Varroasis y mécanismos de defensa de la abeja melífera (Apis mellifera)

Diego Armando Masaquiza Moposita; Lino Miguel Curbelo; Byron Leoncio Díaz Monroy; Amílcar Arenal Cruz

Diego Armando Masaquiza Moposita Center of Studies for the Development of Animal Production (CEDEPA), Faculty of Agricultural Sciences, University of Camagüey, Cuba https://orcid.org/0000-0001-5176-8261
Lino Miguel Curbelo Center of Studies for the Development of Animal Production (CEDEPA), Faculty of Agricultural Sciences, University of Camagüey, Cuba
Byron Leoncio Díaz Monroy Faculty of Animal Sciences, Polytechnic School of Chimborazo, Chimborazo, Ecuador
Amílcar Arenal Cruz Department of Morphophysiology, University of Camaguey "Ignacio Agramonte Loynaz", Camaguey, Cuba

Keywords: Varroa, Apis, Africanized bees, apiculture

Abstract

Background: Honey bees are threatened by acaride Varroa destructor, which among other factors, causes what is known today in the world as Colony Collapse Disorder. The aim of this review is to publish updated information of Varroasis in Apis mellifera, as well as to study some defense mechanisms of bees during their co-evolution with the parasite.

Methods: The databases of Sciencedirect, Google-scholar, Scopus, and NCBI were reviewed under the following key words: Varroa destructor, biological cycle, bees, Apis, Africanized bees, apiculture, and Apis mellifera. Special emphasis was paid to papers published within the last five years.

Results: The features of the acaride and its biological cycle, its effects on bee colonies, and the factors that favor the presence of the parasite were described. Moreover, mechanisms like hygienic behavior, grooming, and suppression of acaride reproduction. The impact of Varroasis worldwide was updated.

Conclusions: Certain bee populations manage to live with acaride varroa, because their defense mechanisms allow for infestation rates at permissible ranges. The current trend is to include these mechanisms in breeding programs.

Key words: Varroa, Apis, Africanized bees, apiculture

Downloads

Download data is not yet available.

References

Abbo, P., Kawasaki, J., Hamilton, M., Cook, S., DeGrandi-Hoffman, G., Li, W. y Chen, Y. (2017). Effects of Im-idacloprid and Varroa destructor on survival and health of European honey bees, Apis mellifera. Insect Science 24(3), 467-477.

Akinwande, K., Badejo, M. y Ogbogu, S. (2014). Hygienic behavioural mechanism of resistance to diseases and parasites in west african honey bee colonies Apis mellifera adansonii (Hymenoptera: apidae). International Journal of Entomology Research 2(2), 73-79.

Anderson, D. y Trueman, J. (2000). Varroa jacobsoni (Acari: Varroidae) is more than one species. Experimental and Applied Acarology 24(3), 165-189.

Annoscia, D., Del Piccolo, F., Covre, F. y Nazzi, F. (2015). Mite infestation during development alters the in-hive be-haviour of adult honeybees. Apidologie 46(3), 306-314.

Arathi, H., Burns, I. y Spivak, M. (2000). Ethology of hygienic behavior in the honey bee Apis mellifera L. (Hyme-noptera: Apidae): behavioral repertoire of hygienic bees. Ethology 106(4), 365-379.

Ardestani, M. M. (2015). Investigating the influence of postcapping period on varroa mite infestation. Journal of Apicultural Research 54(4), 335-341.

Arechavaleta-Velasco, M., Hunt, G., Spivak, M. y Camacho-Rea, C. (2011). Loci de rasgos binarios que influyen en la expresión del comportamiento higiénico de las abejas melíferas. Revista Mexicana de Ciencias Pecuarias, 2(1), 238-298.

Bahreini, R. y Currie, R. (2015). The influence of Nosema (Microspora: Nosematidae) infection on honey bee (Hy-menoptera: Apidae) defense against Varroa destructor (Mesostigmata: Varroidae). Journal of Invertebrate Pa-thology, 132(1), 57-65.

Beaurepaire, A. L., Truong, T.A., Fajardo, A.C., Dinh, T. Q., Cervancia, C. y Moritz, R.F.A. (2015). Host Specificity in the Honeybee Parasitic Mite, Varroa spp. in Apis mellifera and Apis cerana. PLOS ONE, 10(2), 33-40.

Blanken, L., Van Langevelde, F. y Van Dooremalen, C. (2015). Interaction between Varroa destructor and im-idacloprid reduces flight capacity of honeybees. London, UK: Royal Society B.

Büchler, R., Andonov, S., Bienefeld, K., Costa, C., Hatjina, F., Kezic, N., et al. (2013). Standard methods for rearing and selection of Apis mellifera queens. Journal of Apicultural Research, 52(3), 1-30.

Calderón, R., Ureña, S., Sánchez, L. y Calderón, R. (2014). Comparación de la habilidad reproductiva y mortalidad del ácaro Varroa destructor en celdas con cría de obrera y zángano en abejas africanizadas de Costa Rica. Re-vista de Ciencias Veterinarias, 30(1), 7-24.

Cappa, F., Bruschini, C., Protti, I., Turillazzi, S. y Cervo, R. (2016). Bee guards detect foreign foragers with cuticular chemical profiles altered by phoretic varroa mites. Journal of Apicultural Research, 55(1), 268-277.

Cassian, T., Mwakatobe, A., Hamisi, I., Richard, A., y Machumu, R. (2014). Parasitic mite, Varroa species (Parasiti-formes: Varroidae) infesting the colonies of African honeybees, Apis mellifera scutellata (Hymenoptera: Apidi-dae) in Tanzania. J. Entomol. Zool. Stud., 2(3), 188-196.

Cepero, A. (2016). Monitorización de los principales patógenos de las abejas para la detección de alertas y ries-gos sanitarios. Tesis Doctoral, Universidad Complutense de Madrid, España.

Coelho, F., Santos, J. y Bliman, P. (2015). Behavioral modulation of the coexistence between Apis mellifera and Va-rroa destructor: A defense against colony collapse? Peer J. PrePrints, 17(3), 39-44.

Cruzat, R. y Baasch, V. (2016). Resultados y Lecciones en Productos en Base a Aceites Esenciales Microencapsu-lados para el Control del Ácaro Varroa. Región del Maule, Chile: Instituto Pecuario/Apicultor.

Dietemann, V., Nazzi, F., Martin, S. J., Anderson, D. L., Locke, B., Delaplane, K. S., et al. (2013). Standard methods for varroa research. Journal of Apicultural Research, 52(1), 1-54.

Forfert, N., Natsopoulou, M., Frey, E., Rosenkranz, P., Paxton, R. y Moritz, R. (2015). Parasites and pathogens of the honeybee (Apis mellifera) and their influence on inter-colonial transmission. PLOS ONE, 10(2), 41-48.

Froylán, M., Alcalá, E., Leal, H., Rodríguez, A. y Martínez, A. (2011). Manual de capacitación. Prevención de Va-rroosis y suplementación. Cuajimalpa, México: Instituto Nacional de Investigaciones Forestales, Agrícolas y Pe-cuarias-Centro Nacional de Investigación Disciplinaria en Microbiología Animal.

Garrido-Bailón, E. (2012). Repercusión potencial en la cabaña apícola española de agentes nosógenos detectados en colonias de Apis mellifera iberiensis. Tesis Doctoral, Universidad Complutense de Madrid, España.

Genersch, E. y Aubert, M. (2010). Emerging and re-emerging viruses of the honey bee (Apis mellifera L.). Vet. Res., 41(1), 54-59.

Giacobino, A., Bulacio, C., Merke, J., Orellano, E., Bertozzi, E., Masciangelo, G., et al. (2014). Risk factors associat-ed with the presence of Varroa destructor in honey bee colonies from east-central Argentina. Prev. Vet. Med., 115(1), 280-287.

Giménez, P., Mendoza, Y., Invenizzi, C., Fuselli, S., Alonso, R., Fernández, P. y Maggi, M. (2017). Morphometric cor-relation between Apis mellifera morphotypes (Hymenoptera) and Varroa destructor (Acari) from Uruguay. Journal of Apicultural Research, 56(1), 122-129.

Gutiérrez, B. y Bautista, G. (2016). Diagnóstico de enfermedades parasitarias en abejas africanizadas Apis mellifera en el municipio de Marsella, Risaralda, Colombia. Revista de Investigación Agraria y Ambiental, 7(1), 12-19.

Harbo, J. R. y Harris, J. W. (1999). Selecting honey bees for resistance to Varroa jacobsoni. Apidologie, 30(1), 183-196.

Harbo, J. R. y Harris, J. W. (2005). Suppressed mite reproduction explained by the behaviour of adult bees. Journal of Apicultural Research, 44(1), 21-23.

Khongphinitbunjong, K., De Guzman, L., Rinderer, T. E., Tarver, M. R., Frake, A. M., Chen, Y., et al. (2016). Re-sponses of Varroa-resistant honey bees (Apis mellifera L.) to deformed wing virus. Journal of Asia-Pacific En-tomology, 19(1), 921-927.

Khongphinitbunjong, K., De Guzman, L., Tarver, M., Rinderer, T., Chen, Y. y Chantawannakul, P. (2014). Differen-tial viral levels and immune gene expression in three stocks of Apis mellifera induced by different numbers of Varroa destructor. Journal of Insect Physiology, 72(1), 28-34.

Kielmanowicz, M. G., Inberg, A., Lerner, I. M., Golani, Y., Brown, N., Turner, C. L., et al. (2015). Prospective large-scale field study generates predictive model identifying major contributors to colony losses. PLoS pathogens, 11(1), 33-39.

Kuster, R., Oncristiani, H., y Rueppell, O. (2014). Immunogene and viral transcript dynamics during parasitic Varroa destructor mite infection of developing honey bee (Apis mellifera) pupae. J. Exp. Biol., 217(1), 1710-1718.

Lattorff, H., Buchholz, J., Fries, I. y Moritz, R. (2015). A selective sweep in a Varroa destructor resistant honey bee (Apis mellifera) population. Infect. Genet. Evol., 31(1), 169-176.

Le Conte, Y., Huang, Z., Roux, M., Zeng, Z., Christidès, J. y Bagnères, A. (2015). Varroa destructor changes its cutic-ular hydrocarbons to mimic new hosts. Biology Letters, 11(2), 1-10.

Lightbody, K., Davis, P. y Austin, C. (2016). Validation of a novel saliva‐based ELISA test for diagnosing tapeworm burden in horses. Veterinary Clinical Pathology, 30(3), 50-58.

Lin, Z., Page, P., Li, L., Qin, Y., Zhang, Y., Hu, F., et al. (2016). Go east for better honey bee health: Apis cerana is faster at hygienic behavior than A. mellifera. PloS one, 11(1), 100-107.

Locke, B. (2016a). Inheritance of reduced Varroa mite reproductive success in reciprocal crosses of mite-resistant and mite-susceptible honey bees (Apis mellifera). Apidologie, 47(2), 583-588.

Locke, B. (2016b). Natural Varroa mite-surviving Apis mellifera honeybee populations. Apidologie, 47(2), 467-482.

Locke, B., Forsgren, E. y De Miranda, J. (2014). Increased tolerance and resistance to virus infections: a possible factor in the survival of Varroa destructor-resistant honey bees (Apis mellifera). PloS one, 9(2), 33-39.

McDonnell, C., Alaux, C., Parrinello, H., Desvignes, J., Crauser, D., Durbesson, E., et al. (2013). Ecto and endopara-site induce similar chemical and brain neurogenomic responses in the honey bee (Apis mellifera). BMC Ecology, 13(2), 25-30.

Medina-Flores, C., Guzmán-Novoa, E., Hamiduzzaman, M., Aréchiga-Flores, C. y López, M. (2014). Africanized honey bees (Apis mellifera) have low infestation levels of the mite Varroa destructor in different ecological re-gions in México. Genetics and Molecular Research, 13(1), 7282-7293.

Mondet, F., De Miranda, J., Kretzschmar, A., Le Conte, Y. y Mercer, A. (2014). On the Front Line: Quantitative Virus Dynamics in Honeybee (Apis mellifera L.) Colonies along a New Expansion Front of the Parasite Varroa de-structor. PLoS Pathog., 10(1), 33-37.

Mondragón, L., Martin, S. y Vandame, R. (2006). Mortality of mite offspring: a major component of Varroa de-structor resistance in a population of Africanized bees. Apidologie, 37(2), 67-74.

Nazzi, F. y Le Conte, Y. (2016). Ecology of Varroa destructor, the major ectoparasite of the western honey bee, Apis mellifera. Annual review of entomology, 61(1), 417-432.

Newton, D. y Ostasiewski, N. (1986). A Simplified Bioassay for Behavioral Resistance to American Foulbrood in Honey-Bees (Apis mellifera L). American Bee Journal, 126(2), 278-281.

Nganso, B. T., Fombong, A. T., Yusuf, A. A. y Pirk, C. W. (2017). Hygienic and grooming behaviors in African and European honeybees-New damage categories in Varroa destructor. PLoSOne, 12(1), 45-53.

Oddie, M.A., Dahle, B. y Neumann, P. (2017). Norwegian honey bees surviving Varroa destructor mite infestations by means of natural selection. Peer J., 5(1), 39-49.

Peck, D., Smith, M. y Seeley, T. (2016). Varroa destructor mites can nimbly climb from flowers onto foraging honey bees. . PLoS one, 11(3), 98-106.

Pernal, S., Baird, D., Birmingham, A., Higo, H., Slessor, K. y Winston, M. (2005). Semiochemicals inﬂuencing the host-ﬁnding behavior of Varroa destructor. Experimental and Applied Acarology, 37(2), 11-26.

Plettner, E., Eliash, N., Singh, N., Pinnelli, G. y Soroker, V. (2017). The chemical ecology of host-parasite interaction as a target of Varroa destructor control agents. Apidologie, 48(2), 78-92.

Pritchard, D. J. (2016). Grooming by honey bees as a component of varroa resistant behavior. Journal of Apicultur-al Research, 55(2), 38-48.

Ramsey, S. (2018). The acari varroa feeds mainly of the fatty corporal fabric of the melliferous bee. Thesis of Doc-torate. University of Maryland, USA.

Rehm, S. y Ritter, W. (1989). Sequence of the sexes in the offspring of Varroa jacobsoni and the resulting conse-quences for the calculation of the developmental period. Apidologie, 20(1), 339-343.

Reyes, F. (2016). Efectividad de cuatro acaricidas en el control del ácaro (Varroa destructor) en abejas (Apis me-llifera L.). Tesis de Maestría en Producción animal, Universidad Nacional Agraria, Lima, Perú.

Rinderer, T. E., De Guzman, L. I., Delatte, G., Stelzer, J., Lancaster, V., Kuznetsov, V., et al. (2001). Resistance to the parasitic mite Varroa destructor in honey bees from far-eastern Russia. Apidologie, 32(3), 381-394.

Roberts, J., Anderson, D. y Tay, W. (2015). Multiple hostáshifts by the emerging honeybee parasite, Varroa jacob-soni. Molecular Ecology, 24(1), 2379-2391.

Rodriguez, A. (2016). Monitorización de los principales patógenos de las abejas para la detección de alertas y riesgos sanitarios. Madrid, España: Universidad Complutense de Madrid.

Rosenkranz, P., Aumeier, P. y Ziegelmann, B. (2010). Biology and control of Varroa destructor. Journal of inverte-brate pathology, 103(1), 96-103.

Rothenbuhler, W. C. (1964a). Behavior genetics of nest cleaning in honey bees. IV. Responses of F 1 and backcross generations to disease-killed brood. American Zoologist, 4(2), 111-123.

Rothenbuhler, W. C. (1964b). Behaviour genetics of nest cleaning in honey bees. I. Responses of four inbred lines to disease-killed brood. Animal Behaviour, 12(1), 578-583.

Salamanca, G., Osorio, M., y Rodríguez, N. (2012). Presencia e incidencia forética de Varroa destructor (Mesostig-ma: Varroidae) en colonias de abejas Apis mellifera (Hymenoptera: Apidae), en Colombia. Zootecnia Tropical, 30(1), 183-195.

Sánchez-Bayo, F., Goulson, D., Pennacchio, F., Nazzi, F., Goka, K. y Desneux, N. (2016). Are bee diseases linked to pesticides? A brief review. Environment International, 89(90), 7-11.

Seeley, T. y Smith, M. (2015). Crowding honeybee colonies in apiaries can increase their vulnerability to the deadly ectoparasite Varroa destructor. Apidologie, 46(6), 716-727.

Smart, M., Pettis, J., Rice, N., Browning, Z. y Spivak, M. (2016). Linking measures of colony and individual honey bee health to survival among apiaries exposed to varying agricultural land use. PLoS one, 11(1), 15-26.

Smith, K. M., Loh, E. H., Rostal, M. K., Zambrana-Torrelio, C. M., Mendiola, L. y Daszak, P. (2014). Pathogens, pests, and economics: drivers of honey bee colony declines and losses. EcoHealth, 10(4), 434-445.

Spivak, M. y Downey, D. L. (1998). Field assays for hygienic behavior in honey bees (Hymenoptera: Apidae). Jour-nal of economic entomology, 91(1), 64-70.

Steinhauer, N., Kulhanek, K., Antúnez, K., Human, H., Chantawannakul, P. y Chauzat, M. (2018). Drivers of colony losses. Current opinion in Insect science, 26(1), 142-148.

Strauss, U., Dietemann, V., Human, H., Crewe, R. M. y Pirk, C. W. (2016). Resistance rather than tolerance explains survival of savannah honeybees (Apis mellifera scutellata) to infestation by the parasitic mite Varroa destruc-tor. Parasitology, 143(3), 374-387.

Van Der Zee, R., Gray, A., Pisa, L. y De Rijk, T. (2015). An observational study of honey bee colony winter losses and their association with Varroa destructor, neonicotinoids and other risk factors. PloS one, 10(2), 13-16.

Vandame, R. (2001). Control alternativo de Varroa destructor. Chiapas, México: Colegio de la Frontera Sur.

Vaziritabar, S., Aghamirkarimi, A. y Mehdi, S. (2016). Evaluation of the defensive behavior in two honeybee races Iranian honeybee (Apis mellifera meda) and Carniolan honeybee (Apis mellifera carnica) and grooming behav-ior of different bee races in controlling Varroa destructor mite in honey. Journal of Entomology and Zoology Studies 4(5), 586-602.

Verde, M., Demedio, J. y Gómez, T. (2013). Apicultura, Salud y Producción: Guía Técnica para el Apicultor. La Habana, Cuba: Consejo Científico Veterinario de Cuba.

Xie, X., Huang, Z. y Zeng, Z. (2016). Why do Varroa mites prefer nurse bees? Scientiﬁc Reports, 6(1), 28-34.

Xonis, C., Thrasyvoulou, A. y Taj, H. (2015). Variability of hygienic behavior in bee Apis mellifera macedonica. Bulgarian Journal of Agricultural Science 21(3), 674-679.

Varroasis and Defense (Apis mellifera) Mechanisms of Honey Bees

Abstract

Downloads

References