Prevalence of <i>Nosema</i> spp. (Microsporidia: Nosematidae) in Africanized Honeybees in Atenas, Costa Rica: Number of Spores and Infection Level During the Rainy Season

  • Eduardo Moreno Universidad Nacional, Centro de Investigaciones Apícolas Tropicales, Programa Integrado de Patología Apícola, Costa Rica
  • Rafael A. Calderón Universidad Nacional, Centro de Investigaciones Apícolas Tropicales, Programa Integrado de Patología Apícola, Costa Rica
  • Marianyela Ramírez Universidad Nacional, Centro de Investigaciones Apícolas Tropicales, Programa Integrado de Patología Apícola, Costa Rica
  • Johan Van Veen Universidad Nacional, Centro de Investigaciones Apícolas Tropicales, Programa Regional de Apicultura y Meliponicultura, Costa Rica
Keywords: Nosema spp., nosemosis, infection level, rainy season, africanized honeybees


The prevalence of the microsporidium Nosema spp. was studied during the rainy months from July to November 2017 in 10 Africanized honeybees colonies in Atenas-Alajuela, Costa Rica. In addition, the number of spores and the infection level were compared in group and individual samples of adult bees from the same colony. The apiary was sampled once a month. Approximately 100 forager bees per colony were collected, of which 30 were examined for Nosema spp. in group analysis and 30 individually at the Bee Pathology Lab-CINAT. According to the Cantwell method, the abdomens of 30 adult bees were cut and macerated together with 30 ml of distilled water for the group test. For the individual analysis, the same method was used, but each bee was examined separately. Nosema spores were identified under the cover slip using a light microscopy at 40x magnification and were counted with a hemocytometer. The infection level was determined for every colony. The microsporidium Nosema spp. were found in all apiary colonies at different levels, ranging from low to severe infection in both group and individual exams. In July, the highest number of Nosema spores were quantified, with an average of 20,360,000 ± 1,586,957 per bee in the group analysis, and 12,749,733 ± 867,232 per bee in the individual analysis. In the following months, a considerable decrease in the number of spores was observed, and the lowest amount was recorded in November, with an average of 4,375,000 ± 874,132 and 2,087,708 ± 398,895 spores per bee in the group and individual exam, respectively. When comparing the spore count and the infection level of Nosema spp. in group and individual samples, similar results were obtained. Furthermore, by correlating the number of spores, high proximity in the values was found, showing that, by both methods, a similar result is obtained concerning the infection level of the same colony.


Alaux, C., Ducloz, F., Crauser, D. & Le Conte, Y. (2010). Diet effects on honeybee immune competence. Biology Letters, 6, 562–565.

Biganski, S., Kurze, C., Müller, M. & Moritz, R. (2017). Social response of healthy honeybees towards Nosema ceranae – infected workers: care or kill? Apidologie, 49(3), 325-334.

Botías, C., Martín, R., Meana, A. & Higes, M. (2012). Critical aspects of the Nosema spp. diagnostic sampling in honeybee (Apis mellifera L.) colonies. Parasitology Research, 110, 2557-2561.

Botías, C., Martín, R., Barrios, L., Meana, A. & Higes, M. (2013). Nosema spp. infection and its negative effects on honeybees (Apis mellifera iberiensis) at the colony level. Veterinary Research, 44, 25.

Bravo, J., Carbonell, V., Valdebenedito, J. T., Figueroa, C., Valdovinos, C. E., Martín, R. & Delporte, C. (2014). Identification of Nosema ceranae in the Valparaíso, Chile. Archivos de Medicina Veterinaria, 46(3), 487-491.

Calderón, R. A. & Sánchez, L. A. (2007). Detección de enfermedades en abejas africanizadas en Costa Rica. Revista Ciencias Veterinarias, 25(2), 335-348.

Calderón, R. A., Sánchez, L. A., Yañez, O. & Fallas, N. (2008). Presence of Nosema ceranae in Africanized honey bee colonies in Costa Rica. Journal of Apicultural Research and Bee World, 47, 328-329.

Calderón, R. A. & Ramírez, F. (2010). Enfermedades de las abejas melíferas, con énfasis en abejas africanizadas. EUNA.

Calderón, R. A. & Pichardo, J. (2011). Nosemiasis en abejas melíferas: diagnóstico, control y prevalencia. Publicaciones e Impresiones UNA.

Calderón, R. A. & Sánchez, L. A. (2011). Diagnóstico de enfermedades en colmenas de abejas africanizadas en Costa Rica: prevalencia y distribución de setiembre a noviembre del 2007. Agronomía Costarricense, 35(2), 49-60.

Chemurot, M., De Smet, L., Brunain, M., De Rycke, R. & de Graaf, D. (2017). Nosema neumanni (Microsporidia, Nosematidae), a new microsporidian parasite of honeybees, Apis mellifera in Uganda. European Journal of Protistology, 61, 13-19.

Chen, Y., Chung, W., Wang, C., Solter, L. & Huang, W. (2012). Nosema ceranae infection intensity highly correlates with temperature. Journal of Invertebrate Pathology, 111, 264-267.

Chihu, L., Chihu, D. & Fernández, M. (2013). Nosema ceranae, un patógeno emergente en la apicultura mundial. Editorial Academia Española.

Chupia, V., Pikulkacw, S., Krutnuang, P., Mckchay, S. & Patchancc, P. (2016). Molecular epidemology and geographical distribution of Nosema ceranae in honeybees, Northern Thailand. Asian Pacific Journal of Tropical Disease, 6(1), 27-31.

Copley, T., Chen, H., Giovenazzo, P., Houle, E. & Jabaji, S. (2012). Prevalence and seasonality of Nosema species in Québec honeybees. The Canadian Entomologist, 144, 577-588.

DeGrandi-Hoffman, G. & Chen, Y. (2015). Nutrition, immunity and viral infections in honeybees. ScienceDirect, 10, 170-176.

Eiri, D., Suwannapong, G., Endler, M. & Nieh, J. (2015). Nosema ceranae can infect honeybee larvae and reduces subsequent adult longevity. PLOS ONE, 10(5), 1-17.

Emsen, B., Guzman, E., Hamiduzzaman, M., Eccles, L., Lacey, B., Ruiz, R. & Nasr, M. (2015). Higher prevalence and levels of Nosema ceranae than Nosema apis infections in Canadian honeybee colonies. Parasitology Research, 115(1), 175-181.

Foley, K., Fazio, G., Jensen, A. & Hughes, W. (2014). The distribution of Aspergillus spp. opportunistic parasites in hives and their pathogenicity to honeybees. Veterinary Microbiology, 169(3-4), 203-210.

Fries, I. (2010). Nosema ceranae in European honeybees (Apis mellifera). Journal of Invertebrate Pathology, 103, S73-S79.

Hamiduzzaman, M., Guzmán, P. H., Goodwin, M., Reyes, G., Koleoglu, A., Correa, A. & Petukhova, T. (2015). Differential responses of Africanized and European honeybees (Apis mellifera) to viral replication following mechanical transmission or Varroa destructor parasitism. Journal of Invertebrate Pathology, 126, 12-20. j.jip.2014.12.004.

Higes, M., García, R., Martín, R. & Meana, A. (2007). Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). Journal of Invertebrate Pathology, 94(3), 211-217.

Higes, M., Martín, R., Botías, C., Bailón, E. G., González, A. V., Barrios, L. & Meana, A. (2008). How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental Microbiology, 10(10), 2659-2669.

Higes, M., Martin, R. & Meana, A. (2010). Nosema ceranae in Europe: an emergent type C Nosemosis. Apidologie, 41, 375-392.

Huang, W., Solter, L., Aronstein, K. & Huang, Z. (2015). Infectivity and virulence of Nosema ceranae and Nosema apis in commercially available North American honeybees. Journal of Invertebrate Pathology, 124, 107-113.

Huang, S., Ye, K., Huang, W., Ying, B., Su, X., Lin, L., Li, J., Chen, Y., Li, J., Bao, X. & Hu, J. (2018). Influence of feeding type and Nosema ceranae infection on the gut microbiota of Apis cerana workers. American Society for Microbiology Systems, 3(6), 1-11.

Instituto Meteorológico Nacional. (2017). Regiones y subregiones climáticas del país.

Invernizzi, C., Santos, E., Garcia, E., Daners, G., Di Landro, R., Saadoun, A. & Cabrera, C. (2011). Sanitary and nutritional characterization of honeybees colonies in Eucalyptus grandis plantations. Archivos de Zootecnia, 60, 1303-1314.

Jack, C., Lucas, H., Webster, T. & Sagili, R. (2016). Colony level prevalence and intensity of Nosema ceranae in honeybees (Apis mellifera L.). PLOS ONE, 11(9), 1-20.

Jara, L., Muñoz, I., Cepero, A., Martín, R., Serrano, J., Higes, M. & De la Rúa, P. (2015). Stable genetic diversity despite parasite and pathogen spread in honeybee colonies. The Science of Nature, 102, 53.

Martínez, J., Medina, L. & Catzín, A. (2011). Frecuencia de Varroa destructor, Nosema apis y Acarapis woodi en colonias manejadas y enjambres silvestres de abejas (Apis mellifera) en Mérida, Yucatán, México. Revista Mexicana de Ciencias Pecuarias, 2(1), 25-38.

Medina, C., Guzmán, E., Espinosa, L., Uribe, L., Gutiérrez, R. & Gutiérrez, F. (2014). Frecuencia de Varroosis y Nosemosis en colonias de abejas melíferas (Apis mellifera) en el estado de Zacatecas, México. Revista Chapingo Serie Ciencias Forestales y del Ambiente, 20(3), 30-36.

Molina, A., Guzmán, E., Message, D., De Jong, D., Pesante, D., Mantilla, C. & Meneses, G. (1990). Enfermedades y plagas de la abeja melífera occidental. OIRSA.

Mulholland, G., Traver, B., Johnson, N. & Fell, R. (2012). Individual variability of Nosema ceranae infections in Apis mellifera colonies. Insects, 3, 1143-1155.

Muñoz, I., Cepero, A., Pinto, M., Martín, R., Higes, M. & De la Rúa, P. (2014). Presence of Nosema ceranae associated with honeybee queen introductions. Infection, Genetics and Evolution, 23, 161–168.

Organización Mundial de Sanidad Animal (OIE). (2013). Manual de las pruebas de diagnóstico y las vacunas para los animales terrestres.

Organismo Internacional Regional de Sanidad Agropecuaria (OIRSA). (1990). Protocolo de técnicas laboratoriales de diagnóstico para enfermedades y plagas apícolas.

Pacheco, L. (2008). Niveles de infección de Nosema apis Zander (Microspora: Nosematidae) en abejas adultas (Apis mellifera L.) y su relación con características del apicultor. Tesis de Pregrado, Universidad Austral de Chile. Valdivia, Chile.

Pacini, A., Giaocobino, A., Molineri, A., Bulacio, N., Aignasse, A., Zago, A. & Signorini, M. (2016). Risk factors associated whith the abundance of Nosema spp. in apiaries located in temperate and subtropical conditions after honey harvest. Journal of Apicultural Research, 55(4), 342-350.

Papini, R., Manciati, F., Canovai, R., Cosci, F., Rocchigiani, G., Benelli, G. & Canale, A. (2017). Prevalence of the microsporidian Nosema ceranae in honeybee (Apis mellifera) apiaries in Central Italy. Saudi Journal of Biological Sciences, 24(5), 979-982. 2017.01.010.

Pichardo, J., Calderón, R. A., van Veen, J. & Ramírez, F. (2012). Nosemiasis en abejas Africanizadas: detección en cámara de cría y piquera. Notas Apícolas, 15, 26-33.

Prendas-Rojas, J., Figueroa-Mata, G., Ramírez-Montero, M., Calderón-Fallas, R. A., Ramírez-Bogantes, M. & Travieso-González, C. (2018). Diagnóstico automático de infestación por Nosemiasis en abejas melíferas mediante procesado de imágenes. Revista Tecnología En Marcha, 31(2), 14-25.

Retschnig, G., Williams, G., Schneeberger, A. & Neumann, P. (2017). Cold ambient temperature promotes Nosema spp. intensity in honey bees (Apis mellifera). Insects, 8, 20.

Ritter, W. (2001). Enfermedades de las abejas. Acribia S.A.

Rubanov, A., Russell, K., Rothman, J., Nieh, J. & McFrederick, Q. (2019). Intensity of Nosema ceranae infection is associated with specific honeybee gut bacteria and weakly associated with gut microbiome structure. Science Reports, 9, 1-8.

Spivak, M. (1991). The Africanization process in Costa Rica. Westview Press Inc.

Tapia, J., Alcazar, G., Macías, J., Contreras, F., Tapia, J., Chavoya, F. & Martínez, J. (2017). Nosemosis en abejas melíferas y su relación con factores ambientales en Jalisco, México. Revista Mexicana de Ciencias Pecuarias, 8, 3-4.

Traver, B. & Fell, R. (2011). Prevalence and infection intensity of Nosema in honeybee (Apis mellifera L.) colonies in Virginia. Journal of Invertebrate Pathology, 107, 43-49.

Vivas, J. (2015). Prevalencia de Nosema (Nosema spp.) en colmenares de la región norte y centro norte del Ecuador. Tesis de grado, Universidad Central del Ecuador, Quito, Ecuador.

How to Cite
Moreno, E., Calderón, R., Ramírez, M., & Van Veen, J. (2021). Prevalence of <i>Nosema</i&gt; spp. (Microsporidia: Nosematidae) in Africanized Honeybees in Atenas, Costa Rica: Number of Spores and Infection Level During the Rainy Season. Ciencias Veterinarias, 39(1), 1-18.

Comentarios (ver términos de uso)