SECONDARY COMPOUNDS OF PLANTS AND THEIR EFFECT AGAINST THE Varroa destructor MITE

Jesús Humberto Reyna Fuentes, Cecilia Carmela Zapata Campos, José Octavio Merino Charrez, Daniel López Aguirre, Juan Alberto Ascasio Valdéz

Abstract


Background: The honeybee (Apis mellifera L.) represents one of the most important species in the maintenance of ecosystems, since it contributes to crop pollination, which improves crop yields and the reproduction of other plants. However, some factors such as climate change, africanization and various pathological processes, including the presence of the Varroa destructor mite, have led to a decline in A. mellifera populations. Objective: To collect scientific information on the plants used for mite control, as well as the organic derivatives and secondary compounds with bioacaricidal potential used for such control. Main findings: Due to the fact that infestations of this mite have become a major problem, numerous control methods have been developed and tested, mainly based on synthetic acaricides; however, these have generated disadvantages such as the development of resistance and contamination of products such as honey and pollen. Implications: Therefore, it is necessary to implement an organic, environmentally friendly control method that reduces mite populations without developing resistance, and that does not generate contamination of hive sub-products. Conclusions: In general, the most common types of extracts tested were essential oils and hydroalcoholic extracts, which reported mortality ranging from 26.4 to 99.5% on V. destructor. Likewise, some species of plants endemic to Matorral Espinoso Tamaulipeco (MET) have been tested against other arthropods and that could be an important source of components that act as acaricides; however, it is necessary to identify and analyze the secondary compounds, as well as the molecules and their activity on V. destructor.

Keywords


biopesticides; Varroa destructor; bees; health.

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References


Abd El- Wahab, T.E., Shalaby, S.E.M., Al-Kahtani, S.N., Al Naggar, Y., Jamal, Z.A. and Masry, S.H.D., 2021. Mode of application of acaricides against the ectoparasitic mite (Varroa destructor) infesting honeybee colonies, determines their efficiencies and residues in honey and beeswax. Journal of King Saud University. Science, 33(1), p. 101236. https://doi.org/10.1016/j.jksus.2020.101236

Abdelgaleil, S.A.M. and El-Aswad, A.F., 2005. Antifeedant and Growth Inhibitory Effects of Tetranortriterpenoids Isolated from Three Meliaceous Species on the Cotton Leafworm, Spodoptera littoralis (Boisd). Journal of Applied Sciences Research, 1, pp. 234-241.

Aglagane, A., Laghzaoui, E.-M., Soulaimani, B., Er-Rguibi, O., Abbad, A., Mouden, E. H. E. and Aourir, M., 2022. Acaricidal activity of Mentha suaveolens subsp. timija, Chenopodium ambrosioides, and Laurus nobilis essential oils, and their synergistic combinations against the ectoparasitic bee mite, Varroa destructor (Acari: Varroidae). Journal of Apicultural Research, 61(1), pp. 9-18. https://doi.org/10.1080/00218839.2021.1898787

Aguiar, C.M.L., Santos, G.M.M., Martins, C.F. and Presley, S.J., 2013. Trophic niche breadth and niche overlap in a guild of flower-visiting bees in a Brazilian dry forest. Apidologie, 44 (2), pp. 153-162. http://doi.org/10.1007/s13592-012-0167-4

Ahsaei, S.M., Rodríguez-Rojo, S., Salgado, M., Cocero, M. J., Talebi-Jahromi, K. and Amoabediny, G., 2020. Insecticidal activity of spray dried microencapsulated essential oils of Rosmarinus officinalis and Zataria multiflora against Tribolium confusum. Crop Protection, 128(104996), pp. 1-35. https://doi.org/10.1016/j.cropro.2019.104996

Ainane, A., Khammour, F., Charaf, S., Elabboubi, M., Elkouali, M., Talbi, M., Benhima, R., Cherroud, S. and Ainane, T., 2019. Chemical composition and insecticidal activity of five essential oils: Cedrus atlantica, Citrus limonum, Rosmarinus officinalis, Syzygium aromaticum and Eucalyptus globules. Materials Today: Proceedings, 13; pp. 474-485. https://doi.org/10.1016/j.matpr.2019.04.004

Aizen, M.A., Garibaldi, L.A., Cunningham, S.A. and Klein, A.M., 2009. How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Annals of Botany, 103(9), pp. 1-10 https://doi.org/10.1093/aob/mcp076

Al Toufailia, H., Scandian, L., Shackleton, K. and Ratnieks, F. L. W., 2018. Towards integrated control of varroa: 4) varroa mortality from treating broodless winter colonies twice with oxalic acid via sublimation. Journal of Apicultural Research, 57(3), pp. 438-443. https://doi.org/10.1080/00218839.2018.1454035

Alanís, E., Jiménez, J., González, M. A., Yerana J. I., Cuellar, L. G. and Mora-Olivo, A., 2013. Análisis de la vegetación secundaria del matorral espinoso tamaulipeco, México. Phyton, Revista Internacional de Botánica Experimental, 82, pp. 185-191. http://www.scielo.org.ar/scielo.php?script=sci_arttext&pid=S1851-56572013000200005

Almeida Filho, L. C., de Souza, T. M., Tabosa, P. M., Soares, N. G., Rocha-Bezerra, L. C., Vasconcelos, I. M. and Carvalho, A. F., 2017. Trypsin inhibitor from Leucaena leucocephala seeds delays and disrupts the development of Aedes aegypti, a multiple-disease vector: Effect of trypsin inhibitor from L. leucocephalaseeds on Ae. aegypti. Pest Management Science, 73(1), pp. 181-187. https://doi.org/10.1002/ps.4284

Alonso-Salces, R.M., Cugnata, N.M., Guaspari, E., Pellegrini, M.C., Aubone, I., De Piano, F.G., Antunez, K. and Fuselli, S.R., 2017. Natural Strategies for the Control of Paenibacillus larvae, the Causative Agent of American Foulbrood in Honeybees: A Review. Apidologie, 48 (3), pp. 387-400. https://doi.org/10.1007/s13592-016-0483-1

Antunez, K., Invernizzi, C., Mendoza, Y., vanEngelsdorp, D. and Zunino, P., 2017. Honeybee colony losses in Uruguay during 2013-2014. Apidologie, 48 (3), pp. 364-370. https://doi.org/10.1007/s13592-016-0482-2

Ariana, A., Ebadi, R. and Tahmasebi, G., 2002. Laboratory evaluation of some plant essences to control Varroa destructor (Acari: Varroidae). Experimental Apply Acarology, 27, pp. 319-327. http://doi.org/10.1023/A:1023342118549

Bahreini, R., Nasr, M., Docherty, C., de Herdt, O., Muirhead, S. and Feindel, D., 2020. Evaluation of potential miticide toxicity to Varroa destructor and honeybees, Apis mellifera, under laboratory conditions. Scientific Reports, 10(1), pp. 1-15. https://doi.org/10.1038/s41598-020-78561-2

Bahreini, R., Nasr, M., Docherty, C., Feindel, D., Muirhead, S. and de Herdt, O. 2021. New bioassay cage methodology for in vitro studies on Varroa destructor and Apis mellifera. PloS One, 16(4), e0250594. https://doi.org/10.1371/journal.pone.0250594

Bava, R., Castagna, F., Palma, E., Musolino, V., Carresi, C., Cardamone, A., Lupia, C., Marrelli, M., Conforti, F., Roncada, P., Musella, V. and Britti, D., 2022. Phytochemical Profile of Foeniculum vulgare Subsp. piperitum Essential Oils and Evaluation of Acaricidal Efficacy against Varroa destructor in Apis mellifera by In Vitro and Semi-Field Fumigation Tests. Veterinary Sciences, 9(12), pp. 684-695. https://doi.org/10.3390/vetsci9120684

Becsi, B., Formayer, H. and Brodschneider, R., 2021. A biophysical approach to assess weather impacts on honeybee colony winter mortality. Royal Society Open Science, 8(9), pp. 1-19. https://doi.org/10.1098/rsos.210618

Bedini, S. Flamini, G. Girardi, J. Cosci, F. and Conti, B., 2015. Not just for beer: Evaluation of spent hops (Humulus lupulus L.) as a source of eco-friendly repellents for insect pests of stored foods. Journal of Pest Science, 88, pp. 583-592. http://doi.org/10.1007/s10340-015-0647-1

Bendifallah, L., Belguendouz, R., Hamoudi, L. and Arab, K., 2018. Biological Activity of the Salvia officinalis L. (Lamiaceae) Essential Oil on Varroa destructor Infested Honeybees. Plants, 7(2), pp. 1-12 https://doi.org/10.3390/plants7020044

Bogdanov, S., Charrire, J.D., Imdorf, A., Kilchenmann, V. and Fluri, P., 2002. Determination of residues in honey after treatments with formic and oxalic acid under field conditions. Apidologie, 33(4), pp. 399-409. https://doi.org/10.1051/apido:2002029

Brahmachari, G., Gorai, D. and Roy, R., 2013. Argemone mexicana: chemical and pharmacological aspects. Revista Brasileira de Farmacognosia Brazilian Journal of Pharmacognosy, 23, pp. 559-575.

Brown, P., Newstrom-Lloyd, L. E., Foster, B. J., Badger, P. H. and McLean, J. A., 2018. Winter 2016 honeybee colony losses in New Zealand. Journal of Apicultural Research, 57(2), pp. 278-291. https://doi.org/10.1080/00218839.2018.1430980

Calderone, N.W., 1999. Effective fall treatment of Varroa jacobsoni (Acari: Varroidae) with a new formulation of formic acid in colonies of Apis mellifera (Hymenoptera: Apidae) in the northeastern United States. Journal of Economic Entomology, 93(4), pp. 1065-1075. https://doi.org/10.1603/0022-0493-93.4.1065

Castellanos-Potenciano, B. 2017. Spatio-temporal mobility of apiculture affected by the climate change in the beekeeping of the Gulf of Mexico. Applied Ecology and Environmental Research, 15(4), pp. 163-175. https://doi.org/10.15666/aeer/1504_163175

Cavazos, P., Gonzalez, D., Lanorio, J. and Ynalvez, R. 2021. Secondary metabolites, antibacterial and antioxidant properties of the leaf extracts of Acacia rigidula benth. and Acacia berlandieri benth. SN Applied Sciences, 3, pp. 1-14. https://doi.org/10.1007/s42452-021-04513-8

Charrière, J. D., Imdorf, A. and Kuhn, R., 2004. Bee tolerance of different winter Varroa treatments. Schweizerische Bienen-Zeitung, 127, pp. 19-23.

Charriére, J. D. and Imdorf, A., 2002. Oxalic acid treatment by trickling against Varroa destructor: recommendations for use in central Europe and under temperate climate conditions. Bee World, 83(2), pp. 51-60. https://doi.org/10.1080/0005772x.2002.11099541

Chauhan, A., Dabhi, M. V. and Jyotshna, R., 2021. Review on Varroa mite: An invasive threat to apiculture industry. Journal of Entomology and Zoology Studies, 9(1), pp. 535-539. https://www.entomoljournal.com/archives/2021/vol9issue1/PartH/8-6-330-518.pdf

Chen, G., Wang, S., Jia, S., Feng, Y., Hu, F., Chen, Y. and Zheng, H., 2021. A new strain of virus discovered in China specific to the parasitic mite Varroa destructor poses a potential threat to honeybees. Viruses, 13(4), pp. 1-16. https://doi.org/10.3390/v13040679

Cimmino, A., Freda, F., Santoro, E., Superchi, S., Evidente, A., Cristofaro, M. and Masi, M., 2021. ?-Costic acid, a plant sesquiterpene with acaricidal activity against Varroa destructor parasitizing the honey bee. Natural Product Research, 35(9), pp. 1428-1435. https://doi.org/10.1080/14786419.2019.1652291

Clements, J., Groves, R. L., Cava, J., Barry, C. C., Chapman, S. and Olson, J. M. 2019. Conjugated linoleic acid as a novel insecticide targeting the agricultural pest Leptinotarsa decemlineata. PloS One, 14(11), p. e0220830. https://doi.org/10.1371/journal.pone.0220830

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

Conti, B., Bocchino, R., Cosci, F., Ascrizzi, R., Flamini, G. and Bedini, S., 2020. Essential oils against Varroa destructor: a soft way to fight the parasitic mite of Apis mellifera. Journal of Apicultural Research, 59, pp. 774-782. https://doi.org/10.1080/00218839.2020.1790790

Cornelissen, B., Neumann, P. and Schweiger, O., 2019. Global warming promotes biological invasion of a honeybee pest. Global Change Biology, 25(11), pp. 3642-3655. https://doi.org/10.1111/gcb.14791

Cunha, M.S., Cardoso, D.C., Cristiano, M.P., de Oliveira Campos, L.A. and Lopes, D.M., 2021. The Bee Chromosome database (Hymenoptera: Apidae). Apidologie, 52 (2), pp. 493-502. https://doi.org/10.1007/s13592-020-00838-2

Cunningham, M.M., Tran, L., McKee, C.G., Ortega, R., Newman, T., Lansing, L., Griffiths, J.S., Bilodeau, G.J., Rott, M. and Guarna, M., 2022. Honey bees as biomonitors of environmental contaminants, pathogens, and climate change. Ecological Indicators, 134(108457), 108457. https://doi.org/10.1016/j.ecolind.2021.108457

Currie, R.W., Pernal, S.F. and Guzmán-Novoa, E. 2010. Honeybee colony losses in Canada. Journal of apicultural research, 49 (1), pp. 104-106. https://doi.org/10.3896/ibra.1.49.1.18

Damiani, N., Gende, L.B., Bailac, P., Marcangeli, J.A. and Eguaras, M.J., 2009. Acaricidal and insecticidal activity of essential oils on Varroa destructor (Acari: Varroidae) and Apis mellifera (Hymenoptera: Apidae). Parasitology Research,106, pp. 145-152. http://doi.org/10.1007/s00436-009-1639-y

Damiani, N., Fernández, N.J., Porrini, M.P., Gende, L.B., Álvarez, E., Buffa, F., Brasesco, C., Maggi, M.D., Marcangeli, J. A. and Eguaras, M.J., 2014. Laurel leaf extracts for honeybee pest and disease management: antimicrobial, microsporicidal, and acaricidal activity. Parasitology Research, 113(2), pp. 701-709. https://doi.org/10.1007/s00436-013-3698-3

De Jong, D., Morse, R.A. and Eickwort, G.C. 1982. Mite pests of honeybees. Annual Review of Entomology, 27, pp. 229-252. http://doi.org/10.1146/annurev.en.27.010182.001305

Delgado-Núñez, E.J., Zamilpa, A., González-Cortazar, M., Olmedo-Juárez, A., Cardoso-Taketa, A., Sánchez-Mendoza, E., Tapia-Maruri, D., Salinas-Sánchez, D.O. and Mendoza-de Gives, P., 2020. Isorhamnetin: A nematocidal flavonoid from Prosopis laevigata leaves against Haemonchus contortus eggs and larvae. Biomolecules, 10, pp. 773-790. https://doi.org/10.3390/biom10050773

Dimetry, N.Z., El-Wahab, T.E. and Zakaria, M.E., 2005. Effective control of Varroa mite Varroa destructor Anderson and Trueman infesting honeybee colonies Apis mellifera by some natural products. Bulletin Faculty of Agriculture-Cairo University, 56, pp. 295-308.

Dodolo?lu, A. and Emsen, B. 2007. Effect of Supplementary Feeding on Honeybee Colony. Journal of Applied Animal Research, 32, pp. 199-200. http://doi.org/10.1080/09712119.2007.9706878

Domínguez-Gómez, G., González-Rodríguez, H., Ramírez-Lozano, R., Estrada-Castillon, A., Cantú-Silva, I., Gómez-Meza, M., Villareal-Quintana, J. and Alanís-Flores, G., 2013. Diversidad estructural del matorral espinoso tamaulipeco durante las épocas seca y húmeda. Revista Mexicana de Ciencias Forestales, 4, pp. 106-122.

Eguaras, M., Del Hoyo, M., Palacio, M.A., Ruffinengo, S. and Bedascarrasbure, E. L., 2008. A new product with formic acid for Varroa jacobsoni oud. Control in Argentina. I. efficacy: Efficacy of new product for V. jacobsoni control. Journal of Veterinary Medicine. B, Infectious Diseases and Veterinary Public Health, 48 (1), pp, 11-14. https://doi.org/10.1111/j.1439-0450.2001.00418.x

El Zalabani, S.M., El-Askary, H.I., Mousa, O.M., Issa, M.Y., Zaitoun, A.A. and Abdel-Sattar, E., 2012. Acaricidal activity of Swietenia mahogani and Swietenia macrophylla ethanolic extracts against Varroa destructor in honeybee colonies. Experimental Parasitology, 130(2), pp.166-170. http://doi.org/10.1016/j.exppara.2011.10.013

El-Gendy, R. and Sakla, R., 2022. Efficacy of Carum carvi essential oil against the parasitic varroa mite and its impact on honeybee Apis mellifera L. Catrina: The International Journal of Environmntal Sciences, 25 (1), pp. 17-26. https://doi.org/10.21608/cat.2022.134943.1124

Ellaithy, A., Abdel-khalek, A. and Mohammed, M., 2021. Castor bean plant, Ricinus communis, containing the potent biopesticide ricinine, as an alternative host for mass rearing process of Tetranychus urticae and the most common phytoseiid predators. Egyptian Journal of Chemistry, 65(6), pp. 535-549. https://doi.org/10.21608/ejchem.2021.107114.4922

Ellis, J.D., Delaplane, K.S. and Hood, W.M., 2001. Efficacy of a bottom screen device, Apistan®, and Apilife VAR®, in controlling Varroa destructor. The American Bee Journal, 141, pp. 813-816.

Elzen, P.J, Westervelt, D and Lucas, R., 2004. Formic acid treatment for control of Varroa destructor (Mesostigmata: Varroidae) and safety to Apis mellifera (Hymenoptera: Apidae) under southern United States conditions. Journal of Economic Entomology, 97, pp. 1509-1512. http://doi.org/10.1603/0022-0493-97.5.1509

Elzen, P.J., Baxter, J.R., Spivak, M. and Wilson, W.T., 2000. Control of Varroa jacobsoni Oud resistant to fluvalinate and amitraz using coumaphos. Apidologie, 31, pp. 437-441. http://doi.org/10.1051/apido:2000134

Enan, E.E., 1998. Insecticidal action of terpenes and phenols to the cockroaches: effect on octopamine receptors. International Symposium on Crop Protection, Gent, Belgium, May.

Erenler, R., Sen, O., Aksit, H., Demirtas, I., Yaglioglu, A.S., Elmastas, M. and Telci, ?., 2016. Isolation and identification of chemical constituents from Origanum majorana and investigation of antiproliferative and antioxidant activities: Isolation and identification of chemical constituents from Origanum majorana. Journal of the Science of Food and Agriculture, 96(3), pp. 822-836. https://doi.org/10.1002/jsfa.7155

Espinosa-Montaño, L.G. and Guzmán-Novoa, E. 2007. Eficacia de dos acaricidas naturales, ácido fórmico y timol, para el control del ácaro Varroa destrucor de las abejas (Apis mellifera L.) en Villa Guerrero, Estado de México, México. Veterinaria México, 38(1), pp. 9-19.

Eviner, V.T. 2003. Functional matrix: a conceptual framework for predicting multiple plant effects on ecosystem processes. Annual Review Ecology, Evolution and Systematics, 34, pp. 455-485. http://doi.org/10.1146/annurev.ecolsys.34.011802.132342

Fernández-Salas, A., Alonso-Díaz, M. A., Acosta-Rodríguez, R., Torres-Acosta, J.F.J., Sandoval-Castro, C.A. and Rodríguez-Vivas, R.I., 2011. In vitro acaricidal effect oftannin-rich plants against the cattle tick Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Veterinary Parasitology. 175, pp. 113-118. https://doi.org/10.1016/j.vetpar.2010.09.016

Flores, J.M., Gil-Lebrero, S., Gámiz, V., Rodríguez, M.I., Ortiz, M.A. and Quiles, F.J., 2019. Effect of the climate change on honey bee colonies in a temperate Mediterranean zone assessed through remote hive weight monitoring system in conjunction with exhaustive colonies assessment. The Science of the Total Environment, 653, pp. 1111-1119. https://doi.org/10.1016/j.scitotenv.2018.11.004

Foroughbakhch, R., G. Reyes, R., Alvarado, M.A., Hernández, J.L. and Rocha, A., 2005. Use of quantitative methods to determine leaf biomass on 15 woody shrub species in northeastern Mexico. Forest Ecology and Management, 216, pp. 359-366. http://doi.org/10.1016/j.foreco.2005.046

Fries, I., Wallner, K. and Rosenkranz, P., 1998. Effects on Varroa jacobsoni from acaricides in beeswax. Journal of Apiculture Research, 37, pp. 85-90. http://doi.org/10.1080/00218839.1998.111009599

Galindo-Cardona, A., Scannapieco, A.C., Russo, R., Escalante, K., Geria, M., Lepori, N., Ayup, M.M., Muntaabski, I., Liendo, M.C., Landi, L., Giray, T. and Monmany-Garzia, A.C., 2020., Varroa destructor parasitism and genetic variability at honeybee (Apis mellifera) drone congregation areas and their associations with environmental variables in Argentina. Frontiers in ecology and evolution, 8. https://doi.org/10.3389/fevo.2020.590345

Gallai, N., Salles, J.M., Settele, J. and Vaissière, B.E., 2009. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecology Economic, 68, pp. 810-821. https://doi.org/10.1016/j.ecolecon.2008.06.014

Gallardo-López, F., Castellanos-Potenciano, B. P., Díaz-Padilla, G., Pérez-Vázquez, A., Landeros-Sánchez, C. and Sol-Sánchez, Á. 2021. Disonancia cognitiva ante el cambio climático en apicultores: un caso de estudio en México. Revista Mexicana de Ciencias Pecuarias, 12(1), pp. 238-255. https://doi.org/10.22319/rmcp.v12i1.5213

Garcia-Campoy, A., Garcia, E. and Muñiz-Ramirez, A., 2020. Phytochemical and pharmacological study of the Eysenhardtia genus. Plants, 9, pp. 1124-1131. https://doi.org/10.3390/plants9091124

Garrido, C. and Rosenkranz, P., 2003. The reproductive program of female Varroa destructor mites is triggered by its host, Apis mellifera. Experimental and Applied Acaroly, 31, pp. 269-273. https://doi.org/10.1023/b:appa.0000010386.10686.9f

Gashout, H. and Guzman-Novoa, E., 2009. Acute toxicity of essential oils and other natural compounds to the parasitic mite, Varroa destructor, and to larval and adult worker honeybees (Apis mellifera L.). Journal of Apiculture Research, 48, pp. 263-269. http://doi.org/10.3896/IBRA.1.48.4.06

Gashout, H., Guzman-Novoa, E., Goodwin, P.H. and Correa-Benítez, A., 2020. Impact of sublethal exposure to synthetic and natural acaricides on honeybee (Apis mellifera) memory and expression of genes related to memory. Journal of Insect Physiology, 121, pp. 1-8. https://doi.org/10.1016/j.jinsphys.2020.104014

Genath, A., Sharbati, S., Buer, B., Nauen, R. and Einspanier, R., 2020. Comparative transcriptomics indicates endogenous differences in detoxification capacity after formic acid treatment between honey bees and varroa mites. Scientific Reports. 10, pp. 1-14. http://doi.org/10.1038/s41598-020-79057-9

Genath, A., Petruschke, H., von Bergen, M. and Einspanier, R., 2021. Influence of formic acid treatment on the proteome of the ectoparasite Varroa destructor. PloS One, 16(10), p. e0258845. https://doi.org/10.1371/journal.pone.0258845

Giacobino, A., Pacini, A., Molineri, A., Bulacio Cagnolo, N., Merke, J., Orellano, E., Bertozzi, E., Masciangelo, G., Pietronave, H. and Signorini, M., 2017. Environment or beekeeping management: What explains better the prevalence of honeybee colonies with high levels of Varroa destructor? Research in Veterinary Science, 112, pp. 1-6. https://doi.org/10.1016/j.rvsc.2017.01.001

Gómez-Calvario, V., Ramírez-Cisneros, M. Á., Acevedo-Quiroz, M. and Rios, M. Y., 2019. Chemical composition of Helietta parvifolia and its in vitro anticholinesterase activity. Natural Product Research, 33(6), pp. 889-892. https://doi.org/10.1080/14786419.2017.1410808

Go?mez-Flores, R.H., Gracia-Va?zquez, Y.A., Alani?s-Guzma?n, M.G., Tamez-Guerra, R., Garci?a-Di?az, C.L., Monreal-Cuevas, E., and Rodri?guez-Padilla, C., 2009. In Vitro antimicrobial activity and polyalkaloids content of tender and mature Ebenopsis ebano seeds. Medicinal Plants, 1, pp. 11-19.

Gorlenko, C.L., Kiselev, H.Y., Budanova, E.V., Zamyatnin, A.A. and Ikryannikova, L.N., 2020. Plant secondary metabolites in the battle of drugs and drug-resistant bacteria: new heroes or worse clones of antibiotics? Antibiotics, 9, p. 170. https://doi.org/10.3390/antibiotics9040170

Granados-Montelongo, J. A., Núñez-Colima, J. A., Trujillo-Zacarías, I., Cano del Toro, J., Chan-Chablefirma, R. J. and Hidalgo de León, A. 2021. Extracto de Acacia farnesiana para el control de larva de Aedes aegypti. Nova Scientia, 13, pp. 1-20. https://doi.org/10.21640/ns.v13i27.2840

Gray, A., Adjlane, N., Arab, A., Ballis, A., Brusbardis, V., Charrière, J.D., Chlebo, R., Coffey, M.F., Cornelissen, B., Amaro da Costa, C., Dahle, B., Danihlík, J., Draži?, M.M., Evans, G., Fedoriak, M., Forsythe, I., Gajda, A., de Graaf, D.C., Gregorc, A. and Brodschneider, R., 2020. Honeybee colony winter loss rates for 35 countries participating in the COLOSS survey for winter 2018-2019, and the effects of a new queen on the risk of colony winter loss. Journal of Apicultural Research, 59, pp. 744-751. https://doi.org/10.1080/00218 839.2020.1797272

Gregorc, A. and Planinc, I., 2012. Use of thymol formulations, amitraz, and oxalic acid for the control of the varroa mite in honey bee (Apis mellifera carnica) colonies. Journal of Apicultural Science, 56, pp. 61-69. http://dx.doi.org/10.2478/v10289-012-0024-8

Gregorc, A., Knight, P.R. and Adamczyk, J., 2017. Powdered sugar shake to monitor and oxalic acid treatments to control varroa mites (Varroa destructor Anderson and Trueman) in honey bee (Apis mellifera) colonies. Journal of Apicultural Research, 56, pp. 71-75. https://doi.org/10.1080/00218839.2017.1278912

Halliwell, B., 2006. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiology, 141, pp. 312-322. https://doi.org/10.1104/pp.106.077073.

Häußermann, C.K., Giacobino, A., Munz, R., Ziegelmann, B., Palacio, M.A. and Rosenkranz, P., 2020. Reproductive parameters of female Varroa destructor and the impact of mating in worker brood of Apis mellifera. Apidologie, 51, pp. 342-355. http://doi.org/10.1007/s13592-019-00713-9

Häußermann, C.K., Ziegelmann, B. and Rosenkranz, P., 2018. Spermatozoa production in male Varroa destructor and its impact on reproduction in worker brood of Apis mellifera. Experimental and Applied Acarology, 74, pp. 43-54. https://doi.org/10.1007/s10493-018-0216-4

Hegland, S.J., Nielsen, A., Lázaro, A., Bjerknes, A.L. and Totland, Ø., 2009. How does climate warming affect plant-pollinator interactions? Ecology Letters, 12, pp. 184-195. https://doi.org/10.1111/j.1461-0248.2008.01269.x

Hernández-Alvarádo, J., Zaragóza-Bastida, A., López-Rodríguez, G., Peláez-Acero, A., Olmedo-Juárez, A. and Rivero-Perez, N., 2018. Actividad antibacteriana y sobre nematodos gastrointestinales de metabolitos secundarios vegetales: enfoque en Medicina Veterinaria. Abanico Veterinario, 8, pp. 14-27. https://doi.org/10.21929/abavet2018.81.1

Higes, M., Martín-Hernández, R., Garrido-Bailón, E., González-Porto, A. V., García-Palencia, P., Meana, A., Del Nozal, M.J., Mayo, R. and Bernal, J. L., 2009. Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environmental Microbiology Reports, 1, pp. 110-113. https://doi.org/10.1111/j.1758-2229.2009.00014.x

Higes, M., Martin-Hernandez, R., Hernandez-Rodriguez, C.S. and Gonzalez-Cabrera, J., 2020. Assessing the resistance to acaricides in Varroa destructor from several Spanish locations. Parasitology Research. 119, pp. 3595-3601. https://doi.org/10.1007/s00436-020-06879-x

Huang, Q., Liu, X., Zhao, G., Hu, T. and Wang, Y., 2018. Potential and challenges of tannins as an alternative to in-feed antibiotics for farm animal production. Animal Nutrition, 4, pp. 137-150. http://doi.org/10.1016/j.aninu.2017.09.004

Ifantidis, M. O., 1983. Ontogenesis of the mite Varroa jacobsoni Oudemans in worker and drone brood cells of the honeybee Apis mellifera cecropia. Journal of Apiculture Research, 3, pp. 200-206. http://doi.org/10.1080/00218839.1983.11100588

Ifantidis, M.D., 1990. Reexamination of reproduction parameters of the mite Varroa jacobsoni Oudemans. In: Ritter W, Laere van O, Jacobs F, Wael de L (eds) Proc intern symposium on recent research on Bee pathology, Gent 1990. Janssen Pharmaceutica, Beerse, Belgium, pp 20-26.

Iglesias, A.E., Fuentes, G., Mitton, G., Ramos, F., Brasesco, C., Manzo, R., Orallo, D., Gende, L., Eguaras, M., Ramirez, C., Fanovich, A. and Maggi, M., 2022. Hydrolats from Humulus lupulus and Their Potential Activity as an Organic Control for Varroa destructor. Plants, 11(23), p. 3329. https://doi.org/10.3390/plants11233329

Iglesias, A., Mitton, G., Szawarski, N., Cooley, H., Ramos, F., Meroi-Arcerito, F.R., Brasesco, C., Ramirez, C., Gende, L. and Eguaras, M.J., 2020. Essential oils from Humulus lupulus as novel control agents against Varroa destructor. Industrial Crops and Products,158, p. 113043. http://doi.org/10.1016/j.indcrop.2020.113043

Imdorf, A., Bogdanov, S.O., Choa, R.I. and Calderone, N.W. 1999. Use of essential oils for the control of V. jacobsoni Oud in honeybee colonies. Apidologie, 30, pp. 209-228. https://hal.science/hal-00891579/document

Imdorf, A., Kilchenmann, V. and Berger, T., 2006. Toxic effects of essential oils and some of their components on Varroa destructor oud and Apis mellifera L under laboratory conditions. Eidgenössische Forschungsanstaltf. Milchwirtschaft. https://agris.fao.org/agris-search/search.do?recordID=CH2006000172

Isman, M.B., Miresmailli, S. and Machial, C., 2011. Commercial opportunities for pesticides based on plant essential oils in agriculture, industry, and consumer products. Phytochemistry Reviews, 10, pp. 197-204. http://dx.doi.org/10.1007/s11101-010-9170-4

Jack, C.J. and Ellis, J.D., 2021. Integrated Pest Management control of Varroa destructor (Acari: Varroidae), the most damaging pest of (Apis mellifera L. (Hymenoptera: Apidae)) colonies. Journal of Insect Science, 21(5), p. 6. https://doi.org/10.1093/jisesa/ieab058

Juárez-García, J., Sanzón-Gómez, D., Ramírez-Santoyo, L. and Gonzales- Castañeda, J., 2020. REVISIO?N: El ge?nero argemone (papaveraceae) y los usos para el control de plagas en el sector agri?cola. Ciencia e Innovación Agroalimentaria de la Universidad de Guanajuato, 1, pp, 71-83. http://reiagro.ugto.mx/images/pdf/vol2/2/5-Juarez-Garcia-et-al-2020-El-genero-Argemone-y-el-sector-agricola.pdf

Kamler, M., Nesvorna, M., Stara, J., Erban, T. and Hubert, J., 2016. Comparison of tau-fluvalinate, acrinathrin, and amitraz effects on susceptible and resistant populations of Varroa destructor in a vial test. Experimental & Applied Acarology, 69, pp. 1-9. https://doi.org/10.1007/s10493-016-0023-8

Kanga, L.H.B., Adamczyk, J., Marshall, K. and Cox, R., 2010. Monitoring for resistance to organophosphorus and pyrethroid insecticides in Varroa mite populations. Journal of Economic Entomology, 105, pp. 1797-1802. https://doi.org/10.1603/ec10064

Klein, A.M., Vaissière, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C. and Tscharntke, T,. 2007. Importance of pollinators in changing landscapes for world crops. Proceedings Biological Sciences, 274, pp. 95-96. https://doi.org/10.1098/rspb.2006.3721.191

Kodjo, T.A., Gbénonchi, M., Sadate, A., Komi, A., Yaovi, G., Dieudonné, M. and Komla, S., 2011. Bio-insecticidal effects of plant extracts and oil emulsions of Ricinus communis L. ((Malpighiales: Euphorbiaceae) on the diamondback, Plutella xylostella L. ((Lepidoptera: Plutellidae). Journal of Applied Bioscience, 43, p. 2899-2914. https://m.elewa.org/JABS/2011/43/3.pdf

Koleoglu, G., Goodwin, P.H., Reyes-Quintana, M., Hamiduzzaman, M.M. and Guzman-Novoa, E., 2018. Varroa destructor parasitism reduces hemocyte concentrations and prophenol oxidase gene expression in bees from two populations. Parasitology Research, 117, pp. 1175-1183. http://doi.org/10.1007/s00436-018-5796-8

Kuenen, L.P.S. and Calderone, N.W., 1997. Transfers of Varroa mites from newly emerged bees: preferences for age and function-specific adult bees (Hymenoptera: Apidae). Journal of Insects Behaviour, 10, pp. 213-228. http://doi.org/10.1007/BF02765554

Kulhanek, K., Steinhauer, N., Rennich, K., Caron, D.M., Sagili, R.R., Pettis, J.S., Ellis, J.D., Wilson, M.E., Wilkes, J.T. and Tarpy, D.R., 2017. A national survey of managed honey bee 2015-2016 annual colony losses in the USA. Journal of Apiculture Research, 56, pp. 328-340. http://doi.org/10.1080/00218839.2017.1344496

Langowska, A., Micha?, Z., Sparks, T.H., Adam, G. and Peter, W.T., 2016. Long-Term Effect of Temperature on Honey Yield and Honeybee Phenology. International Journal of Biometeorology, 61, pp. 1125-1132. http://doi.org/10.1007/s00484-016-1293-x

Larayetan, R., Ololade, Z., Ogunmola, O. and Ladokun, A., 2019. Phytochemical constituents, antioxidant, cytotoxicity, antimicrobial, antitrypanosomal, and antimalarial potentials of the crude extracts of Callistemon citrinus. Evid-Based Complement Alternative Medicine, 2019, p. e5410923. https://doi.org/10.1155/2019/5410923

Le Conte, Y., Ellis, M. and Ritter, W., 2010. Varroa mites and honeybee health: can Varroa explain part of the colony losses? Apidologie, 41, pp. 353-363. http://doi.org/10.1051/apido/2010017

Lima, R.K., Graças-Cardoso, M., Campos-Moraes, J., Malfitano-Carvalho, S., Gregório-Rodrigues, V. and Lima-Guimarães, L.G., 2011. Chemical composition and fumigant effect of essential oil of Lippia sidoides cham. and monoterpenes against Tenebrio molitor (l.) (Coleoptera: Tenebrionidae). Ciência e Agrotecnologia 35, pp. 664-671. http://dx.doi.org/10.1590/S1413-70542011000400004

Lindberg, C., Melathopoulos, A. and Winston, M., 2000. Laboratory evaluation of miticides to control Varroa jacobsoni (Acari: Varroidae), a honeybee (Hymenoptera: Apidae) parasite. Journal of Economy Entomology, 93, pp. 189-198. http://doi.org/10.1603/0022-0493-93.2.189

Magaña-Magaña, M., Aguilar, A., Lara y Lara. P. and Sanginés, G.R., 2007. Caracterización socioeconómica de la actividad apícola en el estado de Yucatán, México. Agronomía, Universidad de Caldas, Colombia, 15, pp. 17-24.

Maggi, M., Tourn, E., Negri, P., Szawarski, N., Marconi, A., Gallez, L., Medici, S., Ruffinengo, S., Brasesco, C., De Feudis, L., Quintana, S., Sammataro, D. and Eguaras, M., 2016. A new formulation of oxalic acid for Varroa destructor control applied in Apis mellifera colonies in the presence of brood. Apidologie, 47, pp. 596-605. https://doi.org/10.1007/s13592-015-0405-7

Mahir, M. C. 2018. Effectiveness of combining certain biotechnical methods with thymol treatment against Varroa destructor infestation. African Journal of Agricultural Research, 13, pp. 2735-2740. https://doi.org/10.5897/ajar2018.13572

Mahmood, R., Asad, S., Raja, S., Atta-ul-Moshin, Wagchoure, E.S., Sarwar, G.R., Islam, N. and Ahmad, W., 2014. Control of Varroa destructor (Acari: Varroidae) in Apis mellifera (Hymenoptera: Apidae) by using plant oils and extract. Pakistan Journal of Zoology, 46, pp. 609-615.

Martin, S., 1994. Ontogenesis of the mite Varroa jacobsoni Oud. in worker brood of the honeybee Apis mellifera L. under natural conditions. Experimental Applied Acarology, 18, pp. 87-100. http://doi.org/10.1007/BF00055033

Martinez-Velazquez, M., Rosario-Cruz, R., Castillo-Herrera, G., Flores-Fernandez, J.M., Alvarez, A.H. and Lugo-Cervantes, E., 2011. Acaricidal effect of essential oils from Lippia graveolens (Lamiales: Verbenaceae), Rosmarinus officinalis (Lamiales: Lamiaceae), and Allium sativum (Liliales: Liliaceae) against Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Journal of Medical Entomology, 48(4), pp. 822-827. https://doi.org/10.1603/me10140

Mattila, H.R. and Otis, G.W., 2000. The efficacy of Apiguard against varroa and tracheal mites, and its effect on honey production: 1999 trial. The American Bee Journal, 140, pp. 969-973.

Maya-Martínez, O., Medina-Flores, C., Aquino-Pérez, G., Olmos-Oropeza, G. and López-Carlos, M., 2020. Tratamiento estacional con amitraz contra Varroa destructor y sus efectos en colonias de Apis mellifera. Abanico Veterinario, 10 pp. 1-13. https://doi.org/10.21929/abavet2020.38

Mazeed, A. and El-Solimany, E., 2020. Garlic, Allium sativum L. and Onion, Allium cepa L. as a Potent Anti-mite Varroa destructor, Parasited on Honeybee, Apis mellifera L. in Egypt. Journal of Plant Protection and Pathology, 11, pp. 25-28. https://doi.org/10.21608/jppp.2020.82425

Melathopoulos, A.P., Winston, M.L., Whittington, R., Smith, T., Lindberg, C. and Mukai, A., 2000. Comparative laboratory toxicity of neem pesticides to honey bees (Hymenoptera: Apidae), their mite parasites Varroa jacobsoni (Acari: Varroidae) and Acarapis woodi (Acari: Tarsonemidae), and brood pathogens Paenibacillus larvae and Ascosphaera apis, Journal of Economic Entomology, 93, pp. 199-209. https://doi.org/10.1603/0022-0493-93.2.199

Melo, G.A. and Gonçalves, R.B., 2005. Higher-level bee classifications (Hymenoptera, Apoidea, Apidae sensu lato). Revista Brasileria de Zoologia, 22, pp. 153-159. http://doi.org/10.1590/s0101-81752005000100017

Medina-Flores, C.A., Esquivel-Marín, N.H., López-Carlos, M., Medina-Cuellar, S.E. and Aguilera-Soto, J.I.. 2018. Estimación de la pérdida de colonias de abejas melíferas en el altiplano y el norte de México. Ecosistemas y Recursos Agropecuarios, 5, 365-371. https://doi.org/10.19136/era.a5n14.1459

Mohammed, A. and Razzaq, K., 2022. Evaluation of oils and extracts of some natural materials in the management of Varroa Jacobsoni Oudemans mites on Apis Mellifera honey bees in Basrah province. Natural Volatiles & Essential Oils, 9, pp. 561-574. https://www.nveo.org/index.php/journal/article/view/4550

Mortensen, A.N., Jack, C.J. and Ellis, J.D., 2018. The discovery of Varroa destructor on drone honey bees, Apis mellifera, at drone congregation areas. Parasitology Research, 117, pp. 3337-3339. http://doi.org/10.1007/s00436-018-6035-z

Mráz, P., Hýbl, M., Kopecký, M., Bohatá, A., Hošti?ková, I., Šipoš, J., Vo?adlová, K. and ?urn, V., 2021. Screening of honeybee pathogens in the Czech Republic and their prevalence in various habitats. Insects, 12, p. 1051. https://doi.org/10.3390/insects12121051

Mutinelli, F. and Baggio, S. 2004. Use of medical drugs against varroosis. Apiacta, 39, pp. 53-62.

Nadeem, M. and Riaz, A. 2012. Cumin (Cuminum cyminum) as a potential source of antioxidants. Pakistan Journal of Food Science, 22, pp. 101-107.

Neumann, H., Tedeschi, L., Zeller, W. and Huntley, N., 2017. The role of condensed tannins in ruminant animal production: Advances, limitations, and future directions. Revista Brasileria de Zootecnia, 46, pp. 929-949. http://doi.org/10.1590/s1806-92902017001200009

Negi, P., Rawat, B.S. and Negi, D.S., 2016. Antifeedant Constituents from Leucaena leucocephala. Journal of Applied Pharmaceutical Science, 6, 028-031. https://doi.org/10.7324/JAPS.2016.601204

Neumann, P. and Carreck, N.L., 2010. Honeybee colony losses. Journal of Apicultural Research, 49, pp. 1-6. http://doi.org/10.3896/IBRA.1.49.1.01

Ollerton, J., Winfree, R. and Tarrant, S., 2011. How many flowering plants are pollinated by animals? Oikos, 120, pp. 321-326. http://doi.org/10.1111/j.1600-0706.2010.18644.x

Olmstead, S., Menzies, C., McCallum, R., Glasgow, K. and Cutler, C., 2019. Apivar® and Bayvarol® suppress varroa mites in honeybee colonies in Canadian Maritime Provinces. Journal of the Acadian Entomology Society, 15, pp. 46-49. https://acadianes.org/journal/papers/olmstead_19-7.pdf

Omar, S., Macotte, M., Fields, P., Sanchez, P.E., Poveda, L., Mata, R., Jimenez, A., Durst, T., Zhang, J., Mockinnon, S., Leaman, D., Arnason, J.T. and Philogene, B.J.R., 2007. Antifeedant activities of terpenoids isolated from tropical Rutales. Journal of Stored Products Research, 43, pp. 92-96. http://doi.org/10.1016/j.jspr.2005.11.005

Owis, A.I., Abo-Youssef, A.M. and Osman, A.H., 2017. Leaves of Cordia boissieri A. DC. as a potential source of bioactive secondary metabolites for protection against metabolic syndrome-induced in rats. Zeitschrift Für Naturforschung. C, Journal of Biosciences, 72, pp. 107-118. https://doi.org/10.1515/znc-2016-0073

Pan, L., Ren, L., Chen, F., Feng, Y. and Luo, Y., 2016. Antifeedant Activity of Ginkgo biloba Secondary Metabolites against Hyphantria cunea Larvae: Mechanisms and Applications. PLoS ONE, 11(5), p. e0155682. http://doi.org/10.1371/journal.pone.0155682

Papezikova, I., Palikova, M., Kremserova, S., Zachova, A., Peterova, H., Babak, V. and Navratil, S., 2017. Effect of oxalic acid on the mite Varroa destructor and its host the honey bee Apis mellifera. Journal of Apiculture Research, 56, pp. 400-408. http://doi.org/10.1080/00218839.2017.1327937

Peck, D.T., Smith, M.L. and Seeley, T.D., 2016. Varroa destructor mites can nimbly climb from flowers onto foraging honeybees. PloS One, 11, p. e0167798. https://doi.org/10.1371/journal.pone.0167798

Peck, D.T., and Seeley, T.D., 2019. Mite bombs or robber lures? The roles of drifting and robbing in Varroa destructor transmission from collapsing honey bee colonies to their neighbors. PLoS One, 14, p. e0218392. http://doi.org/10.1371/journal.pone.0218392

Peters, R.S., Krogmann, L., Mayer, C., Donath, A., Gunkel, S., Meusemann, K., Kozlov, A., Podsiadlowski, L., Petersen, M., Lanfear, R., Diez, P. A., Heraty, J., Kjer, K.M., Klopfstein, S., Meier, R., Polidori, C., Schmitt, T., Liu, S., Zhou, X. and Niehuis, O. 2017. Evolutionary history of the Hymenoptera. Current Biology, 27, pp. 1013-1018. https://doi.org/10.1016/j.cub.2017.01.027

Pettis, J.S., 2004. A scientific note on Varroa destructor resistance to coumaphos in the United States. Apidologie, 35, pp. 91-92. http://doi.org/10.1051/apido:2003060

Piot, N., Schweiger, O., Meeus, I., Yañez, O., Straub, L., Villamar-Bouza, L., De la Rúa, P., Jara, L., Ruiz, C., Malmstrøm, M., Mustafa, S., Nielsen, A., Mänd, M., Karise, R., Tlak-Gajger, I., Özgör, E., Keskin, N., Diévart, V., Dalmon, A. and Miranda, J. R., 2022. Honeybees and climate explain viral prevalence in wild bee communities on a continental scale. Scientific Reports, 12, pp. 1904-1910. https://doi.org/10.1038/s41598-022-05603-2

Popovska-Stojanov, D., Dimitrov, L., Danihlík, J., Uzunov, A., Golubovski, M., Andonov, S. and Brodschneider, R. 2021. Direct economic impact assessment of winter honeybee colony losses in three European countries. Agriculture, 11, p. 398. https://doi.org/10.3390/agriculture11050398

Qadir, Z.A., Idrees, A., Mahmood, R., Sarwar, G., Bakar, M.A., Ahmad, S., Raza, M.M. and Li, J., 2021. Effectiveness of different soft acaricides against honeybee ectoparasitic mite Varroa destructor (Acari: Varroidae). Insects, 12, pp. 1032-1043. https://doi.org/10.3390/insects12111032

Quintana-Obregón, A., Sánchez-Mariñez, R., Cortes-Rocha, M. and González-Aguilar, M., 2017. Actividad antifúngica in vitro de mezcla de terpenos de naranja contra Alternaria tenuissima. Scientia Fongorum, 45, pp. 7-12. https://www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S0187-31802017000100007

Rademacher, E. and Harz, M. 2006. Oxalic acid for the control of varroosis in honeybee colonies-a review. Apidologie, 37, pp. 98-120. https://doi.org/10.1051/apido:2005063

Ramírez, R.G. and Lara, J.A., 1998. Influence of native shrubs Acacia rigidula, Cercidium macrum and Acacia farnesiana on digestibility and nitrogen utilization by sheep. Small Ruminant Research, 28, pp. 39-45. http://doi.org/10.1016/s0921-4488(97)00066-7

Ramos-López, M.A., González-Chávez, M.M., Cárdenas-Ortega, N.C., Zavala-Sánchez, M.A. and Pérez, G.S., 2012. Activity of the main fatty acid components of the hexane leaf extract of Ricinus communis against Spodoptera frugiperda. The African Journal of Biotechnology, 11, pp. 4274-4278. http://doi.org/10.5897/AJB11.3727

Ramsey, S.D., Ochoa, R., Bauchan, G., Gulbronson, C., Mowery, J.D., Cohen, A., Lim, D., Joklik, J., Cicero, J.M. and Ellis, J.D., 2019. Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proceedings of the National Academy of Sciences, 116, pp. 1792-1801. http://doi.org/10.1073/pnas.1818371116

Ramzi, H., Ismaili, M.R., Aberchane, M. and Zaanoun, S., 2017. Chemical characterization and acaricidal activity of Thymus satureioides C. & B. and Origanum elongatum E. & M. (Lamiaceae) essential oils against Varroa destructor Anderson & Trueman (Acari: Varroidae). Industrial Crops and Products, 108, pp. 201-207. https://doi.org/10.1016/j.indcrop.2017.06.031

Rasool, K., Ahad, I. and Rasool, R., 2017. Efficacy of various botanicals and chemicals on ectoparasitic mite, Varroa destructor feeding on European honeybee, Apis mellifera. Journal of Entomology and Zoology Studies, 5, pp. 589-595. https://www.entomoljournal.com/archives/2017/vol5issue5/PartH/5-4-291-787.pdf

Razavi, S.M., Asadpour, M., Jafari, A. and Malekpour, S.H., 2015. The field efficacy of Lepidium latifolium and Zataria multiflora methanolic extracts against Varroa destructor. Parasitology Research, 114, pp. 4233-4238. https://doi.org/10.1007/s00436-015-4661-2

Reams, T. and Rangel, J., 2022. Understanding the Enemy: A Review of the Genetics, Behavior and Chemical Ecology of Varroa destructor, the Parasitic Mite of Apis mellifera. Journal of Insect Science, 22, pp. 1-10 https://doi.org/10.1093/jisesa/ieab101

Reher, T., Van Kerckvoorde, V., Verheyden, L., Wenseleers, T., Beliën, T., Bylemans, D. and Martens, J.A., 2019. Evaluation of hop (Humulus lupulus) as a repellent for the management of Drosophila suzukii. Crop Protection, 124, p. 104839. http://doi.org/10.1016/j.cropro.2019.05.033

Rehm, S. and Ritter, W., 1989. Sequence of the sexes in the offspring of Varroa jacobsoni and the resulting consequences for the calculation of the developmental period. Apidologie, 20, pp. 339-343. http://doi.org/10.1051/apido:19890406

Reyes-Quintana, M., Espinosa-Montaño L.G., Prieto-Merlos, D., Koleoglu, G., Petukhova, T., Correa-Benítez, A. and Guzman-Novoa, E., 2019. Impact of Varroa destructor and deformed wing virus on emergence, cellular immunity, wing integrity and survivorship of Africanized honeybees in Mexico. Journal of Invertebrate Pathology, 164, pp. 43-48 http://doi.org/10.1016/j.jip.2019.04.009

Reyna-Fuentes, J. H., Martínez González, J. C., Silva Contreras, M., y López Aguirre, D. 2022. Efecto de tres moliendas vegetales contra el ácaro Varroa destructor en colonias de Apis mellifera. Nova Scientia, 14, 1-10. http://doi.org/10.21640/ns.v14i28.3019

Ribani, A., Utzeri, V.J., Taurisano, V. and Fontanesi, L., 2020. Honey as a source of environmental DNA for the detection and monitoring of honey bee pathogens and parasites. Veterinary Sciences, 7, pp. 113-120. https://doi.org/10.3390/vetsci7030113

Rinkevich, F.D., 2020 Detection of amitraz resistance and reduced treatment efficacy in the Varroa mite, Varroa destructor, within commercial beekeeping operations. PLoS One, 15, p. e0227264. http://doi.org/10.1371/journal.pone.0227264

Romo-Chacón, A., Martínez-Contreras, L. Molina-Corral, J., Acosta-Muñiz, F. J., Ríos-Velasco, C. H., León-Door, C. and Rivera, R., 2016. Evaluation of Oregano (Lippia berlandieri) Essential Oil and Entomopathogenic Fungi for Varroa destructor Control in Colonies of Honeybee, Apis mellifera. The Southwestern Entomologist, 41, pp. 971-982. https://doi.org/10.3958/059.041.0427

Rosenkranz, K. and Rothwell, J.C., 2004. The effect of sensory input and attention on the sensorimotor organization of the hand area of the human motor cortex: Muscle vibration and sensorimotor organization. The Journal of Physiology, 561, 307-320. https://doi.org/10.1113/jphysiol.2004.069328

Rosenkranz, P., Aumeier, P. and Ziegelmann, B., 2010. Biology and control of Varroa destructor. Journal of Invertebrate Pathology, 103, pp. 96-119. https://doi.org/10.1016/j.jip.2009.07.016

Roth, M.A., Wilson, J.M., Taylor, K.R., and Gross, A.D., 2020. Biology and management of Varroa destructor (Mesostigmata: Varroidae) in Apis mellifera (Hymenoptera: Apidae) colonies. Journal of Integrate Pest Management, 11, pp. 1-8. https://doi.org/10.1093/jipm/pmz036

Ruffinengo, S.R., Maggi, M., Marcangeli, J., Eguaras, M., Principal, J., Barrios, C., De Piano, F. and Mitton, G., 2014. Integrated Pest Management to control Varroa destructor and its implications to Apis mellifera colonies. Zootecnia Tropical, 32(2), pp. 149-168. https://ve.scielo.org/scielo.php?script=sci_arttext&pid=S0798-72692014000200006

Ruffinengo, S., Eguaras, M., Floris, I., Faverin, C., Bailac, P. and Ponzi, M. 2005. LD50 and repellent effects of essential oils from Argentinian wild plant species on Varroa destructor. Journal of Economic Entomology, 98(3), pp. 651-655. https://doi.org/10.1603/0022-0493-98.3.651

Ruffinengo, S., Maggi, M. and Fuselli, S., 2006. Laboratory evaluation of Heterothalamus alienus essential oil against different pests of Apis mellifera. Journal of Essential Oils Research, 18, pp. 704-707. http://doi.org/10.1080/10412905.2006.9699211

Ruffinengo, S., Maggi, M., Faverin, C., De la Rosa, S.G.B., Bailac, P. and Principal, J., 2007. Essential oils toxicity related to Varroa destructor and Apis mellifera under laboratory conditions. Zootecnia Tropical, 25, pp. 63-69. https://ve.scielo.org/scielo.php?pid=S0798-72692007000100009&script=sci_abstract&tlng=en

Sabahi, Q., Gashout, H., Kelly, P. G. and Guzman-Novoa, E., 2017. Continuous release of oregano oil effectively and safely controls Varroa destructor infestations in honey bee colonies in a northern climate. Experimental and Applied Acarology, 72, pp. 263-275. https://doi.org/10.1007/s10493-017-0157-3

Sabahi, Q., Morfin, N., Emsen, B., Gashout, H. A., Kelly, P.G., Otto, S., Merrill, A.R. and Guzman-Novoa, E., 2020. Evaluation of dry and wet formulations of oxalic acid, thymol, and oregano oil for Varroa mite (Acari: Varroidae) control in honeybee (Hymenoptera: Apidae) colonies. Journal of Economic Entomology, 113, pp. 2588-2594. https://doi.org/10.1093/jee/toaa218

Sammataro, D., Untalan, P., Guerrero, F. and Finley, J., 2005. The resistance of varroa mites (Acari: Varroidae) to acaricides and the presence of esterase. International Journal of Acarology, 31(1), pp. 67-74. https://doi.org/10.1080/01647950508684419

Schittny, D., Yañez, O. and Neumann, P., 2020. Honeybee virus transmission via hive products. Veterinary Sciences, 7, pp. 96-103. https://doi.org/10.3390/vetsci7030096

Serra, V., Salvatori, G. and Pastorelli, G., 2021. Dietary Polyphenol Supplementation in Food Producing Animals: Effects on the Quality of Derived Products. Animals, 11, 1-44. http://doi.org/10.3390/ani11020401

Smith, J., Cleare, X.L., Given, K. and Li-Byarlay, H., 2021. Morphological changes in the mandibles accompany the defensive behavior of Indiana mite biting honeybees against Varroa destructor. Frontiers in Ecology and Evolution, 9, p. 638308. http://doi.org/10.3389/fevo.2021.638308

Smoli?ski, S., Langowska, A. and Glazaczow, A., 2021. Raised seasonal temperatures reinforce autumn Varroa destructor infestation in honey bee colonies. Scientific Reports, 11, pp. 124-141. https://doi.org/10.1038/s41598-021-01369-1

Soto-Muciño, L., Elizarraras-Baena, R. y Soto-Muciño, I., 2017. Situación apícola en México y perspectiva de la producción de miel en el Estado de Veracruz. Revista de Estrategias del Desarrollo Empresarial, 3, pp. 40-64.

Stanimirovi?, Z., Glavini?, U., Laki?, N., Radovi?, D., Ristani?, M., Tari?, E. and Stevanovi?, J., 2017. Efficacy of plant-derived formulation “Argus Ras” in Varroa destructor control. Acta Veterinaria, 67, pp. 191-200. https://doi.org/10.1515/acve-2017-0017

Steinhauer, N., vanEngelsdorp, D. and Saegerman, C., 2021. ‘Prioritizing changes in management practices associated with reduced winter honeybee colony losses for US beekeepers,’ Science of The Total Environment, 753, p. 141629. http://doi.org/10.1016/j.scitotenv.2020.141629

Tanabe, N., Kuboyama, T., Kazuma, K., Konno, K. and Tohda, C., 2015. The extract of roots of Sophora flavescens enhances the recovery of motor function by axonal growth in mice with a spinal cord injury. Frontiers in Pharmacology, 6, pp. 326-340. https://doi.org/10.3389/fphar.2015.00326

Toomemaa, K., 2018. The synergistic effect of weak oxalic acid and thymol aqueous solutions on Varroa mites and honeybees. Journal of Apicultural Research, 58, pp. 37-52. https://doi.org/10.1080/00218839.2018.1486695

Torres-Fajardo, R.A. and Higuera-Piedrahita, R.I., 2021. Actividad antihelmíntica in vivo de terpenos y aceites esenciales en pequeños rumiantes. Revista MVZ Cordoba, 26, e2317. https://doi.org/10.21897/rmvz.2317

Traynor, K.S., Mondet, F., de Miranda, J.R., Techer, M., Kowallik, V., Oddie, M.A. Y., Chantawannakul, P. and McAfee, A., 2020. Varroa destructor: A complex parasite, crippling honeybees worldwide. Trends in Parasitology, 36, pp. 592-606. https://doi.org/10.1016/j.pt.2020.04.004

Vilarem, C., Piou, V., Vogelweith, F. and Vétillard, A., 2021. Varroa destructor from the laboratory to the field: Control, biocontrol and IPM perspectives-A review. Insects, 12, pp. 800-815. https://doi.org/10.3390/insects12090800

Viveros-Valdez, E., Jaramillo-Mora, C., Oranday-Cardenas, A., Mordn-Martinez, J. and Carranza-Rosales, P., 2016. Antioxidant, cytotoxic and alpha-glucosidase inhibition activities from the Mexican berry "Anacahuita" (Cordia boissieri). Archivos Latinoamericanos de Nutrición, 66, pp. 211-218. https://www.alanrevista.org/ediciones/2016/3/art-7/

Wang, R., Liu, Z., Dong, K., Elzen, P. J., Pettis, J. and Huang, Z.Y., 2002. Association of novel mutations in a sodium channel gene with fluvalinate resistance in the mite, Varroa destructor. Journal of Apiculture Research, 40, pp. 17-25. http://doi.org/10.1080/00218839.2002.11101064

Wang, X., Zhang, Y., Wu, N., Cao, J., Tao, Y. and Yu, R., 2021. A method to separate two main antioxidants from Lepidium latifolium L. extracts using online medium pressure chromatography tower and two-dimensional inversion/hydrophobic interaction chromatography based on online HPLC-DPPH assay. Separations, 8, p. 238. https://doi.org/10.3390/separations8120238

Wegener, J., Ruhnke, H., Scheller, K., Mispagel, S., Knollmann, U., Kamp, G. and Bienefeld, K., 2016. Pathogenesis of varroosis at the level of the honeybee (Apis mellifera) colony. Journal of Insect Physiology, 91, pp. 1-9. http://doi.org/j.jisphys.2016.06004

Wei, J., Ding, W., Zhao, Y.G. and Vanichpakorn, P. 2011 Acaricidal activity of Aloe vera L. leaf extracts against Tetranychus cinnabarinus (Boisduval) (Acarina: Tetranychidae). Journal of Asia-Pacific Entomology, 14, pp. 353-356. http://doi.org/j.aspen.2011.04.006

Xavier, V.M., Message, D., Picanço, M.C., Chediak, M., Júnior, P.A.S., Ramos, R.S. and Martins, J.C., 2015. Acute toxicity and sublethal effects of botanical insecticides to honey bees. Journal of Insect Science, 15, p. 137. https://doi.org/10.1093/jisesa/iev110

Xie, X., Huang, Z.Y. and Zeng, Z., 2016. Why do Varroa mites prefer nurse bees? Scientific Reports, 6, pp. 1-6. https://doi.org/10.1038/srep28228

Yousef, H., El-Lakwah, S.F. and El Sayed, Y.A., 2013. Insecticidal activity of linoleic acid against Spodoptera littoralis (boisd.). Egyptian Journal of Agricultural Research, 91(2), pp. 573-580. https://doi.org/10.21608/ejar.2013.163516

Zanni, V., De?irmenci, L., Annoscia, D., Scheiner, R. and Nazzi, F., 2018. The reduced brood nursing by mite-infested honeybees depends on their accelerated behavioral maturation. Journal of Insect Physiology, 109, pp. 47-54. https://doi.org/10.1016/j.jinsphys.2018.06.006

Zapata-Campos, C.C. and Mellado-Bosque, M.A., 2021. La cabra: selección y hábitos de consumo de plantas nativas en agostadero árido. CienciaUAT, 15, pp. 169-185. https://doi.org/10.29059/cienciauat.v15i2.1409

Zapata-Campos, C.C., García-Martínez, J.E., Chavira, J.S., Valdés, J.A., Morales, M.A. and Mellado, M., 2020. Chemical composition and nutritional value of leaves and pods of Leucaena leucocephala, Prosopis laevigata and Acacia farnesiana in a xerophilous shrubland. Emirates Journal of Food and Agriculture, 32, pp. 723-730. http://doi.org/10.9755/ejfa.2020.v32.i10.2148

Zárate-Martínez, W., González-Morales, S., Ramírez-Godina, F., Robledo-Olivo, A. and Juárez-Maldonado, A. 2021. Efecto de los ácidos fenólicos en el sistema antioxidante de plantas de tomate (Solanum lycopersicum Mill.). Agronomia Mesoamericana: Organo Divulgativo Del PCCMCA, Programa Cooperativo Centroamericano de Mejoramiento de Cultivos y Animales, 854-868. https://doi.org/10.15517/am.v32i3.45101

Zayed, M.Z. and Samling, B., 2016. Phytochemical constituents of the leaves of Leucaena leucocephala from Malaysia. International Journal of Pharmacy and Pharmaceutical Sciences, 8 pp. 174-179 https://doi.org/10.22159/ijpps.2016v8i12.11582

Zhang, Y., Zhang, Q., Luo, J. and Ding, W., 2017. Acaricidal active fractions from acetone extract of Aloe vera L. against Tetranychus cinnabarinus and Panonychus citri. Acta Physiologiae Plantarum, 39, pp. 1-7 https://doi.org/10.1007/s11738-017-2496-4

Zhou, F. and Pichersky, E., 2020. The complete functional characterisation of the terpene synthase family in tomato. The New Phytologist, 226, pp. 1341-1360. https://doi.org/10.1111/nph.16431

Ziegler, J. and Facchini, P.J., 2008. Alkaloid biosynthesis: Metabolism and trafficking. Annual Review of Plant Biology, 59, pp. 735-769. https://doi.org/10.1146/annurev.arplant.59.032607.092730




URN: http://www.revista.ccba.uady.mx/urn:ISSN:1870-0462-tsaes.v27i1.45271

DOI: http://dx.doi.org/10.56369/tsaes.4527

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Copyright (c) 2023 Jesús Humberto Reyna Fuentes, Cecilia Carmela Zapata Campos, José Octavio Merino Charrez, Daniel López Aguirre, Juan Alberto Ascasio Valdéz

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