Varroa destructor: una amenaza mortal para la colmena de Apis mellifera

F. E. Airahuacho; S. S. Rubina

doi:10.51431/par.v3i1.664

Autores/as

F. E. Airahuacho Departamento de Zootecnia, Universidad Nacional José Faustino Sánchez Carrión, Lima, Perú. https://orcid.org/0000-0001-7484-0449
S. S. Rubina Centro de Educación Técnico Productiva Estatal San Antonio de Padua, UGEL 09, Lima, Perú.

DOI:

https://doi.org/10.51431/par.v3i1.664

Palabras clave:

Comportamiento higiénico, hemolinfa, kairomona, tejido graso

Resumen

La apicultura en el Perú ha crecido en los últimos años, influenciado principalmente por los cultivos como el palto (Persea americana Mill.), cuya polinización es asistida por los insectos. Sin embargo, cada año las colmenas de abejas enfrentan graves problemas que disminuyen su población, siendo uno de los causantes principales, el parasitismo por el ácaro Varroa destructor. Este ácaro invade celdas de larvas de abejas para reproducirse y evitan ser eliminadas de las mismas por las abejas obreras gracias a una estrategia kairomonal. Varios acaricidas son utilizados para controlar la invasión por varroa, sin embargo, existen reportes que la varroa estaría presentando resistencia a estos plaguicidas, ya sea por mutaciones en los canales de sodio dependientes de voltaje o acetilcolinesterasas, así como un incremento de la actividad desintoxicante. Como alternativa viable a la resistencia de la varroa hacia los acaricidas, se viene seleccionando colmenas con buen comportamiento higiénico, que, mediante acciones específicas como el aseo, minimizan la infestación por el ácaro. La presente revisión expone la información actual relacionada con la biología reproductiva y la alimentación de la varroa dentro de la colmena. Asimismo, describe los posibles mecanismos moleculares que explican la resistencia reportada hacia los acaricidas, proponiéndose la selección de colmenas de buen comportamiento higiénico como estrategia viable para el control de la varroa.

Descargas

Los datos de descargas todavía no están disponibles.

Citas

Abou-Shaara, H.F. (2017). Using safe materials to control Varroa mites with studying grooming behavior of honey bees and morphology of Varroa over winter. Annals of Agricultural Sciences, 62(2), 205-210. https://doi. org/10.1016/j.aoas.2017.12.002

Alattal, Y., AlGhamdi, A., Single, A., Ansari, M. J., & Alkathiri, H. (2017). Fertility and reproductive rate of Varroa mite, Varroa destructor, in native and exotic honeybee, Apis mellifera L., colonies under Saudi Arabia conditions. Saudi journal of biological sciences, 24(5), 992–995. https://doi.org/10.1016/j.sjbs.2016.12.018.

Al-Ghamdi, A. A., Al-Ghamdi, M. S., Ahmed, A. M., Mohamed, A., Shaker, G. H., Ansari, M. J., Dorrah, M. A., Khan, K. A., & Ayaad, T. H. (2021). Immune investigation of the honeybee Apis mellifera jemenitica broods: A step toward production of a bee-derived antibiotic against the American foulbrood. Saudi journal of biological sciences, 28(3), 1528-1538. https://doi.org/10.1016/j.sjbs.2020.12.026.

Anderson, D. L., & Trueman, J. W. (2000). Varroa jacobsoni (Acari: Varroidae) is more than one species. Experimental & applied acarology, 24(3), 165–189. https://doi.org/10.1023/a:1006456720416.

Brosi, B. J., Delaplane, K. S., Boots, M., & de Roode, J. C. (2017). Ecological and evolutionary approaches to managing honeybee disease. Nature ecology & evolution, 1(9), 1250-1262. https://doi.org/10.1038/s41559-017-0246-z.

Cervo, R., Bruschini, C., Cappa, F., Meconcelli, S., Pieraccini, G., Pradella, D., & Turillazzi, S. (2014). High Varroa mite abundance influences chemical profiles of worker bees and mite-host preferences. The Journal of experimental biology, 217(17), 2998-3001. https://doi.org/10.1242/jeb.099978.

Dainat, B., Evans, J. D., Chen, Y. P., Gauthier, L., & Neumann, P. (2012). Dead or alive: deformed wing virus and Varroa destructor reduce the life span of winter honeybees. Applied and environmental microbiology, 78(4), 981-987. https://doi.org/10.1128/AEM.06537-11.

de Miranda, J. R., Cordoni, G., & Budge, G. (2010). The Acute bee paralysis virus-Kashmir bee virus-Israeli acute paralysis virus complex. Journal of invertebrate pathology, 103 Suppl 1, S30-S47. https://doi.org/10.1016/j.jip.2009.06.014.

Decourtye, A., Alaux, C., Le Conte, Y., Henry, M. (2019). Toward the protection of bees and pollination under global change: present and future perspectives in a challenging applied science. Current Opinion in Insect Science, 35, 123-131. https://doi.org/10.1016/j.cois.2019.07.008.

Dmitryjuk, M., Żołtowska, K., Frączek, R., & Lipiński, Z. (2014). Esterases of Varroa destructor (Acari: Varroidae), parasitic mite of the honeybee. Experimental & applied ácarology, 62(4), 499-510. https://doi.org/10.1007/s10493-013-9754-y.

Eliash, N., & Mikheyev, A. (2020). Varroa mite evolution: a neglected aspect of worldwide bee collapses?. Current Opinion in Insect Science, 39, 21-26. https://doi.org/10.1016/j.cois.2019.11.004.

Evans, J. D., & Cook, S. C. (2018). Genetics and physiology of Varroa mites. Current Opinion in Insect Science, 26,130-135. https://doi.org/10.1016/j.cois.2018.02.005.

Flores, J. M., Gámiz, V., Jiménez-Marín, Á., Flores-Cortés, A., Gil-Lebrero, S., Garrido, J. J., & Hernando, M. D. (2021). Impact of Varroa destructor and associated pathologies on the colony collapse disorder affecting honey bees. Research in veterinary science, 135, 85-95. https://doi.org/10.1016/j.rvsc.2021.01.001.

Frey, E., Odemer, R., Blum, T., & Rosenkranz, P. (2013). Activation and interruption of the reproduction of Varroa destructor is triggered by host signals (Apis mellifera). Journal of invertebrate pathology, 113(1), 56-62. https://doi.org/10.1016/j.jip.2013.01.007.

Fukuto, T. R. (1990). Mechanism of action of organophosphorus and carbamate insecticides. Environmental health perspectives, 87, 245-254. https://doi.org/10.1289/ehp.9087245.

Garedew, A., Schmolz, E., & Lamprecht, I. (2004). The energy and nutritional demand of the parasitic life of the mite Varroa destructor. Apidologie, 35, 419-430. https://doi.org/10.1051/apido:2004032.

González-Cabrera, J., Davies, T. G., Field, L. M., Kennedy, P. J., & Williamson, M. S. (2013). An amino acid substitution (L925V) associated with resistance to pyrethroids in Varroa destructor. PloS one, 8(12), e82941. https://doi.org/10.1371/journal.pone.0082941.

González-Cabrera, J., Rodríguez-Vargas, S., Davies, T. G., Field, L. M., Schmehl, D., Ellis, J. D., Krieger, K., & Williamson, M. S. (2016). Novel Mutations in the Voltage-Gated Sodium Channel of Pyrethroid-Resistant Varroa destructor Populations from the Southeastern USA. PloS one, 11(5), e0155332. https://doi.org/10.1371/journal.pone.0155332.

Grozinger, C. M., & Flenniken, M. L. (2019). Bee Viruses: Ecology, Pathogenicity, and Impacts. Annual review of entomology, 64, 205-226. https://doi.org/10.1146/annurev-ento-011118-111942.

Hamiduzzaman, M. M., Emsen, B., Hunt, G. J., Subramanyam, S., Williams, C. E., Tsuruda, J. M., & Guzman-Novoa, E. (2017). Differential Gene Expression Associated with Honey Bee Grooming Behavior in Response to Varroa Mites. Behavior genetics, 47(3), 335-344. https://doi.org/10.1007/s10519-017-9834-6.

Häußermann, C. K., Ziegelmann, B., & Rosenkranz, P. (2016). Spermatozoa capacitation in female Varroa destructor and its influence on the timing and success of female reproduction. Experimental & applied ácarology, 69(4), 371-387. https://doi.org/10.1007/s10493-016-0051-4.

Hubert, J., Erban, T., Kamler, M., Kopecky, J., Nesvorna, M., Hejdankova, S., Titera, D., Tyl, J., & Zurek, L. (2015). Bacteria detected in the honeybee parasitic mite Varroa destructor collected from beehive winter debris. Journal of applied microbiology, 119(3), 640-654. https://doi.org/10.1111/jam.12899.

Iwasaki, J. M., & Hogendoorn, K. (2021). How protection of honey bees can help and hinder bee conservation. Current Opinion in Insect Science, 46, 112-118. https://doi.org/10.1016/j.cois.2021.05.005.

Khan, K., & Ghramh, H. (2021). An investigation of the efficacy of hygienic behavior of various honey bee (Apis mellifera) races toward Varroa destructor (Acari: Varroidae) mite infestation. Journal of King Saud University - Science, 33 (3) 101393. https://doi.org/10.1016/j.jksus.2021.101393.

Kita, T., Hayashi, T., Ohtani, T., Takao, H., Takasu, H., Liu, G., Ohta, H., Ozoe, F., & Ozoe, Y. (2017). Amitraz and its metabolite differentially activate α- and β-adrenergic-like octopamine receptors. Pest management science, 73(5), 984–990. https://doi.org/10.1002/ps.4412.

Klein, A., Vaissière, B., Cane, J., Steffan-Dewenter, I., Cunningham, S., Kremen, C., Tscharntke, T. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B, 274, 303-313. http://doi.org/10.1098/rspb.2006.3721.

Le Conte, Y., Arnold, G., Trouiller, J., Masson, C., Chappe, B., & Ourisson, G. (1989). Attraction of the parasitic mite varroa to the drone larvae of honey bees by simple aliphatic esters. Science, 245(4918), 638–639. https://doi.org/10.1126/science.245.4918.638.

Le Conte, Y., Ellis, M., & Ritter, W. (2010). Varroa mites and honey bee health: can Varroa explain part of the colony losses?. Apidologie, 41, 353-363. https://doi.org/10.1051/apido/2010017.

Martin, S. J., & Brettell, L. E. (2019). Deformed Wing Virus in Honeybees and Other Insects. Annual review of virology, 6(1), 49–69. https://doi.org/10.1146/annurev-virology-092818-015700.

Martin, S. J., Hawkins, G. P., Brettell, L. E., Reece, N., Correia-Oliveira, M. E., & Allsopp, M. H. (2020). Varroa destructor reproduction and cell re-capping in mite-resistant Apis mellifera populations. Apidologie, 51, 369-381. https://doi.org/10.1007/s13592-019-00721-9.

Martin, S.J. (1994). Ontogenesis of the mite Varroa jacobsoni Oud. in worker brood of the honeybee Apis mellifera L. under natural conditions. Exp Appl Ácarol., 18, 87–100. https://doi.org/10.1007/BF00055033.

Martin, S.J. (1995). Ontogenesis of the mite Varroa jacobsoni Oud. in drone brood of the honeybee

Apis mellifera L. under natural conditions. Exp Appl Ácarol., 19, 199–210. https://doi.org/10.1007/BF00130823.

Masry, S.H.D., Abd El-Wahab, T.E. & Rashad, M. (2020). Evaluating the impact of jatropha oil extract against the Varroa mite, Varroa destructor Anderson & Trueman (Arachnida: Acari: Varroidae), infesting honeybee colonies (Apis mellifera L.). Egypt J Biol Pest Control, 30, 91. https://doi.org/10.1186/s41938-020-00292-3.

McAfee, A., Chapman, A., Iovinella, I., Gallagher-Kurtzke, Y., Collins, T. F., Higo, H., Madilao, L. L., Pelosi, P., & Foster, L. J. (2018). A death pheromone, oleic acid, triggers hygienic behavior in honey bees (Apis mellifera L.). Sci Rep., 8, 5719. https://doi.org/10.1038/s41598-018-24054-2.

Mondet, F., Alaux, C., Severac, D., Rohmer, M., Mercer, A., & Conte, Y. L. (2015). Antennae hold a key to Varroa-sensitive hygiene behaviour in honey bees. Scientific Reports, 5, 10454. https://doi.org/10.1038/srep10454.

Mondet, F., Kim, S., de Miranda, J., Beslay, D., Le Conte, Y., & Mercer, A. R. (2016). Specific Cues Associated With Honey Bee Social Defence against Varroa destructor Infested Brood. Sci Rep., 6, 25444. https://doi.org/10.1038/srep25444.

Nazzi, F., & Le Conte, Y. (2016). Ecology of Varroa destructor, the Major Ectoparasite of the Western Honey Bee, Apis mellifera. Annual review of entomology, 61, 417–432. https://doi.org/10.1146/annurev-ento-010715-023731.

Ollerton, J. (2017). Pollinator diversity: distribution, ecological function, and conservation. Annual Review of Ecology, Evolution and Systematics, 48. https://doi.org/10.1146/annurev-ecolsys-110316-022919.

Palacio, M. A., Figini, E., Ruffinengo, S., Rodríguez, E., Hoyo, M. D., & Bedascarrasbure, E. (2000). Changes in a population of Apis mellifera L. selected for hygienic behaviour and its relation to brood disease tolerance. Apidologie, 31, 471-478. https://doi.org/10.1051/apido:2000139.

Palacio, M. A., Rodriguez, E., Goncalves, L., Bedascarrasbure, E., & Spivak, M. (2010). Hygienic behaviors of honey bees in response to brood experimentally pin-killed or infected with Ascosphaera apis. Apidologie, 41(6), 602-612. https://doi.org/10.1051/apido/2010022.

Plettner, E., Eliash, N., Singh, N.K., Pinnelli, G.R., & Soroker, V. (2017). The chemical ecology of host-parasite interaction as a target of Varroa destructor control agents. Apidologie 48, 78-92. https://doi.org/10.1007/s13592-016-0452-8.

Pritchard, D. (2016). Grooming by honey bees as a component of Varroa resistant behavior. Journal of Apicultural Research, 55, 38-48. https://doi.org/10.1080/00218839.2016.1196016.

Prullage, J. B., Tran, H. V., Timmons, P., Harriman, J., Chester, S. T., & Powell, K. (2011). The combined mode of action of fipronil and amitraz on the motility of Rhipicephalus sanguineus. Veterinary parasitology, 179(4), 302-310. https://doi.org/10.1016/j.vetpar.2011.03.041.

Purves, D., Augustine, G. J., Fitzpatrick, D., Hall, W. C., LaMantia, A.-S., McNamara, J. O., & Williams, S. M. (Eds.). (2004). Neuroscience (3rd ed.). Sinauer Associates.

Ramsey, S. D., Ochoa, R., Bauchan, G., Gulbronson, C., Mowery, J. D., Cohen, A., Lim, D., Joklik, J., Cicero, J. M., Ellis, J. D., Hawthorne, D., & vanEngelsdorp, D. (2019). Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proceedings of the National Academy of Sciences of the United States of America, 116(5), 1792–1801. https://doi.org/10.1073/pnas.1818371116.

Ramsey, S., Gulbronson, C., Mowery, J., Ochoa, R., VanEngelsdorp, D., & Bauchan, G. (2018). A Multi-Microscopy Approach to Discover the Feeding Site and Host Tissue Consumed by Varroa destructor on Host Honey Bees. Microscopy and Microanalysis, 24(S1), 1258-1259. https://doi.org/10.1017/S1431927618006773.

Sajid, Z.N., Aziz, M.A., Bodlah, I., Rana, R., Ghramh, H.A., & Khan, K.A. (2020). Efficacy assessment of soft and hard acaricides against Varroa destructor mite infesting honey bee (Apis mellifera) colonies, through sugar roll method. Saudi Journal of Biological Sciences, 27, 53-59. https://doi.org/10.1016/j.sjbs.2019.04.017.

Spivak, M. (1996). Honey bee hygienic behavior and defense against Varroa jacobsoni. Apidologie 27(4), 245-260. https://doi.org/10.1051/apido:19960407.

Spivak, M., & Danka, R. G. (2021). Perspectives on hygienic behavior in Apis mellifera and other social insects. Apidologie, 52, 1-16. https://doi.org/10.1007/s13592-020-00784-z.

Spivak, M., & Reuter, G. S. (2001). Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior. Apidologie, 32(6), 555-565. https://doi.org/10.1051/apido:2001103.

Tantillo, G., Bottaro, M., Di Pinto, A., Martella, V., Di Pinto, P., & Terio, V. (2015). Virus Infections of Honeybees Apis Mellifera. Italian journal of food safety, 4(3), 5364. https://doi.org/10.4081/ijfs.2015.5364.

Traynor, K. S., Mondet, F., de Miranda, J. R., Techer, M., Kowallik, V., Oddie, M., Chantawannakul, P., & McAfee, A. (2020). Varroa destructor: A Complex Parasite, Crippling Honey Bees Worldwide. Trends in parasitology, 36(7), 592-606. https://doi.org/10.1016/j.pt.2020.04.004.

Vu, P.D., Rault, L., Jenson, L.J., Bloomquist, J., & Anderson, T. (2020). Voltage-gated chloride channel blocker DIDS as an acaricide for Varroa mites. Pesticide biochemistry and physiology, 167, 104603. https://doi.org/10.1016/j.pestbp.2020.104603.

Xie, X., Huang, Z. Y., & Zeng, Z. (2016). Why do Varroa mites prefer nurse bees?. Scientific reports, 6, 28228. https://doi.org/10.1038/srep28228.

Yew, J. Y., & Chung, H. (2015). Insect pheromones: An overview of function, form, and discovery. Progress in lipid research, 59, 88-105. https://doi.org/10.1016/j.plipres.2015.06.001.

Zanni, V., Değirmenci, L., Annoscia, D., Scheiner, R., Nazzi, F. (2018). The reduced brood nursing by mite-infested honey bees depends on their accelerated behavioral maturation. Journal of insect physiology, 109, 47-54. https://doi.org/10.1016/j.jinsphys.2018.06.006.

Ziegelmann, B., & Rosenkranz, P. (2014). Mating disruption of the honeybee mite Varroa destructor under laboratory and field conditions. Chemoecology, 24, 137-144. https://doi.org/10.1007/s00049-014-0155-4.