Honey Bee (Apis mellifera) Health in Stationary and Migratory Apiaries


  • Lubiane Guimarães Cestaro Federal University of Viçosa
  • Maria Luisa Teles Marques Florêncio Alves São Paulo State Agribusiness Technology Agency
  • Dejair Message Federal Rural University of the Semiarid
  • Marcos Vinícius Gualberdo Barbosa Silva Embrapa Dairy Cattle
  • Érica Weinstein Teixeira São Paulo State Agribusiness Technology Agency




Honey bee health, Apis mellifera, Varroa destructor, Nosema spp., Paenibacillus larvae.


The practice of migratory beekeeping is based on moving honey bee (Apis mellifera) colonies between different locations to intensify agricultural production through improved pollination services. However, due to stress caused by exposure of bee hives to different environments, migratory beekeeping activities can lead colonies to greater susceptibility of these insects to pathogens and pests, thus leading to population decline and mortality. The aim of this study was to evaluate the health profile of apiaries that adopt two types of management (stationary and migratory), located in the central-eastern region of São Paulo state, Brazil, during two sampling periods, one in spring (October 2010), and one in autumn (May 2011). We collected 474 samples of honeycomb from the brood area, combs containing capped brood, adult bees that covered the brood area, and foraging bees, to evaluate the presence and prevalence of Paenibacillus larvae, Varroa destructor, Nosema apis and N. ceranae. Seasonality was identified as a determining factor in the health condition of Africanized A. mellifera colonies, causing a stronger effect on health than the type of management employed (stationary vs migratory beekeeping). The infection rates of N. ceranae were higher during the autumn in relation to the spring (387 ± 554 spores per bee in the spring and 1,167 ± 1,202 spores per bee in the autumn in stationary apiaries and 361 ± 687 spores per bee in the spring and 1,082 ± 1,277 spores per bee in the autumn in migratory apiaries). The same pattern was found for infestation rates of V. destructor (2.83 ± 1.97 in the spring and 9.48 ± 6.15 in the autumn in stationary apiaries and 3.25 ± 2.32 in the spring and 6.34 ± 6.58 in the autumn in migratory apiaries). These results demonstrate that the seasonality affects the health of A. mellifera colonies, but it does not depend on the type of management adopted (stationary or migratory).


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Author Biographies

Lubiane Guimarães Cestaro, Federal University of Viçosa


Maria Luisa Teles Marques Florêncio Alves, São Paulo State Agribusiness Technology Agency


Dejair Message, Federal Rural University of the Semiarid

Animal Sciences

Marcos Vinícius Gualberdo Barbosa Silva, Embrapa Dairy Cattle

Bioinformatics and Animal Genomics

Érica Weinstein Teixeira, São Paulo State Agribusiness Technology Agency



Anderson, D. L., Trueman, J. W. H. (2000). Varroa jacobsoni (Acari: Varroidae) is more than one species. Experimental and Applied Acarology, 24(3): 165-189. doi: 10.1023/A:1006456720416.

Bacandritsos, N., Granato, A., Budge, G., Papanatasiou, I., Roinioti, E., Caldon, M., Falcaro, C., Gallina, A., Mutinelli, F. (2010). Sudden deaths and colony population decline in Greek honey bee colonies. Journal of Invertebrate Pathology, 105(3): 335-340. doi:10.1016/j.jip.2010.08.004.

Bailey, L., & Ball, B. V. (1991). Honey Bee Pathology. London: Academic Press. 193p.

Brasil. (2003). Ministério da Agricultura e do Abastecimento. Instrução Normativa n.° 62, de 26 de agosto de 2003. Métodos Analíticos Oficiais para Análises Microbiológicas para Controle de Produtos de Origem Animal. Anexo, Capítulo XIX Pesquisa de Paenibacillus larvae subsp. larvae. Diário Oficial da União, 18/09/2003.

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

Carneiro, F. E., Barros, G. V., Strapazzon, R., Moretto, G. (2014). Reproductive ability and level of infestation of the Varroa destructor mite in Apis mellifera apiaries in Blumenau, State of Santa Catarina, Brazil. Acta Scientiarum, 36(1): 109-112. doi:10.4025/actascibiolsci.v36i1.20366.

Corrêa-Marques, M. H., Medina, L. M., Martin, S. J., De Jong, D. (2003). Comparing data on the reproduction of Varroa destructor. Genetics and Molecular Research, 2(1): 1-6.

De Jong, D. & Soares, A. E. E. (1997). An isolated population of Italian bees that has survived Varroa jacobsoni infestation without treatment for over 12 years. American Bee Journal, 137(10): 742-745.

De Jong, D., Gonçalves, L. S. (1998). The africanized bees of Brazil have become tolerant to Varroa. Apiacta, 33: 65-70.

De Jong, D., Roma, D. A., Gonçalves, L.S. (1982). A comparative analysis of shaking solutions for the detection of Varroa jacobsoni on adult honey bees. Apidologie, 13(3): 297-306.

Dietemann, V., Nazzi, F., Martin, S., Anderson, D. L., Locke, B., Delaplnae, K. S., Wauquiez, Q., Tannahill, C., Frey, E., Ziegelmann, B., Rosenkranz, P., Ellis, J. D. (2013). Standard methods for Varroa research. Journal of Apicultural Research, 52(1). doi:10.3896/IBRA.

Dooremalen, C., Gerritsen, L., Cornelissen, B., Steen, J. J. M., Langeveld, F., Blacquie, T. (2012). Winter Survival of Individual Honey Bees and Honey Bee Colonies Depends on Level of Varroa destructor Infestation. Plos One, 7(4): e36285. doi:10.1371/journal.pone.0036285.

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(5): e0126330.


Fries I. (2010). Nosema ceranae in European honey bees (Apis mellifera). Journal of Invertebrate Pathology, 103(1): 573-579. doi:10.1016/j.jip.2009.06.017.

Funfhaus, A., Poppinga, L., Genersch, E. (2013). Identification and characterization of two novel toxins expressed by the lethal honey bee pathogen Paenibacillus larvae, the causative agent of American foulbrood. Environmental Microbiology, 15: 2951-2965. doi:10.1111/1462-2920.12229.

Genersch, E. (2008). Paenibacillus larvae and American foulbrood – long since known and still surprising. Journal für Verbraucherschutz und Lebensmittelsicherheit. 3(4): 429-434. doi:10.1007/s00003-008-0379-8.

Genersch, E. (2010). American foulbrood in honey bees and its causative agent, Paenibacillus larvae. Journal of Invertebrate Pathology, 103: S3-S19. doi:10.1016/j.jip.2009.06.015.

Guimarães-Cestaro, L., Serrão, J. E., Message, D., Martins, M. F., Teixeira, E. W. (2016). Simultaneuos 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.

Higes, M., García-Palencia, P., Martín-Hernández, R., Botías, C., Garrido-Bailón, E., González-Porto, A. V., Barrios, L., Del Nozal, M. J., Berna, J. L., Jiménez, J. J., Palencia, P. G., Meana, A. (2008). How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental Microbiology, 10(10): 2659-2669. doi:10.1111/j.1462-2920.2008.01687.x.

Higes, M., Martín-Hernandez, R., Meana, A. (2010). Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie, 41(3): 375-392. doi:10.1051/apido/2010019.

Junkes, L., Guerra-Júnior, J. C. V., Moretto, G. (2007). Varroa destructor mite mortality rate according to the amount of worker broods in africanized honey bee (Apis mellifera L.) colonies. Acta Scientiarum, 29(3): 305-308.

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): 1-10. doi:10.1016/j.jip.2007.02.014.

Le Conte, Y., Marion, E., Wolfgang, R. Varroa mites and honey bee health: can Varroa

explain part of the colony losses? Apidologie, 41(3): 353–363. doi:10.1051/apido/2010017.

Locke, B., Forsgren, E., Miranda, J. (2014). Increased Tolerance and Resistance to Virus Infections: A Possible Factor in the Survival of Varroa destructor - Resistant Honey Bees (Apis mellifera). PlosOne, 9(6): e99998. doi:10.1371/journal.pone.0099998.

MAPA. Nota técnica DSA nº52/2006. Ocorrência de “Cria Pútrida Americana” no município de Quatro Barras, estado do Paraná-Brasil. Ministry of Agriculture of Brasil, Brasília, 2006.

Martin, S. J. (1994). Ontogenesis of the mite Varroa jacobsoni Oud. in worker brood of the honeybee Apis mellifera L. under natural conditions. Experimental and Applied Acarology, 18(2): 87–100.

Martin, S. J. (2001). The role of Varroa and viral pathogens in the collapse of honeybee colonies: a modeling approach. Journal Applied Ecology, 38(5): 1082-1093. doi:10.1046/j.1365-2664.2001.00662.

Martin, S. J., Highfield, A. C., Brettell, L., Villalobos, E. M., Budge, G. C., Powell, M. (2012). Global honey bee viral landscape altered by a parasitic mite. Science, 336(6086): 1304-1306. doi:10.1126/science.1220941.

Martín-Hernández, R., Meana, A., Prieto, L., Salvador, A. M., Garrido-Bailon, E., Higes, M. (2007). Outcome of colonization of Apis mellifera by Nosema ceranae. Applied and Environmental Microbiology, 73(20): 6331-6338. doi:10.1128/AEM.00270-07.

Martín-Hernández, R., Meana, A., García-Palencia, P., Marín, P., Botías, C., Garrido-Bailón, E, Barrios, L., Higes, M. (2009). Temperature effect on biotic potential of honey bee microsporidia. Appllied and Environmental Microbiology, 75(8): 2554-2557. doi:10.1128/AEM.02908-08.

Medina, L., Martin S. J. (1999). A comparative study of Varroa jacobsoni reproduction in worker cells of honeybees (Apis mellifera) in England and Africanized bees in Yucatan, Mexico. Experimental and Applied Acarology, 23(8): 659–667. doi:10.1023/A:1006275525463.

Moretto, G., Gonçalves, L. S., De Jong, D. Bichuette, M. Z. (1991). The effects of climate of and bee race on Varroa jacobsoni Oud infestations in Brasil. Apidologie, 22 (3): 197-23.

Moretto, G., Gonçalves, L. S., De Jong, D. (1997). Relationship between food availability and the reproductive ability of the mite Varroa jacobsoni in Africanized bee colonies. American Bee Journal, 137(10): 67-69.

Naug, D. (2009). Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biological Conservation, 142(10): 2369-2372. doi:10.1016/j.biocon.2009.04.007.

OIE. (2014). American Foulbrood of Honey Bees in: Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. World Organization of Animal Health. v. 1, section 2.2, Chapter 2.2.2. Retrieved from http://www.oie.int/fileadmin/Home/fr/Health_standards/tahm/2.02.02_AMERICAN_FOULBROOD.pdf

Paxton, R., Klee, J.S., 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.

Pettis, J. S., VanEngelsdorp, D., Johnson, J., Dively, G. (2012). Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften, 99(2): 153–158. doi:10.1007/s00114-011-0881-1.

Rosenkranz, P, Aumeier, P, Ziegelmann B. (2010). Biology and control of Varroa destructor. Journal of Invertebrate Pathology, 103(1): 96–119. doi:10.1016/j.jip.2009.07.016.

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(3): 307-312. doi:10.13102/sociobiology.v61i3.307-312.

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

Schuch, D. M. T., Madden, R. H., Sattler, A. (2001). An improved method for the detection and presumptive identification Paenibacillus larvae spores in honey. Journal of Apiculture Research, 40(2): 59-64. doi:10.1080/00218839.2001.11101052.

Schuch, D. M. T., Tochetto, L. G., Sattler, A. (2001). Isolamento de esporos de Paenibacillus larvaesubsp. larvae no Brasil, Pesquisa Agropecuária Brasileira, 38(3): 441-444,. doi:10.1590/S0100-204X2003000300015.

Souza, D. L., Rodrigues, A. E., Pinto, M. S. C. (2007). As abelhas como agentes polinizadores. Revista Eletrônica de Veterinária, 8(3). Retrived from: http://www.veterinaria.org/revistas/redvet/n030307/030710.pdf

Stokstad, E. (2007). The case of the empty hives. Science. 316(5827): 970–97. doi:10.1126/science.316.5827.970.

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., 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(3): 250-254. doi:10.1016/j. jip.2013.19.002.

Tozkar, C. O., Kence, M., Kence, A., Huang, Q., Evans, J. D. (2015), Metatranscriptomic analyses of honey bee colonies. Frontiers in Genetics 6(100): 1-12. doi:10.3389/fgene.2015.00100.

VanEngelsdorp, D., Tarpy, D. R., Lemgerich, E. J., Pettis, J. S. (2013). Idiopathic brood disease syndrome and queen events as precursors of colony mortality in migratory beekeeping operations in the eastern United States. Preventive Veterinary Medicine 108(2-3): 225-233. doi:10.1016/j.prevetmed.2012.08.004.

Zhang, Z. Q. (2000). Notes on Varroa destructor (Acari: Varroidae) parasitic on honeybees in New Zealand. Systematic & Applied Acarology Special Publications 5: 9-14. doi:10.11158/saasp.5.1.2.




How to Cite

Cestaro, L. G., Alves, M. L. T. M. F., Message, D., Silva, M. V. G. B., & Teixeira, Érica W. (2017). Honey Bee (Apis mellifera) Health in Stationary and Migratory Apiaries. Sociobiology, 64(1), 42–49. https://doi.org/10.13102/sociobiology.v64i1.1183



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