Revista Chapingo Serie Ciencias Forestales y del Ambiente
Frequency of varroatosis and nosemosis in honeybee (Apis mellifera) colonies in the state of Zacatecas, Mexico
ISSNe: 2007-4018   |   ISSN: 2007-3828
PDF

Keywords

Ecological zones
fall and spring
Nosema spp.
Varroa destructor

How to Cite

Medina-Flores, C. A. ., Guzmán-Novoa, E., Espinosa-Montaño, L. G. ., Uribe-Rubio, J. L. ., Gutiérrez-Luna, R. ., & Gutiérrez-Piña, F. J. . (2014). Frequency of varroatosis and nosemosis in honeybee (Apis mellifera) colonies in the state of Zacatecas, Mexico. Revista Chapingo Serie Ciencias Forestales Y Del Ambiente, 20(3), 159–167. https://doi.org/10.5154/r.rchscfa.2013.08.028

Abstract

The aim of this study was to determine the frequency and degree of infestation of varroatosis (Varroa destructor) and infection of nosemosis (Nosema spp.) in honeybee (Apis mellifera) colonies in the state of Zacatecas during the fall and spring. We inspected 299 commercial honeybee colonies located in 15 municipalities in the state of Zacatecas and in three different ecological zones: 1) temperate semi-dry, 2) semi-warm semi-dry, and 3) temperate sub-humid. Results showed a general prevalence of 2.3 % for nosemosis and 88 % for varroatosis. The varroa infestation level varied significantly (P = 0.05) between fall and spring, and among zones only during the spring (P < 0.001). Infestation levels of 5 % or higher were found in 44 % of the colonies during fall, while 28 % of them exceeded 5 % infestation levels in spring. Nosema spp. was only observed in 4.7 % of the sampled population in spring; most of the cases (86 %) were detected in the semi-warm semi-dry zone. The results of this study indicate that varroatosis is the most common parasitic disease of adult honeybees in the state of Zacatecas. Nosemois does not pose a serious problem for beekeeping in the state, due to its low frequency.

https://doi.org/10.5154/r.rchscfa.2013.08.028
PDF

References

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

Arechavaleta-Velasco, M. E., & Guzmán-Novoa, E. (2000). Producción de miel de colonias de abejas (Apis mellifera L.) tratadas y no tratadas con fluvalinato contra Varroa jacobsoni Oudemans en Valle de Bravo, Estado de México. Veterinaria México, 31(4), 381–384. http://www.medigraphic.com/pdfs/vetmex/vm-2000/vm004m.pdf

Arechavaleta-Velasco, M. E., & Guzmán-Novoa, E. (2001). Relative effect of four characteristics that restrain the population growth of the mite Varroa destructor in honey bee (Apis mellifera) colonies. Apidologie, 32, 157–174. doi: https://doi.org/10.1051/apido:2001121

Aumeier, P., Rosenkranz, P., & Gonçalves, L. S. (2000). A comparison of the hygienic response of Africanized and European (Apis mellifera carnica) honey bees to Varroa-infested brood in tropical Brazil. Genetics and Molecular Biology, 23(4), 787–791. http://www.scielo.br/pdf/gmb/v23n4/6230.pdf

Bailey, L., & Ball, B. V. (1991). Honey bee pathology (2a ed.). London: Academic Press.

Behrens, D., Huang, Q., Gebner, C., Rosenkranz, P., Frey, E., Locke, B., 8c Kraus, F. B. (2011). Three QTL in the honey bee Apis mellifera L. suppress reproduction of the parasitic mite Varroa destructor. Ecology and Evolution, 1(4), 451–458. doi: https://doi.org/10.1002/ece3.17

Calatayud, F., & Verdú, M. J. (1992). Evolución anual de parámetros poblacionales de colonias Apis mellifera L. (Hymenoptera: Apidae) parasitadas por Varroa jacobsoni Oud. (Mesostigmata: Varroidae). Boletín de Sanidad Vegetal Plagas, 18, 777–788.

Chihu, A. D., Rojas, A. L. M., & Rodríguez, D. S. (1992). Presencia en Veracruz, México del ácaro Varroa jacobsoni, causante de la varroasis de la abeja melífera (Apis mellifera L.). Técnica Pecuaria México, 30(2), 132–135.

Cobey, S. (2001). The Varroa species complex: Identifying Varroa destructor and news strategies of control. American Bee Journal, 141(3), 194–196.

Corrêa-Marques, M. H., & De Jong, D. (1998). Uncapping of worker bee brood, a component of the hygienic behavior of Africanized honey bees against the mite Varroa jacobsoni Oudemans. Apidologie, 29, 283–289. doi: https://doi.org/10.1051/apido:19980307

De Jong, D. (1997). Mites: Varroa and other parasites of brood. In Morse, R. A., & Flottum K. (Eds.), Honey bee pests, predators and diseases (pp. 279–328). Ithaca, NY, USA: Root Publishing.

De Jong, D., Roma, D. A., & Goncalves, L. S. (1982). A comparative analysis of shaking solutions for the detection of Varroa jacobsoni on adult honeybees. Apidologie,13, 297–306. doi: https://doi.org/10.1051/apido:19820308

De Jong, D., & Soares, E. A. (1997). An isolated population of Italian bees that has survived Varroa jacobsoni infestation without treatment for over 12 years. American Bee Journal, 137, 742–745. http://www.imkervlaamsear-imkervlaamseardennen. be/images/pdffolder/art-De-Jong-bee-survivevarroa. pdf

Fries, I., Hansen, H., Imdorf, A., & Rosenkranz, P. (2003). Swarming in honey bees (Apis mellifera) and Varroa destructor population development in Sweden. Apidologie, 34, 389– 398. doi: https://doi.org/10.1051/apido:2003032

García, M. M., & Quezada-Euan, J. J. (1993). Distribución de la nosemosis en apiarios comerciales del estado de Yucatán. Apicultura Moderna, 5, 22–24.

Gris, V. A. G., Guzmán-Novoa, E., Correa, B. A., & Zozaya, R. J. A. (2004). Efecto del uso de dos reinas en la población, peso, producción de miel y rentabilidad de colonias de abejas melíferas (Apis mellifera L.) en el altiplano mexicano. Técnica Pecuaria México, 42(3), 361–377. http://www.tecnicapecuaria.org.mx/trabajos/200410183721.pdf

Guzmán-Novoa, E. (2007). Elemental genetics and breeding for the honeybee. Guelph, Ontario, Canada: Ontario Beekeepers Association.

Guzmán-Novoa, E., Emsen, B., Unger, P., Espinosa-Montaño, L. G., & Petukhova, T. (2012). Genotypic variability and relationships between mite infestation levels, mite damage, grooming intensity, and removal of Varroa destructor mites in selected strains of worker honey bees (Apis mellifera L.). Journal of Invertebrate Pathology, 110, 314–320. doi: https://doi.org/10.1016/j.jip.2012.03.020

Guzmán-Novoa, E., Hamiduzzaman, 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(2), 167–169. doi: https://doi.org/10.3896/IBRA.1.50.2.09

Guzmán-Novoa, E., Eccles, L., Calvete, Y., McGowan, J., Kelly, P. G., & Correa-Benítez A. (2010). Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apidologie, 41(4), 443–450. doi: https://doi.org/10.1051/apido/2009076

Guzmán-Novoa, E., Vandame, R., & Arechavaleta-Velazco, M. (1999). Susceptibility of European and Africanized honey bees (Apis mellifera L.) to Varroa jacobsoni Oud. in Mexico. Apidologie, 30, 173–182. doi: https://doi.org/10.1051/apido:19990207

Guzmán-Novoa, E., Zozaya, J. A., Anguiano-Baez, R., & Vásquez- Valencia, I. (2012). Técnicas de diagnóstico de laboratorio de las enfermedades y parásitos de las abejas. En E. Guzmán- Novoa, & A. Correa-Benítez (Eds.), Patología, diagnóstico y control de las principales enfermedades y plagas de las abejas melíferas. México, D. F: Editorial Yire.

Higes, M., Martín-Hernández, R., & Meana, A. (2010). Nosema ceranae in Europe: An emergent type C nosemosis. Apidologie, 41, 375–392. doi: https://doi.org/10.1051/apido/2010019

Higes, M., Martín-Hernández, R., Garrido-Bailón, E., García- Palencia, P., & Meana, A. (2008). Detection of infective Nosema ceranae (Microsporidia) spores in corbicular pollen of forager honeybees. Journal of Invertebrate Pathology, 97, 76–78. doi: https://doi.org/10.1016/j.jip.2007.06.002

Instituto Nacional de Estadística y Geografía (INEGI). (2005). Sistema para la consulta de los cuadernos estadísticos municipales y delegacionales, 2005. http://www.inegi.gob.mx/est/contenidos/espanol/sistemas/cem05/nacional/index.htm

Junkes, L., Guerra, C. V., & Moretto, J. G. (2007). Varroa destructor mite mortality rate according to the amount of worker broods in Africanized honey bee (Apis mellifera L.) colonies. Acta Scientiarum Biological Sciences, 29, 305–308. http://www.redalyc.org/articulo.oa?id=187115762010

Kraus, B., & Page, R. E. (1995). Population growth of Varroa jacobsoni Oud in Mediterranean climates of California. Apidologie, 26, 149–157. doi: https://doi.org/10.1051/apido:19950208

Marcangeli, J. A. (1999). Reproduction of the mite Varroa jacobsoni in hygienic honeybee colonies of Apis mellifera. Apiacta, 34, 21–25.

Marcangeli, J. A., Eguaras, M. A., & Fernández, N. (1992). Reproduction of Varroa jacobsoni (Acari: Mesostigmata: Varroidae) in temperate climates of Argentina. Apidologie, 23, 57–60. doi: https://doi.org/10.1051/apido:19920106

Martín-Hernández, R., Botias, C., Bailón, E. G., Martínez-Salvador, A., Prieto, L., Meana, A. A., & Higes, M. (2012). Microsporidia infecting Apis mellifera: Coexistence or competition. Is Nosema ceranae replacing Nosema apis? Environmental Microbiology, 14(8), 2127–2138. doi: https://doi.org/10.1111/j.1462-2920.2011.02645.x

Matheson, A. (1993). World bee health report. Bee World, 74(4), 176–212.

Medina, L. (1998). Frequency and infestation level of the mite Varroa jacobsoni Oud. in managed honey bee (Apis mellifera L.) colonies in Yucatan, Mexico. American Bee Journal, 138(2), 125–127.

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

Medina-Flores, C. A., Guzmán-Novoa, E., Aréchiga-Flores, C., Aguilera-Soto, J., & Gutiérrez-Piña, F. (2011). Efecto del nivel de infestación de Varroa destructor sobre la producción de miel de colonias de Apis mellifera en el altiplano semiárido de México. Revista Mexicana de Ciencias Pecuarias, 2(3), 313–317. http://www.scielo.org.mx/pdf/rmcp/v2n3/v2n3a6.pdf

Medina-Flores, C. A., Guzmán-Novoa, E., Hamiduzzaman, M. M., Aréchiga-Flores, C. F., & López-Carlos, M. A. (2014). Africanized honey bees (Apis mellifera) have low infestation levels of the mite Varroa destructor in different ecological regions in Mexico. Genetics and molecular research: GMR, 13(3): 7282-7293. doi: https://doi.org/10.4238/2014.February.21.10

Moretto, G., Gonçalves, L. S., De Jong, D., & Bichuette, M. Z. (1991). The effects of climate and bee race on Varroa jacobsoni Oud infestations in Brazil. Apidologie, 22, 197–203. doi: https://doi.org/10.1051/apido:19910303

Moretto, G., & Mello, L. J. (1999).Varroa jacobsoni infestation of adult Africanized and Italian honey bees (Apis mellifera) in mixed colonies in Brazil. Genetics and Molecular Biology, 22, 321–323. doi: https://doi.org/10.1590/S1415-47571999000300006

Moretto, G., & Mello, L. J. (2000). Resistance of Africanized bees (Apis mellifera L.) as a cause of mortality of the mite Varroa jacobsoni Oud. in Brazil. American Bee Journal, 140(11), 895–897.

Organización Mundial de Salud Animal (OIE). (2008). Código sanitario para los animales terrestres 2008. http://www.oie.int/es/normas-internacionales/codigo-terrestre/acceso-en-linea/

Paxton, R. J. (2010). Does infection by Nosema ceranae cause “Colony Collapse Disorder” in honey bees (Apis mellifera)? Journal of Apicultural Research, 49, 80–84. doi: https://doi.org/10.3896/IBRA.1.49.1.11

Puc, J. F. M., Medina, L. A. M., & Ventura, G. A. C. (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. http://www.redalyc.org/pdf/2656/265619707003.pdf

Ruíz-Flores, A., Ramírez-Hernández, E., Maldonado-Simán, E., Palafox-Guillén, J., Ochoa-Torres, E., & López-Ordaz, R. (2012). Incidencia y nivel de infestación por varroasis en abejas (Apis mellifera) en el laboratorio de identificación y diagnóstico apícola de 2002 a 2006. Revista Chapingo Serie Ciencias Forestales y del Ambiente, 18(2), 175–182. doi: https://doi.org/10.5154/r.rchscfa.2011.03.023

Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación. (SAGARPA). (2011). Servicio de información estadística agroalimentaria y pesquera (SIAP). http://www.siap.sagarpa.gob.mx

Secretaría de Agricultura y Recursos Hidráulicos (SARH). (1994). Norma Oficial Mexicana NOM-001-ZOO-1994, campaña nacional contra la varroasis de las abejas. http://sagarpa.gob.mx/ganaderia/Paginas/Legislacion.aspx

Spivak, M., & Reuter, G. (2001). Varroa destructor infestation in untreated honey bee (Hymenoptera: Apidae) colonies selected for hygienic behavior. Journal Economical Entomology, 94(2), 326–331. doi: https://doi.org/Spivak, M., & Reuter, G. (2001). Varroa destructor infestation in untreated honey bee (Hymenoptera: Apidae) colonies selected for hygienic behavior. Journal Economical Entomology, 94(2), 326–331.

Statistical Analysis System (SAS Institute). (2002). Statistical Analysis System, version 9.0. Cary, NC, USA: Autor.

Szabo, T. I., & Walker, C. R. (1996). Rate of infestation of honey bee colonies by Varroa jacobsoni. American Bee Journal, 136(6), 447–448.

Uribe, R. J. L., Guzmán-Novoa, E., Hunt, G. J., Correa, B. A., & Zozaya, R. J. A. (2003) Efecto de la africanización sobre la producción de miel, comportamiento defensivo y tamaño de las abejas melíferas (Apis mellifera L.) en el altiplano mexicano. Veterinaria México, 34, 47–59. http://www.medigraphic.com/pdfs/vetmex/vm-2003/vm031e.pdf

Vandame, R., Morand, S., Colin, M., & Belzunces, L. P. (2002). Parasitism in the social bee Apis mellifera: Quantifying cost and benefits of behavioral resistance to Varroa destructor mites. Apidologie, 33, 432–445. doi: https://doi.org/10.1051/apido:2002025

VanEngelsdorp, D., & Meixner, M. D. (2010). A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. Journal of Invertebrate Pathology, 103, 580–595. doi: https://doi.org/10.1016/j.jip.2009.06.011

Winston, M. L. (1991). The biology of the honey bee. USA: Harvard University Press.

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

Copyright (c) 2014 Revista Chapingo Serie Ciencias Forestales y del Ambiente