{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,23]],"date-time":"2026-08-23T17:13:41Z","timestamp":1787505221778,"version":"build-2736575974"},"reference-count":59,"publisher":"MDPI AG","issue":"13","license":[{"start":{"date-parts":[[2022,7,5]],"date-time":"2022-07-05T00:00:00Z","timestamp":1656979200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Consejo Nacional de Ciencia y Tecnolog\u00eda (Conacyt)","award":["# 629727"],"award-info":[{"award-number":["# 629727"]}]},{"name":"Universidad de Guadalajara","award":["# 629727"],"award-info":[{"award-number":["# 629727"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>This is a preliminary study conducted to analyze the presence and concentration of pesticides in honey obtained from honey bee colonies located in two regions with managed ecosystems that differ in the intensity and technification of agricultural practices. Fourteen pesticides at variable concentrations were detected in 63% of the samples analyzed. The pesticides most frequently found at higher concentrations were insecticides (neonicotinoids, followed by organophosphates), herbicides, and fungicides. The number, frequency, and concentration of pesticides were higher in samples collected from hives located where intensive and highly-technified agriculture is practiced. Forty-three percent of the samples from that zone had residues of imidacloprid, compared with only 13% of the samples from the less-technified zone. Furthermore, 87.5% of those samples had imidacloprid concentrations that were above sublethal doses for honey bees (&gt;0.25 ng\/g) but that are not considered hazardous to human health by the European Commission. The results of this study suggest that honey can be used as a bioindicator of environmental contamination by pesticides, which highlights the need to continue monitoring contaminants in this product to determine the risks of pesticide impacts on pollinator health, on ecosystems, and on their potential implications to human health and other non-target organisms.<\/jats:p>","DOI":"10.3390\/ijerph19138199","type":"journal-article","created":{"date-parts":[[2022,7,5]],"date-time":"2022-07-05T10:21:33Z","timestamp":1657016493000},"page":"8199","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":34,"title":["Detection and Concentration of Neonicotinoids and Other Pesticides in Honey from Honey Bee Colonies Located in Regions That Differ in Agricultural Practices: Implications for Human and Bee Health"],"prefix":"10.3390","volume":"19","author":[{"given":"Gilda","family":"Ponce-Vejar","sequence":"first","affiliation":[{"name":"Departamento de Ciencias Ambientales, Centro Universitario de Ciencias Biol\u00f3gicas y Agropecuarias, Universidad de Guadalajara, Guadalajara 44600, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3080-8209","authenticated-orcid":false,"given":"S. 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Desaf\u00edos Globales, Poblaci\u00f3n. Available online: https:\/\/www.un.org\/es\/sections\/issues-depth\/population\/index.html."},{"key":"ref_2","unstructured":"World Health Organization (WHO) (2021, February 03). Connecting Global Priorities: Biodiversity and Human Health: A State of Knowledge Review. Available online: http:\/\/apps.who.int\/iris\/bitstream\/handle\/10665\/174012\/9789241508537_eng.pdf;jsessionid=9246190A9D78ACDAAF4C35ECBA1E5760?sequence=1."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"307","DOI":"10.19136\/era.a6n17.1972","article-title":"An\u00e1lisis clim\u00e1tico para la agricultura de temporal en Michoac\u00e1n, M\u00e9xico","volume":"6","author":"Bautista","year":"2019","journal-title":"Ecosistem. Rec. Agropec."},{"key":"ref_4","unstructured":"Jensen, M.H., and Malter, A.J. (1995). Protected Agriculture: A Global Review. World Bank Publications."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Rathore, H., and Nollet, L. (2012). Uses and environmental pollution of biocides. Pesticides: Evaluation of Environmental Pollution, Taylor and Francis.","DOI":"10.1201\/b11864"},{"key":"ref_6","unstructured":"Frumkin, H. (2010). Pest control and pesticides. Environmental Health from Global to Local, Jossey-Bass."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"2883","DOI":"10.1021\/jf103856c","article-title":"Neonicotinoids insecticides: Highlights of a symposium on strategic molecular designs","volume":"59","author":"Tomizawa","year":"2011","journal-title":"J. Agric. Food Chem."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1007\/s11356-014-3470-y","article-title":"Systemic insecticides (neonicotinoids and fipronil): Trends, uses, mode of action and metabolites","volume":"22","author":"Belzunces","year":"2015","journal-title":"Environ. Sci. Poll. Res."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Ichikawa, G., Kuribayashi, R., Ikenaka, Y., Ichise, T., Nakayama, S.M., Ishizuka, M., Taira, K., Fujioka, K., Sairecnchi, T., and Kobashi, G. (2019). LC-ESI\/MS\/MS analysis of neonicotinoids in urine of very low birth weight infants at birth. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0219208"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"11709","DOI":"10.1007\/s11356-021-12853-6","article-title":"An update of the worldwide integrated assessment (WIA) on systemic insecticides","volume":"28","author":"Bonmatin","year":"2021","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"11749","DOI":"10.1007\/s11356-017-0341-3","article-title":"An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 2: Impacts on organisms and ecosystems","volume":"28","author":"Pisa","year":"2017","journal-title":"Environ. Sci. Poll. Res."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.chemosphere.2017.10.149","article-title":"Human exposure to neonicotinoid insecticides and the evaluation of their potential toxicity: An overview","volume":"192","author":"Han","year":"2018","journal-title":"Chemosphere"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1016\/j.ecoenv.2004.10.005","article-title":"Assessing the genotoxicity of imidacloprid and RH-5849 in human peripheral blood lymphocytes in vitro with comet assay and cytogenetic tests","volume":"61","author":"Feng","year":"2005","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_14","first-page":"99","article-title":"In Situ replication of honey bee colony collapse disorder","volume":"65","author":"Lu","year":"2012","journal-title":"Bull. Insectology"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/j.cosust.2013.05.007","article-title":"Neonicotinoids, bee disorders and the sustainability of pollinator services","volume":"5","author":"Goulson","year":"2013","journal-title":"Curr. Opin. Environ. Sustain."},{"key":"ref_16","first-page":"599","article-title":"Estimate of managed colony losses in the winter of 2006\u20132007: A report commissioned by the apiary inspectors of America","volume":"147","author":"Underwood","year":"2007","journal-title":"Am. Bee J."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s11356-014-3220-1","article-title":"Worldwide integrated assessment on systemic pesticides","volume":"22","author":"Bonmatin","year":"2015","journal-title":"Environ. Sci. Poll. Res."},{"key":"ref_18","unstructured":"Guzman-Novoa, E. (2016). Colony collapse disorder and other threats to honey bees. One Health Case Studies: Addressing Complex Problems in a Changing World, Cork, S., Hall, D., Liljebjelke, K., Eds., 5M Publishing Ltd."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"S80","DOI":"10.1016\/j.jip.2009.06.011","article-title":"A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them","volume":"103","author":"Meixner","year":"2010","journal-title":"J. Invertebr. Pathol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1007\/s11356-014-3332-7","article-title":"Environmental fate and exposure; neonicotinoids and fipronil","volume":"22","author":"Bonmatin","year":"2015","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1007\/s13592-019-00672-1","article-title":"Sublethal exposure to clothianidin during the larval stage causes long-term impairment of hygienic and foraging behaviours of honey bees","volume":"50","author":"Morfin","year":"2019","journal-title":"Apidologie"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"5196","DOI":"10.1038\/s41598-019-41365-0","article-title":"Effects of sublethal doses of clothianidin and\/or V. destructor on honey bee (Apis mellifera) self-grooming behavior and associated gene expression","volume":"9","author":"Morfin","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Morfin, N., Goodwin, P.H., Correa-Benitez, A., and Guzman-Novoa, E. (2020). The combined effects of Varroa destructor parasitism and exposure to neonicotinoids affects honey bee (Apis mellifera L.) memory and gene expression. Biology, 9.","DOI":"10.3390\/biology9090237"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Morfin, N., Goodwin, P.H., and Guzman-Novoa, E. (2020). Interaction of Varroa destructor and sublethal clothianidin doses during the larval stage on subsequent adult honey bee (Apis mellifera L.) health, cellular immunity, deformed wing virus levels and differential gene expression. Microorganisms, 8.","DOI":"10.3390\/microorganisms8060858"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Morfin, N., Goodwin, P.H., and Guzman-Novoa, E. (2020). Interaction of field realistic doses of clothianidin and Varroa destructor parasitism on adult honey bee (Apis mellifera L.) health and neural gene expression, and antagonistic effects on differentially expressed genes. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0229030"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"gmr16039908","DOI":"10.4238\/gmr16039908","article-title":"Sub-lethal doses of neonicotinoid and carbamate insecticides reduce the lifespan and alter the expression of immune health and detoxification related genes of honey bees (Apis mellifera)","volume":"17","author":"Tarek","year":"2018","journal-title":"Gen. Mol. Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/j.ecoenv.2019.05.007","article-title":"The neonicotinoid clothianidin impairs memory processing in honey bees. Ecotoxicol","volume":"180","author":"Tison","year":"2019","journal-title":"Environ. Saf."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1007\/s11356-014-3277-x","article-title":"Risk of large-scale use of systemic insecticides to ecosystem functioning and services. Environ","volume":"22","author":"Chagnon","year":"2015","journal-title":"Sci. Pollut. Res."},{"key":"ref_29","first-page":"147","article-title":"The death of honey bees and environmental pollution by pesticides: The honey bees as biological indicators","volume":"56","author":"Porrini","year":"2003","journal-title":"Bull. Insectology"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"116566","DOI":"10.1016\/j.envpol.2021.116566","article-title":"Pesticides in honey bee colonies: Establishing a baseline for real world exposure over seven years in the USA","volume":"279","author":"Traynor","year":"2021","journal-title":"Environ. Pollut."},{"key":"ref_31","unstructured":"Bejarano-Gonz\u00e1lez, F. (2017). Abejas e insecticidas. Los Plaguicidas Altamente Peligrosos en M\u00e9xico, Red de Acci\u00f3n sobre Plaguicidas y Alternativas en M\u00e9xico (RAPAM)."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"108457","DOI":"10.1016\/j.ecolind.2021.108457","article-title":"Honey bees as biomonitors of environmental contaminants, pathogens, and climate change","volume":"134","author":"Cunningham","year":"2022","journal-title":"Ecol. Indic."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1080\/02772240802294870","article-title":"Bee honey as environmental indicator for pollution with heavy metals","volume":"91","author":"Rashed","year":"2009","journal-title":"Toxicol. Environ. Chem."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/j.envpol.2013.03.029","article-title":"Ionic profile of honey as potential indicator of botanical origin and global environmental pollution","volume":"178","author":"Fermo","year":"2013","journal-title":"Environ. Pollut."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1007\/BF01685763","article-title":"Honey as an environmental indicator of radionuclide contamination","volume":"19","author":"Gilbert","year":"1978","journal-title":"Bull. Environ. Cont. Toxicol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1126\/science.aan3684","article-title":"A worldwide survey of neonicotinoids in honey","volume":"358","author":"Mitchell","year":"2017","journal-title":"Science"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Cernansky, R. (2017). Controversial pesticides found in honey samples from six continents. Nature.","DOI":"10.1038\/nature.2017.22762"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1080\/00218839.2017.1340798","article-title":"Agricultural pesticide residues in honey and wax combs from Southeastern and Northeastern Mexico","volume":"56","year":"2017","journal-title":"J. Apic. Res."},{"key":"ref_39","unstructured":"Instituto Nacional de Estad\u00edstica, and Geograf\u00eda e Inform\u00e1tica (INEGI) (2020, August 05). Encuesta Nacional Agropecuaria. Superficie Cultivada y Producci\u00f3n de Cultivos Anuales por Entidad. Producci\u00f3n de Agricultura protegida por entidad., Available online: https:\/\/www.inegi.org.mx\/programas\/ena\/2017\/default.html#Tabulados."},{"key":"ref_40","unstructured":"Servicio de Informaci\u00f3n Agroalimentaria y Pesquera (SIAP) (2020, October 08). Agricultura de Temporal por Municipio. Available online: https:\/\/nube.siap.gob.mx\/cierreagricola\/."},{"key":"ref_41","unstructured":"Servicio de Informaci\u00f3n Agroalimentaria y Pesquera (SIAP) (2020, February 01). Anuario Estad\u00edstico de Producci\u00f3n Ganadera\/miel por Municipio de Jalisco. Available online: https:\/\/nube.siap.gob.mx\/cierre_pecuario\/."},{"key":"ref_42","unstructured":"Google Earth (2021, March 03). Jalisco State Map, Mexico at Google Maps. Available online: https:\/\/www.google.com\/maps\/place\/Jalisco."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1093\/jaoac\/92.1.279","article-title":"Determination of 142 pesticides in fruit and vegetable based infant foods by liquid chromatography\/electrospray ionization-tandem mass spectrometry and estimation of measurement uncertainty","volume":"92","author":"Wang","year":"2009","journal-title":"J. AOAC Int."},{"key":"ref_44","unstructured":"Pesticide Action Network International (PAN) (2021, July 07). Pesticide Info. by Chemical Search. Available online: http:\/\/www.pesticideinfo.org."},{"key":"ref_45","unstructured":"European Commission (EC) (2021, January 02). Maximum Residue Levels. Available online: https:\/\/ec.europa.eu\/food\/plant\/pesticides\/max_residue_levels_en."},{"key":"ref_46","first-page":"1799","article-title":"Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees","volume":"216","author":"Williamson","year":"2013","journal-title":"J. Exp. Biol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1007\/s11356-014-3471-x","article-title":"Effects of neonicotinoids and fipronil on non-target invertebrates","volume":"22","author":"Pisa","year":"2015","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/j.pestbp.2014.12.026","article-title":"The formulation makes the honey bee poison","volume":"120","author":"Mullin","year":"2015","journal-title":"Pestic. Biochem. Physiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"6145","DOI":"10.1007\/s11356-017-9227-7","article-title":"Exposure assessment of honeybees through study of hive matrices: Analysis of selected pesticide residues in honeybees, beebread, and beeswax from French beehives by LC-MS\/MS","volume":"25","author":"Daniele","year":"2018","journal-title":"Environ. Sci. Pollut Res."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Scripc\u00e2, L.A., and Amariei, S. (2021). The Influence of Chemical Contaminants on the Physicochemical Properties of Unifloral and Multifloral Honey. Foods, 10.","DOI":"10.3390\/foods10051039"},{"key":"ref_51","first-page":"257","article-title":"The flight range of the honeybee","volume":"47","author":"Eckert","year":"1933","journal-title":"J. Agric. Res."},{"key":"ref_52","first-page":"474","article-title":"Research review. How far will bees fly? Glean","volume":"112","author":"Morse","year":"1984","journal-title":"Bee Cult."},{"key":"ref_53","unstructured":"Herrero-LaTorre, C., Barciela-Garc\u00eda, J., Garc\u00eda-Mart\u00edn, S., and Crescente-Pe\u00f1a, R.M. (2021, January 15). The Use of Honeybees and Honey as Environmental Bioindicators for Metals and Radionuclides: A Review. Available online: https:\/\/tspace.library.utoronto.ca\/bitstream\/1807\/78891\/1\/er-2017-0029.pdf."},{"key":"ref_54","unstructured":"Pesticide Action Network International (PAN) (2021, December 07). PAN International List of Highly Hazardous Pesticides. Available online: https:\/\/www.uccs.mx\/images\/library\/file\/externos\/HHP_Lista_PAN_2015corr.pdf."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"047014","DOI":"10.1289\/EHP2698","article-title":"Effects of neonicotinoid pesticides on promoter-specific aromatase (CYP19) expression in Hs578t breast cancer cells and the role of the VEGF pathway","volume":"126","author":"Viau","year":"2018","journal-title":"Environ. Health Persp."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Yang, E.C., Chang, H.C., Wu, W.Y., and Chen, Y.-W. (2012). Impaired olfactory associative behavior of honeybee workers due to contamination of imidacloprid in the larval stage. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0049472"},{"key":"ref_57","unstructured":"Winston, M.L. (1987). The Biology of the Honey Bee, Harvard University Press."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"2022","DOI":"10.1242\/jeb.068718","article-title":"A nicotinic acetylcholine receptor agonist affects honey bee sucrose responsiveness and decreases waggle dancing","volume":"215","author":"Eiri","year":"2012","journal-title":"J. Experim. Biol."},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Schneider, C.W., Tautz, J., Gr\u00fcnewald, B., and Fuchs, S. (2012). RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0030023"}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/19\/13\/8199\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:42:49Z","timestamp":1760139769000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/19\/13\/8199"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,7,5]]},"references-count":59,"journal-issue":{"issue":"13","published-online":{"date-parts":[[2022,7]]}},"alternative-id":["ijerph19138199"],"URL":"https:\/\/doi.org\/10.3390\/ijerph19138199","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,7,5]]}}}