Insecticide Susceptibility and Detoxifying Enzyme Activity in Managed Honey Bees in a Southern Mexico Landscape
References
- Araújo, M. F., Castanheira, E. M., Sousa, S. F. (2023). The buzz on insecticides: A review of uses, molecular structures, targets, adverse effects, and alternatives. Molecules, 28(8), 3641. https://doi.org/10.3390/molecules28083641
- Berenbaum, M. R., & Johnson, R. M. (2015). Xenobiotic detoxification pathways in honey bees. Current Opinion in Insect Science, 10, 51-58. https://doi.org/10.1016/j.cois.2015.03.005
- Blacquiere, T., Smagghe, G., Van Gestel, C. A., Mommaerts, V. (2012). Neonicotinoids in bees: A review on concentrations, side-effects and risk assessment. Ecotoxicology, 21, 973-992. https://doi.org/10.1007/s10646-012-0863-x
- Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2), 248-254. https://doi.org/10.1016/0003-2697(76)90527-3
- Calatayud-Vernich, P., Calatayud, F., Simó, E., Picó, Y. (2018). Pesticide residues in honey bees, pollen and beeswax: Assessing beehive exposure. Environmental Pollution, 241, 106-114. https://doi.org/10.1016/j.envpol.2018.05.062
- Carvalho, S. M., Belzunces, L. P., Carvalho, G. A., Brunet, J., Badiou-Beneteau, A. (2013). Enzymatic biomarkers as tools to assess environmental quality: A case study of exposure of the honeybee Apis mellifera to insecticides. Environmental Toxicology and Chemistry, 32(9), 2117-2124. https://doi.org/10.1002/etc.2288
- Chakrabarti, P. (2019). Multifactorial declines in global insect pollinator populations - Case studies in honey bees. Environmental Issues: Approaches and Practices, 1, 20-31.
- Chauzat, M., & Faucon, J. (2007). Pesticide residues in beeswax samples collected from honey bee colonies (Apis mellifera L.) in France. Pest Management Science: Formerly Pesticide Science, 63(11), 1100-1106. https://doi.org/10.1002/ps.1451
- Christen, V., & Fent, K. (2017). Exposure of honey bees (Apis mellifera) to different classes of insecticides exhibit distinct molecular effect patterns at concentrations that mimic environmental contamination. Environmental Pollution, 226, 48-59. https://doi.org/10.1016/j.envpol.2017.04.003
- Córdova-Córdova, C. I., Ramírez-Arriaga, E., Martínez-Hernández, E., Zaldívar-Cruz, J. M. (2013). Caracterización botánica de miel de abeja (Apis mellifera L.) de Cuatro Regiones Del Estado de Tabasco, México, Mediante Técnicas Melisopalinológicas. Universidad y Ciencia, 29(2), 163-178.
- Cuadriello-Aguilar, J. I., Hernández, M., Ramírez Arriaga, E., Sosa Nájera, M. S., Sánchez, M., Eva, J., Medina Camacho, M. D., Lozano García, M. del S. (1993). Atlas de las plantas y el polen utilizados por las cinco especies principales de abejas productoras de miel en la región del Tacaná, Chiapas, México.
- Danner, N., Keller, A., Härtel, S., Steffan-Dewenter, I. (2017). Honey bee foraging ecology: Season but not landscape diversity shapes the amount and diversity of collected pollen. PLoS One, 12(8), e0183716. https://doi.org/10.1371/journal.pone.0183716
- Desneux, N., Decourtye, A., Delpuech, J. M. (2007). The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52(1), 81-106. https://doi.org/10.1146/annurev.ento.52.110405.091440
- Di Pasquale, G., Alaux, C., Le Conte, Y., Odoux, J. F., Pioz, M., Vaissière, B. E., Belzunces, L. P., Decourtye, A. (2016). Variations in the availability of pollen resources affect honey bee health. PLoS One, 11(9), e0162818. https://doi.org/10.1371/journal.pone.0162818
- Di Pasquale, G., Salignon, M., Le Conte, Y., Belzunces, L. P., Decourtye, A., Kretzschmar, A., S... Alaux, C. (2013). Influence of pollen nutrition on honey bee health: Do pollen quality and diversity matter? PLoS One, 8(8), e72016. https://doi.org/10.1371/journal.pone.0072016
- Donkersley, P., Rhodes, G., Pickup, R. W., Jones, K. C., Power, E. F., Wright, G. A., Wilson, K. (2017). Nutritional composition of honey bee food stores vary with floral composition. Oecologia, 185, 749-761. https://doi.org/10.1007/s00442-017-3968-3
- Erdtman, G. (1960). The Acetolysis Method-a Revised Description. Svensk Botanisk Tidskrift, 54, 516-564.
- 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
- González, I., & Déjean, S. (2021). CCA: Canonical correlation analysis. R package version 1.2. 1.
- James, R. R., & Pitts-Singer, T. L. (2008). Bee pollination in agricultural ecosystems. Oxford University Press.
- Jensen, I. M., & Whatling, P. (2010). Malathion: A review of toxicology. Hayes’ Handbook of Pesticide Toxicology, 1527-1542. https://doi.org/10.1016/B978-0-12-374367-1.00071-9
- Lara-Pulido, J. A., Guevara-Sanginés, A., Torres-Rojo, J. M., Núñez-Hernández, J. M., Riojas, J., Pérez-Cirera, V., ... Jiménez-Quiroga, C. (2021). Honey-guacamole: Assessment of pollination environmental service in avocado production in Michoacan, Mexico. Acta Universitaria, 31, e3083. https://doi.org/10.15174/au.2021.3083
- Li, X., Schuler, M. A., Berenbaum, M. R. (2007). Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology, 52(1), 231-253. https://doi.org/10.1146/annurev.ento.51.110104.151104
- Li, X. M., Wang, Y., Lei, L., Zhang, G., Xu, B. H. (2025). Effects of three different bee pollen on digestion, immunity, antioxidant capacity, and gut microbes in Apis mellifera. Insects, 16(5), 505. https://doi.org/10.3390/insects16050505
- López-Roblero, E., Espinoza-Toledo, C., López García, J. A., Grajales-Conesa, J., Quiroz-García, D. (2021). Floral resources collected by four native bees species in Southern Mexico. Grana, 60(1), 57-68. https://doi.org/10.1080/00173134.2020.1767195
- Malagnini, V., Cappellari, A., Marini, L., Zanotelli, L., Zorer, R., Angeli, G., Ioriatti, C., Fontana, P. (2022). Seasonality and landscape composition drive the diversity of pollen collected by managed honey bees. Frontiers in Sustainable Food Systems, 6, 865368. https://doi.org/10.3389/fsufs.2022.865368
- Menzel, U. (2012). CCP: Significance tests for canonical correlation analysis (CCA). R Package Version. 1(1)
- Noi, A. D., Casini, S., Campani, T., Cai, G., Caliani, I. (2021). Review on sublethal effects of environmental contaminants in honey bees (Apis mellifera), knowledge gaps and future perspectives. International Journal of Environmental Research and Public Health, 18(4), 1-19. https://doi.org/10.3390/ijerph18041863
- Padilha, A., Piovesan, B., Morais, M., de B. Pazini, J., Zotti, M., Botton, M., Grützmacher, A. (2020). Toxicity of insecticides on neotropical stingless bees Plebeia emerina (Friese) and Tetragonisca fiebrigi (Schwarz) (Hymenoptera: Apidae: Meliponini). Ecotoxicology, 29, 119-128. https://doi.org/10.1007/s10646-019-02150-x
- Palacios-Chávez, R., & Ludlow-Wiechers, B. (1991). Flora Palinológica de La Reserva de La Biosfera de Sian Ka’an, Quintana Roo, México. Centro de Investigaciones de Quintana Roo.
- Penilla, P. R., Rodriguez, A. D., Hemingway, J., Torres, J. L., Arredondo-Jiménez, J. I., Rodriguez, M. H. (1998). Resistance management strategies in malaria vector mosquito control. Baseline data for a large-scale field trial against Anopheles albimanus in Mexico. Medical and Veterinary Entomology, 12(3), 217-233. https://doi.org/10.1046/j.1365-2915.1998.00123.x
- Pérez-Barraza, M . H., Avitia-García, E., Cano-Medrano, R., Gutiérrez-Espinosa, M. A., Osuna-Enciso, T., Pérez-Luna, A. I. (2018). Temperatura e inhibidores de giberelinas En El Proceso de Floración Del Mango ‘Ataulfo’. Revista Fitotecnia Mexicana, 41(4A), 543-549.
- Pervez, M., & Manzoor, F. (2023). Honey Bee Losses and Pesticides Threat: An Asian Perspective. Journal of Apicultural Research, 62(1), 64-75. https://doi.org/10.1080/00218839.2022.2103331
- R Core Team. (2020). A language and environment for statistical computing. R Foundation for Statistical Computing.
- Ramírez-Arriaga, E., Navarro-Calvo, L. A., Díaz-Carbajal, E. (2011). Botanical characterisation of Mexican honeys from a subtropical region (Oaxaca) based on pollen analysis. Grana, 50(1), 40-54.
- Ranganathan, M., Narayanan, M., Kumarasamy, S. (2022). Importance of metabolic enzymes and their role in insecticide resistance. In new and future development in biopesticide research: Biotechnological exploration (pp. 243-260). Springer Nature.
- Requier, F., Odoux, J.-F., Tamic, T., Moreau, N., Henry, M., Decourtye, A., Bretagnolle, V. (2015). Honey bee diet in intensive farmland habitats reveals an unexpectedly high flower richness and a major role of weeds. Ecological Applications, 25(4), 881-890. https://doi.org/10.1890/14-1011.1
- Reyes-Moreno, J. (2017). Floración y fructificación en rambután (Nephelium lappaceum L). Masther's thesis.
- Roubik, D. W., & Moreno, J. E. (1992). Pollen and spores of Barro Colorado Island. Kew Bulletin, 47(4), 791. https://doi.org/10.2307/4110734
- Ruiz-Toledo, J., & Sánchez, D. (2024). Glyphosate Contamination: Implications for honeybee Apis mellifera and consumers in Southeastern Mexico. Agro Productividad. https://doi.org/10.32854/agrop.v17i6.2748
- Ruiz-Toledo, J., Vandame, R., Castro-Chan, R. A., Penilla-Navarro, R. P., Gómez, J., Sánchez, D. (2018). Organochlorine pesticides in honey and pollen samples from managed colonies of the honey bee Apis mellifera Linnaeus and the stingless bee Scaptotrigona mexicana Guérin from southern, Mexico. Insects, 9(2), 54. https://doi.org/10.3390/insects9020054
- Sabo, R., Staroň, M., Sabová, L., Majchrák, T., Bischoff, G., Pistorius, J., ... Alkassab, A. T. (2024). Honey bees for pesticide monitoring in the landscape: Which bee matrices should be used? Chemosphere, 364, 143130. https://doi.org/10.1016/j.chemosphere.2024.143130
- Sanchez-Bayo, F., & Goka, K. (2014). Pesticide residues and bees - a risk assessment. PLoS One, 9(4), e94482. https://doi.org/10.1371/journal.pone.0094482
- Serrão, J. E., Plata-Rueda, A., Martínez, L. C., Zanuncio, J. C. (2022). Side-effects of pesticides on non-target insects in agriculture: A mini-review. The Science of Nature, 109(2), 17. https://doi.org/10.1007/s00114-022-01788-8
- Simon-Delso, N., San Martin, G., Bruneau, E., Hautier, L. (2018). Time-to-death approach to reveal chronic and cumulative toxicity of a fungicide for honeybees not revealed with the standard tenday test. Scientific Reports, 8(1), 7241. https://doi.org/10.1038/s41598-018-24746-9
- Soderlund, D. M. (2010). Toxicology and Mode of Action of Pyrethroid Insecticides. In Hayes’ Handbook of Pesticide Toxicology (pp. 1665–1686). Elsevier/AP.
- Solís-Santoyo, F., Rodríguez, A. D., Black, W., Saavedra-Rodríguez, K., Sánchez-Guillén, D., Castillo-Vera, A., ... Penilla-Navarro, R. P. (2022). Current enzyme-mediated insecticide resistance status of Aedes aegypti populations from a dengue-endemic city in Southern Mexico. Salud Pública de México, 65(1), 19-27. https://doi.org/10.21149/13910
- Sponsler, D. B., & Johnson, R. M. (2017). Mechanistic modeling of pesticide exposure: The missing keystone of honey bee toxicology. Environmental Toxicology and Chemistry, 36(4), 871-881. https://doi.org/10.1002/etc.3661
- Tamburini, G., Bommarco, R., Kleijn, D., van der Putten, W. H., Marini, L. (2019). Pollination contribution to crop yield is often context-dependent: A review of experimental evidence. Agriculture, Ecosystems & Environment, 280, 16-23. https://doi.org/10.1016/j.agee.2019.04.022
- Thany, S. H. (2023). Molecular mechanism of action of neonicotinoid insecticides. International Journal of Molecular Sciences, 24(6), 5484. https://doi.org/10.3390/ijms24065484
- Therneau, T. (2023). A Package for Survival Analysis in R.
- Valdovinos-Flores, C., Alcantar-Rosales, V. M., Gaspar-Ramírez, O., Saldaña-Loza, L. M., Dorantes-Ugalde, J. A. (2017). Agricultural pesticide residues in honey and wax combs from southeastern, central and northeastern Mexico. Journal of Apicultural Research, 56(5), 667-679. https://doi.org/10.1080/00218839.2017.1340798
- Villa, S., Vighi, M., Finizio, A., Bolchi-Serini, G. (2000). Risk assessment for honeybees from pesticide-exposed pollen. Ecotoxicology, 9, 287-297. https://doi.org/10.1023/A:1026522112328
- Winston, M. L. (1991). The Biology of the Honey Bee. Harvard University Press.
- Zhao, H., Li, G., Cui, X., Wang, H., Liu, Z., Yang, Y., Xu, B. (2022). Review on effects of some insecticides on honey bee health. Pesticide Biochemistry and Physiology, 188, 105219. https://doi.org/10.1016/j.pestbp.2022.105219
Language: English
Page range: 51 - 68
Submitted on: Jul 14, 2025
Accepted on: Mar 27, 2026
Published on: Jul 1, 2026
In partnership with: Paradigm Publishing Services
Keywords:
Related subjects:
© 2026 Augusto Campollo-Ovalle, Jovani Ruiz-Toledo, Julio Rojas, Juan F. Barrera, Daniel Sánchez, published by The National Institute of Horticultural Research and Apicultural Research Association
This work is licensed under the Creative Commons Attribution 4.0 License.