérez, R. A. & Nasr, M. (2016). Higher prevalence and levels of Nosema ceranae than Nosema apis infections in Canadian honey bee colonies. Parasitology Research, 115: 175-181. doi: 10.1007/s00436-015-4733-3

Ferroglio, E., Zanet, S., Peraldo, N., Tachis, E., Trisciuoglio, A., Laurino, D. & Porporato, M. (2013). Nosema ceranae has been infecting honey bees Apis mellifera in Italy since at least 1993. Journal of Apicultural Research, 52: 60–61. doi: 10.3896/IBRA.

Fleites-Ayil, F. A., Quezada-Euán J. G. & Medina-Medina, L. A., (2018). Onset of foraging and lifespan of Africanized honey bees (Apis mellifera) infected with different levels of Nosema ceranae spores in Neotropical Mexico. Apidologie, 49: 781-788. doi: 10.1007/s13592-018-0602-2

Fries, I, Feng, F., Silva, A., Slemenda, S. B. & Pieniazek, N. J. (1996). Nosema ceranae sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). European Journal of Protistology, 32: 356–365. doi: 10.1016/S0932-4739(96)80059-9

Fries, I., Martín, R., Meana A., García-Palencia, P. & Higes, M. (2006). Natural infections of Nosema ceranae in European honey bees. Journal of Apicultural Research, 45: 230-233. doi: 10.3896/IBRA.

Fries, I. (2010). Nosema ceranae in European honey bees (Apis mellifera). Journal of Apicultural Research, 103:573-579. doi: 10.1016/j.jip.2009.06.017

Fries, I., Chauzat, M. P., Chen, Y., Doublet, V., Genersch, E., Gisder, S., Higes, M., McMahon, D. P., Martín-Hernández, R., Natsopoulou, M., Paxton, R. J., Tanner, G., Webster, T. C. & Williams, G. R. (2013). Standart methods for Nosema research. Journal of Apicultural Research, 52: 1 –28. doi: 10.3896/IBRA.

Gisder, S., Hedtke, K., Mockel, 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? Applied and Environmental Microbiology, 76- 3032–3038. doi: 10.1128/AEM.03097-09

Gisder, S., Schüle, V., Horchler, L. L. Groth, D. & Genersch, E. (2017). Long-term temporal trends of Nosema spp. infection prevalence innortheast germany: continuousspread of Nosema ceranae, an emerging pathogen of honey bees (Apis mellifera), but no general replacement of Nosema apis. Frontiers in Cellular and Infection Microbiology, 7: 1-14. doi:10.3389/fcimb.2017.00301

Guerrero-Molina, C., Correa-Benítez, A., Hamiduzzaman, M. M. & Guzman-Novoa, E. (2016). Nosema ceranae is an old resident of honey bee (Apis mellifera) colonies in Mexico, causing infection levels of one million spores per bee or higher during summer and fall. Journal of Invertebrate Pathology, 141:38-40. doi: 10.1016/j.jip.2016.11.001

Guimarães-Cestaro, L., Serrão, J. E., Message, D., Martins, M. F. & Teixeira, E. W. (2016). Simultaneous detection of Nosema spp., Ascosphaera apis and Paenibacillus larvae in honey bee products. Journal of Hymenoptera Research, 49: 43–50. doi: 10.3897/JHR.49.7061

Guimarães-Cestaro, L, Alves, M. L. T. M. F., Message, D, Silva, M. V. G. B. & Teixeira, E. W. (2017a). A scientific note on occurrence of pathogens in colonies of honey bee Apis mellifera in Vale do Ribeira, Brazil. Apidologie , 48: 384–386. doi: 10.1007/s13592-016-0481-3

Guimarães-Cestaro, L., Alves, M. L. T. M. F., Message, D. Silva, M. V. G. B & Teixeira, E. W. (2017b). Honey bee (Apis mellifera) health in stationary and migratory apiaries. Sociobiology, 64: 42-49. doi: 10.13102/sociobiology.v64i1.1183

Guzman-Novoa, E., Hamiduzzaman, M. M., Arechavaleta-Velasco, M. E., Koleoglu, G., Valizadeh, P. & Correa-Benítez, A. (2011). Nosema ceranae has parasitized Africanized honey bees in Mexico since at least 2004. Journal of Apicultural Research, 50: 167–169. doi: 10.3896/IBRA.

Higes, M., Martín, R. & Meana, A. (2006). Nosema ceranae, a new microsporidian parasite in honeybees in Europe. Journal of Invertebrate Pathology, 92: 93–95. doi: 10.1016/j.jip.2006.02.005

Higes, M., Martín-Hernandez, R., Botías, C., Garrido-Bail, O. E., Gonzalez-Porto, A. V. & Barrios L (2008). How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental microbiology,10: 2659 – 2669. doi: 10.1111/j.1462-2920.2008.01687.x

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. (2009). Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environmental Microbiology Reports, 1: 110–113. doi: 10.1111/j.1758-2229.2009.00014.x

Higes, M., Martín-Hernández, R., Garrido-Bailón, E., González-Porto, A. V., Meana & A, Bernal, J. L. (2010a). A preliminary study of the epidemiological factors related to honey bee colony loss in Spain. Environmental Microbiology Reports, 2: 243–250. doi: 10.1111/j.1758-2229.2009.00099.x

Higes, M., Matin-Hemandez, R. & Meana, A. (2010b). Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie, 41:375-392. doi: 10.1051/apido/2010019

Huang, W. F., Jiang, J. H., Chen, Y.W. & Wang, C. H. (2007). A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie, 38: 30–37. doi: 10.1051/apido/2010019

Invernizzi, C., Abud, C., Tomasco, I. H., Harriet, J. Ramallo, G., Campá, J., Katz, H., Gardiol, G. & Mendoza, Y. (2009). Presence of Nosema ceranae in honeybees (Apis mellifera) in Uruguay. Journal of Invertebrate Pathology, 101: 150 –153. doi: 10.1016/j.jip.2009.03.006

Klee, J., Besana, A. M., Genersch, E., Gisder, S., Nanetti, A., Tam, D. Q., Chinh, T. X., Puerta, F., Ruz, J. M., Kryger, P., Message, D., Hatjina, F., Korpela, S., Fries, I. & Paxton, R. J. (2007). Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. Journal of Invertebrate Pathology, 96: 1-10. doi: 10.1016/j.jip.2007.02.014

Lecocq, A., Jensen, A. B., Kryger, P. & Nieh, J. C. (2016). Parasite infection accelerates age polyethism in young honey bees. Scientific Reports, 6: 22042. doi: 10.1038/srep22042

Martín-Hernandez, R., Botías, C., Barrios, L., Martínez-Salvador, A., Meana, A., Mayack, C. & Higes, M. (2011). Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honeybees (Apis mellifera). Parasitology Research, 109: 605-612. doi: 10.1007/s00436-011-2292-9

Martín-Hernández, R., Meana, A., García-Palencia, P., Marrin, P., Botías, C., Garrido-Bailón, E., Barrios, L. & Higes, M. (2009). Temperature effect on biotic potencial of honey bee microsporidia. Applied and Environmental Microbiology, 75: 2554-2557. doi: 10.1128/AEM.02908-08

Martín-Hernández, R., Bartolome, C., Chejanovsky, N., Le Conte, Y., Dalmon, A., Dussaubat, C., Dussaubat, C., Meana, A. Pinto, M., Soroker, V. & Higes, M. (2018). Nosema ceranae in Apis mellifera: a 12 years post-detection perspective: Nosema ceranae in Apis mellifera. Environmental Microbiology, 20: 1302–1329. doi:10.1111/1462-2920.14103

Mayack, C. & Naug, D. (2009). Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. Journal of Invertebrate Pathology, 100: 185–188. doi: 10.1016/j.jip.2008.12.001

Özkırım, A., Schiesser, A. & Keskin, N. (2019). Dynamics of Nosema apis and Nosema ceranae co-infection seasonally in honey bee (Apis mellifera L.) colonies. Journal of Apicultural Science, 63. doi: 10.2478/jas-2019-0001

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

Pires, C. S. S., Pereira, F. M., Lopes, M. T. R., Ferreira, R. C. N., Malaspina, O., Pettis , J. S. & Teixeira, E. W. (2016) Enfraquecimento e perda de colônias de abelhas no Brasil: há casos de CCD? Pesquisa Agropecuaria Brasileira, 51: 422-442. doi: 10.1590/S0100-204X2016000500003

Santos, L. G., Alves, M. L. T. M. F., Message, D., Pinto, F. A., Silva, M. V. G. B. & Teixeira, E. W. (2014). Honey bee health in apiaries in the Vale do Paraíba, São Paulo state, southeastern Brazil. Sociobiology, 61: 307-312. doi:10.13102/sociobiology.v61i3.307-312

SAS (1990). SAS/STAT user’s guide version, 6, 4. Cary.

Silva, R. M. B., Moreti, A. C. C. C., Silva, E. C. A. & Alves, M. L. T. M. F. (1995). Fluxo nectarífero na região de Pindamonhangaba, SP. Períodos de secreção. Boletim da Industria Animal, 52: 23-28.

Simeunovic, P., Stevanovic, J., Cirkovic, D., Radojicic, S., Lakic, N., Stanisic, L. & Stanimirovic, Z. (2014). Nosema ceranae and queen age influence the reproduction and productivity of the honey bee colony. Journal of Apicultural Research, 53: 545-554. doi: 10.3896/IBRA.

Schwarz, R. S., Teixeira, E. W., Tauber, J. P., Birke, J. M., Martins, M. F., Fonseca, I. & Evans, J. D. (2014). Honey bee coolies act as reservoirs for two Spiroplasma facultative symbionts, and incur complex, multiyear infection dynamics. Microbiology Open. 3. doi: 10.1002/mbo3.172

Sulborska, A., Horecka, B., Cebrat, M., Kowalczyk, M., Skrzypek, T. H., Kazimierczak, W., Trytek, M., Borsuk, G. (2019). Microsporidia Nosema spp. – obligate bee parasites are transmitted by air. Sci. Rep. 9:14376. doi: 10.1038/s41598-019-50974-8

Teixeira, E. W., Chen, Y., Message, D., Pettis, J. S. & Evans, J. D. (2008a). Virus infection in Brazilian honey bees. Journal of Invertebrate Pathology, 99: 117‑119. doi: 10.1016/j.jip.2008.03.014

Teixeira, E. W., Message, D., Chen, Y., Pettis, J. S. & Evans, J. D. (2008b). First metagenomic analysis of microorganisms in honey bees from Brazil. Boletim da Industria Animal, 65: 355‑361.

Teixeira, E. W. & Message, D. (2010). Abelhas Apis mellifera. In: Manual veterinário de colheita e envio de amostras: manual técnico. Cooperação técnica MAPA/OPAS-PANAFTOSA. Editora Horizonte. São Paulo.

Teixeira, E. W., Chen, Y., Message, D., Pettis, J & Evans, J. D., Bonscristiani, H. F., Pettis, J. S. & Evans, J. D. (2012) Israeli acute paralysis virus in Africanized honey bees in southeastern Brazilian apiaries. Journal of Apicultural Research, 51: 282-284. doi: 10.3896/IBRA.

Teixeira, E. W., Santos, L. G., Sattler, A., Message, D., Alves, M. L. T. M. F., Martins, M. F., Grassi-Sella, M. F. & Francoy, T. M. (2013). Nosema ceranae has been present in Brazil for more than three decades infecting Africanized honey bees. Journal of Invertebrate Pathology, 114: 250-254. doi: 10.1016/j. jip.2013.19.002.

Teixeira, E. W., Guimarães-Cestaro, L., Alves, M. L. T. M. F., Message, D., Martins, M. F., Luz, C. F. P. & Serrão, J. E. (2018). Spores of Paenibacillus larvae, Ascosphaera apis, Nosema ceranae and Nosema apis in bee products supervised by the Brazilian Federal Inspection Service. Revista Brasileira de Entomologia, 62: 188-194. doi: 10.1016/j.rbe.2018.04.001

Traver, B. E. & Fell, R. D. (2015). A scientific note: Survey for Nosema spp. in preserved Apis spp. Apidologie, 46: 194–196. doi:10.1007/s13592-014-0306-1

Winston, M. L. (1987). The Biology of the Honey Bee. Cambridge, Harvard University Press.

Zheng, H. Q., Lin, Z. G., Huang S. K., Sohr, A. & Chen Y. (2014) Spore loads may not be used alone as a direct indicator of the severity of Nosema ceranae infection in honey bees Apis mellifera (Hymenoptera: Apidae). Journal of Economic Entomology 107: 2037-2014. doi: 10.1603/EC13520




How to Cite

Guimarães-Cestaro, L., Maia, T. S., Martins, R., Alves, M. L. T. M. F., Otsuk, I. P., Message, D., & Teixeira, E. W. (2020). Nosema ceranae (Microsporidia: Nosematidae) Does Not Cause Collapse of Colonies of Africanized Apis mellifera (Hymenoptera: Apidae) in Tropical Climate. Sociobiology, 67(3), 408–416.



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