{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,28]],"date-time":"2026-04-28T06:39:29Z","timestamp":1777358369895,"version":"3.51.4"},"reference-count":38,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2023,8,15]],"date-time":"2023-08-15T00:00:00Z","timestamp":1692057600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Science and Technology Council of Taiwan","award":["MOST109-2314-B-320-002-MY2"],"award-info":[{"award-number":["MOST109-2314-B-320-002-MY2"]}]},{"name":"National Science and Technology Council of Taiwan","award":["610400184-11"],"award-info":[{"award-number":["610400184-11"]}]},{"name":"Tzu Chi University","award":["MOST109-2314-B-320-002-MY2"],"award-info":[{"award-number":["MOST109-2314-B-320-002-MY2"]}]},{"name":"Tzu Chi University","award":["610400184-11"],"award-info":[{"award-number":["610400184-11"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Toxics"],"abstract":"<jats:p>While pollinating, honeybees are subject to exposure to a variety of pesticides; with their characteristics of certain foraging distances, they could serve as bioindicators of pesticide exposure in a neighborhood. We conducted a study to assess availability by collecting and analyzing bee samples from 15 apiaries located in East Taiwan and dust samples from the adjacent environment, and by finding relations between both samples. Seventeen pesticides were selected for the analysis using gas or liquid chromatography coupled with mass spectrometry, and eight (three insecticides, two herbicides, and three fungicides) were more frequently detected from bee or dust samples; the levels of these pesticides were mostly under 1000 ng\/g. Significant correlation results (r \u2245 0.8) between residue concentrations in bees and in dust suggest that honeybees could be a good bioindicator for exposure to herbicides and fungicides within certain ranges. The pesticide contents of sick\/dead bees were much higher than those of healthy counterparts regarding any pesticide type, with the mean total concentrations of 635 ng\/g and 176 ng\/g, respectively. We conclude that honeybees could be used as bioindicators of pesticide exposure; sick\/dead bees could serve as a warning sign of the severity of pesticide pollution.<\/jats:p>","DOI":"10.3390\/toxics11080703","type":"journal-article","created":{"date-parts":[[2023,8,15]],"date-time":"2023-08-15T11:15:08Z","timestamp":1692098108000},"page":"703","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["Availability of Using Honeybees as Bioindicators of Pesticide Exposure in the Vicinity of Agricultural Environments in Taiwan"],"prefix":"10.3390","volume":"11","author":[{"given":"Chien-Che","family":"Hung","sequence":"first","affiliation":[{"name":"Department of Public Health, Tzu Chi University, 701, Sec. 3, Zhongyang Road, Hualien City 970374, Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7732-9291","authenticated-orcid":false,"given":"Lih-Ming","family":"Yiin","sequence":"additional","affiliation":[{"name":"Department of Public Health, Tzu Chi University, 701, Sec. 3, Zhongyang Road, Hualien City 970374, Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,8,15]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1023\/A:1010655503471","article-title":"An investigation of the relationship between pesticide usage and climate change","volume":"50","author":"Chen","year":"2001","journal-title":"Clim. Chang."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.foodres.2014.09.030","article-title":"Literature review: Impact of climate change on pesticide use","volume":"68","author":"Delcour","year":"2015","journal-title":"Food Res. Int."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"121","DOI":"10.2478\/v10001-008-0014-z","article-title":"Prenatal and childhood exposure to pesticides and neurobehavioral development: Review of epidemiological studies","volume":"21","author":"Jurewicz","year":"2008","journal-title":"Int. J. Occup. Med. Environ. Health"},{"key":"ref_4","first-page":"719","article-title":"Limitation of point source pesticide pollution: Results of bioremediation system","volume":"69","author":"Spanoghe","year":"2004","journal-title":"Commun. Agric. Appl. Biol. Sci."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Simaremare, S.R.S., Hung, C.-C., Yu, T.-H., Hsieh, C.-J., and Yiin, L.-M. (2021). Association between Pesticides in House Dust and Residential Proximity to Farmland in a Rural Region of Taiwan. Toxics, 9.","DOI":"10.3390\/toxics9080180"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1006\/enrs.2000.4076","article-title":"Pesticide exposure of children in an agricultural community: Evidence of household proximity to farmland and take home exposure pathways","volume":"84","author":"Lu","year":"2000","journal-title":"Environ. Res."},{"key":"ref_7","first-page":"S269","article-title":"Proximity to agricultural pesticide use and concentrations in carpet dust","volume":"19","author":"Gunier","year":"2008","journal-title":"Epidemiology"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"19632","DOI":"10.1007\/s11356-019-05313-9","article-title":"Agricultural and domestic pesticides in house dust from different agricultural areas in France","volume":"26","author":"Billoir","year":"2019","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1162","DOI":"10.1289\/ehp.1002843","article-title":"Acute Pesticide Illnesses Associated with Off-Target Pesticide Drift from Agricultural Applications: 11 States, 1998\u20132006","volume":"119","author":"Lee","year":"2011","journal-title":"Environ. Health Perspect."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1016\/j.ecolind.2015.06.036","article-title":"How do ecologists select and use indicator species to monitor ecological change? Insights from 14 years of publication in Ecological Indicators","volume":"60","author":"Siddig","year":"2016","journal-title":"Ecol. Indic."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1080\/15555270600701540","article-title":"Bioindicators: A review of their use in the environmental literature 1970\u20132005","volume":"1","author":"Burger","year":"2006","journal-title":"Environ. Bioindic."},{"key":"ref_12","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. Insectol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1007\/s41207-020-00204-9","article-title":"Bioindicators and biomonitoring: Honeybees and hive products as pollution impact assessment tools for the Mediterranean area","volume":"5","author":"Girotti","year":"2020","journal-title":"Euro-Mediterr. J. Environ. Integr."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"970","DOI":"10.1126\/science.316.5827.970","article-title":"The case of the empty hives","volume":"316","author":"Stokstad","year":"2007","journal-title":"Science"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1016\/j.jinsphys.2016.01.001","article-title":"The neonicotinoids thiacloprid, imidacloprid, and clothianidin affect the immunocompetence of honey bees (Apis mellifera L.)","volume":"86","author":"Brandt","year":"2016","journal-title":"J. Insect. Physiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1007\/s40726-020-00142-8","article-title":"A review of sub-lethal neonicotinoid insecticides exposure and effects on pollinators","volume":"6","author":"Lu","year":"2020","journal-title":"Curr. Pollut. Rep."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"11798","DOI":"10.1007\/s11356-017-1052-5","article-title":"An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 3: Alternatives to systemic insecticides","volume":"28","author":"Furlan","year":"2021","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_18","first-page":"7","article-title":"Are bee diseases linked to pesticides?\u2014A brief review","volume":"89","author":"Goulson","year":"2016","journal-title":"Environ. Int."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"111013","DOI":"10.1016\/j.ecoenv.2020.111013","article-title":"Mixtures of an insecticide, a fungicide and a herbicide induce high toxicities and systemic physiological disturbances in winter Apis mellifera honey bees","volume":"203","author":"Almasri","year":"2020","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_20","first-page":"305","article-title":"Comparison of acute toxicity of different groups of pesticides to honey bee workers (Apis mellifera L.)","volume":"34","author":"Ulziibayar","year":"2019","journal-title":"J. Apic."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"81","DOI":"10.3389\/fenvs.2020.00081","article-title":"Effects of fungicide and herbicide chemical exposure on Apis and non-Apis bees in agricultural landscape","volume":"8","author":"Belsky","year":"2020","journal-title":"Front. Environ. Sci."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Farruggia, F.T., Garber, K., Hartless, C., Jones, K., Kyle, L., Mastrota, N., Milone, J.P., Sankula, S., Sappington, K., and Stebbins, K. (2022). A retrospective analysis of honey bee (Apis mellifera) pesticide toxicity data. PLoS ONE, 17.","DOI":"10.1371\/journal.pone.0265962"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Migdal, P., Murawska, A., Berbe\u0107, E., Plotnik, M., Skorus, A., and Latarowski, K. (2022). Selected Biochemical Markers Change after Oral Administration of Pesticide Mixtures in Honey Bees. Toxics, 10.","DOI":"10.3390\/toxics10100590"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Zawislak, J., Adamczyk, J., Johnson, D.R., Lorenz, G., Black, J., Hornsby, Q., Stewart, S.D., and Joshi, N. (2019). Comprehensive survey of area-wide agricultural pesticide use in southern United States row crops and potential impact on honey bee colonies. Insects, 10.","DOI":"10.3390\/insects10090280"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"140436","DOI":"10.1016\/j.scitotenv.2020.140436","article-title":"Beyond neonicotinoids\u2013Wild pollinators are exposed to a range of pesticides while foraging in agroecosystems","volume":"742","author":"Main","year":"2020","journal-title":"Sci. Total Environ."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"154697","DOI":"10.1016\/j.scitotenv.2022.154697","article-title":"Pesticide exposure of wild bees and honey bees foraging from field border flowers in intensively managed agriculture areas","volume":"831","author":"Ward","year":"2022","journal-title":"Sci. Total Environ."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Ostiguy, N., Drummond, F.A., Aronstein, K., Eitzer, B., Ellis, J.D., Spivak, M., and Sheppard, W.S. (2019). Honey bee exposure to pesticides: A four-year nationwide study. Insects, 10.","DOI":"10.3390\/insects10010013"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Berg, C.J., King, H.P., Delenstarr, G., Kumar, R., Rubio, F., and Glaze, T. (2018). Glyphosate residue concentrations in honey attributed through geospatial analysis to proximity of large-scale agriculture and transfer off-site by bees. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0198876"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"23349","DOI":"10.1007\/s11356-018-2413-4","article-title":"Pesticides in indoor and outdoor residential dust: A pilot study in a rural county of Taiwan","volume":"25","author":"Hung","year":"2018","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"\u017baneta Barga\u0144ska, M.S., and Namie\u015bnik, J. (2014). Determination of pesticide residues in honeybees using modified QUEChERS sample work-up and liquid chromatography-tandem mass spectrometry. Molecules, 19.","DOI":"10.3390\/molecules19032911"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1502","DOI":"10.4315\/0362-028X-65.9.1502","article-title":"Analytical methods for pesticide residue determination in bee products","volume":"65","author":"Manes","year":"2002","journal-title":"J. Food Prot."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1051\/apido:19990607","article-title":"Pesticide residues in bee products collected from cherry trees protected during blooming period with contact and systemic fungicides","volume":"30","author":"Kubik","year":"1999","journal-title":"Apidologie"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1051\/apido:2000144","article-title":"Residues of captan (contact) and difenoconazole (systemic) fungicides in bee products from an apple orchard","volume":"31","author":"Kubik","year":"2000","journal-title":"Apidologie"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1111\/j.1365-2583.2006.00672.x","article-title":"A deficit of detoxification enzymes: Pesticide sensitivity and environmental response in the honeybee","volume":"15","author":"Claudianos","year":"2006","journal-title":"Insect Mol. Biol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s10646-016-1742-7","article-title":"Current knowledge of detoxification mechanisms of xenobiotic in honey bees","volume":"26","author":"Gong","year":"2017","journal-title":"Ecotoxicology"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1080\/02772248.2018.1460369","article-title":"Environmental fate and ecotoxicology of paraquat: A California perspective","volume":"100","author":"Sartori","year":"2018","journal-title":"Toxicol. Environ. Chem."},{"key":"ref_37","first-page":"1771","article-title":"Paraquat","volume":"Volume 1","author":"Krieger","year":"2010","journal-title":"Hayes\u2019 Handbook of Pesticide Toxicology"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2448","DOI":"10.1021\/es051392i","article-title":"New risk assessment approach for systemic insecticides: The case of honey bees and imidacloprid (Gaucho)","volume":"40","author":"Halm","year":"2006","journal-title":"Environ. Sci. Technol."}],"container-title":["Toxics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2305-6304\/11\/8\/703\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:33:45Z","timestamp":1760128425000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2305-6304\/11\/8\/703"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8,15]]},"references-count":38,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2023,8]]}},"alternative-id":["toxics11080703"],"URL":"https:\/\/doi.org\/10.3390\/toxics11080703","relation":{},"ISSN":["2305-6304"],"issn-type":[{"value":"2305-6304","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,8,15]]}}}