{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T11:02:02Z","timestamp":1790074922012,"version":"4.0.1"},"reference-count":76,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2019,9,2]],"date-time":"2019-09-02T00:00:00Z","timestamp":1567382400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Insects"],"abstract":"<jats:p>Honey bees forage across a large area, continually scouting the local landscape for ephemeral food resources. Beekeepers often rely on flowering plants in and around irrigated farmland to maintain their colonies during dry seasons, despite the potential risk of pesticide exposure. Recent declines in pollinator abundance and diversity have focused attention on the role of pesticides and their effects on honey bee health. This investigation examined two types of landscapes within a two-mile (3.2 km) radius of honey bee colonies: an intensive agricultural setting and a rural setting without intensive agriculture. More than 10,000 acres of agricultural land was surveyed to quantify the area of cultivated crops and the area treated with pesticides, including seed treatments and foliar applications of insecticides. Samples of honey, bee bread (stored pollen), beeswax, and adult bees were collected from hives in both landscape types and screened for pesticide residues to determine if foraging bees were transporting pesticides to hives. Some samples of bee bread and honey did contain pesticide residues, but these were below known lethal dose (LD50) levels for honey bees. Beeswax samples contained the highest levels of contamination, but most were still relatively low. Samples were screened for 174 common agricultural pesticides and metabolites, but only 26 compounds were detected during the two-year study. These included one defoliant, one insect growth regulator, five herbicides, six fungicides, six insecticides never used in beekeeping, and five insecticides\/miticides and their metabolites, which are used in beekeeping and for various other agricultural purposes, as well as two miticides exclusively used by beekeepers to control Varroa destructor. Bee colonies foraging in agricultural landscapes are potentially exposed to numerous pesticide applications. While the residues detected in this study did not pose an acute lethal risk to adult honey bees, this study did not measure sublethal effects on bee colony health or performance, which merit further investigation.<\/jats:p>","DOI":"10.3390\/insects10090280","type":"journal-article","created":{"date-parts":[[2019,9,3]],"date-time":"2019-09-03T03:06:14Z","timestamp":1567479974000},"page":"280","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":29,"title":["Comprehensive Survey of Area-Wide Agricultural Pesticide Use in Southern United States Row Crops and Potential Impact on Honey Bee Colonies"],"prefix":"10.3390","volume":"10","author":[{"given":"Jon","family":"Zawislak","sequence":"first","affiliation":[{"name":"Department of Entomology and Plant Pathology, University of Arkansas System, Division of Agriculture, Little Rock, AR 72204, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6536-7255","authenticated-orcid":false,"given":"John","family":"Adamczyk","sequence":"additional","affiliation":[{"name":"Southern Horticultural Laboratory, Agricultural Research Service, United States Department of Agriculture, Poplarville, MS 39470, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Donald R.","family":"Johnson","sequence":"additional","affiliation":[{"name":"Department of Entomology and Plant Pathology, University of Arkansas System, Division of Agriculture, Lonoke, AR 72086, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gus","family":"Lorenz","sequence":"additional","affiliation":[{"name":"Department of Entomology and Plant Pathology, University of Arkansas System, Division of Agriculture, Lonoke, AR 72086, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joe","family":"Black","sequence":"additional","affiliation":[{"name":"Department of Entomology and Plant Pathology, University of Arkansas System, Division of Agriculture, Lonoke, AR 72086, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Quinton","family":"Hornsby","sequence":"additional","affiliation":[{"name":"Department of Entomology and Plant Pathology, University of Arkansas System, Division of Agriculture, Lonoke, AR 72086, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Scott D.","family":"Stewart","sequence":"additional","affiliation":[{"name":"Department of Entomology and Plant Pathology, Department of Entomology and Plant Pathology, The University of Tennessee, Knoxville, TN 37996, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Neelendra","family":"Joshi","sequence":"additional","affiliation":[{"name":"Department of Entomology and Plant Pathology, University of Arkansas, Fayetteville, AR 72701, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,9,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1790","DOI":"10.2307\/1940121","article-title":"Foraging Strategy of Honeybee Colonies in a Temperate Deciduous Forest","volume":"63","author":"Visscher","year":"1982","journal-title":"Ecology"},{"key":"ref_2","first-page":"1","article-title":"Foraging Range of Honey Bees, Apis mellifera, in Alfalfa Seed Production Fields","volume":"11","author":"Hagler","year":"2011","journal-title":"J. Insect Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1098\/rspb.2002.2292","article-title":"Honeybee foraging in differentially structured landscapes","volume":"270","author":"Kuhn","year":"2003","journal-title":"Proc. R. Soc. B Boil. Sci."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1007\/s13592-014-0302-5","article-title":"Honey bee foraging distance depends on month and forage type","volume":"46","author":"Couvillon","year":"2015","journal-title":"Apidologie"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"490","DOI":"10.1046\/j.1365-2435.2000.00443.x","article-title":"Long-range foraging by the honey-bee, Apis mellifera L.","volume":"14","author":"Beekman","year":"2000","journal-title":"Funct. Ecol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1007\/BF00679014","article-title":"Honey bee foraging profitability and round dance correlates","volume":"148","author":"Waddington","year":"1982","journal-title":"J. Comp. Physiol. A"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"622","DOI":"10.1046\/j.1365-2311.2003.00548.x","article-title":"Are honey bees\u2019 foraging preferences affected by pollen amino acid composition?","volume":"28","author":"Cook","year":"2003","journal-title":"Ecol. Entomol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1007\/s00265-016-2067-5","article-title":"Honey bee foragers balance colony nutritional deficiencies","volume":"70","author":"Hendriksma","year":"2016","journal-title":"Behav. Ecol. Sociobiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1016\/j.tree.2013.01.019","article-title":"Pollinator-mediated evolution of floral signals","volume":"28","author":"Schiestl","year":"2013","journal-title":"Trends Ecol. Evol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1007\/s00442-007-0752-9","article-title":"Bee foraging ranges and their relationship to body size","volume":"153","author":"Greenleaf","year":"2007","journal-title":"Oecologia"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"233","DOI":"10.2307\/2398797","article-title":"Dispersal versus gene flow in plants","volume":"68","author":"Levin","year":"1981","journal-title":"Ann. Mo. Bot. Gard."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1111\/eea.12424","article-title":"Beyond nectar provision: The other resource requirements of parasitoid biological control agents","volume":"159","author":"Gillespie","year":"2016","journal-title":"Entomol. Exp. Appl."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Heidel-Baker, T.T., O\u2019Neal, M.E., Batzer, J.C., and Gleason, M.L. (2014). Attracting Beneficial Insects to Iowa Agricultural Crops through Floral Provisioning, Iowa State University.","DOI":"10.31274\/farmprogressreports-180814-1782"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.agee.2014.08.024","article-title":"Optimizing field margins for biocontrol services: The relative role of aphid abundance, annual floral resources, and overwinter habitat in enhancing aphid natural enemies","volume":"199","author":"Ramsden","year":"2015","journal-title":"Agric. Ecosyst. Environ."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Calderone, N.W. (2012). Insect Pollinated Crops, Insect Pollinators and US Agriculture: Trend Analysis of Aggregate Data for the Period 1992\u20132009. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0037235"},{"key":"ref_16","unstructured":"McGregor, S.E. (1976). Insect Pollination of Cultivated Crop Plants."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1080\/00218839.1981.11100480","article-title":"A Chronology of Pollen Collection by Honeybees","volume":"20","author":"Severson","year":"1981","journal-title":"J. Apic. Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1093\/jee\/71.4.601","article-title":"Honey Bee Pollination Increases Soybean Yields in the Mississippi Delta Region of Arkansas and Missouri","volume":"71","author":"Erickson","year":"1978","journal-title":"J. Econ. Entomol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1590\/S1516-89132005000100005","article-title":"Pollination of soybean (Glycine max L. Merril) by honeybees (Apis mellifera L.)","volume":"48","author":"Chiari","year":"2005","journal-title":"Braz. Arch. Biol. Technol."},{"key":"ref_20","first-page":"221","article-title":"Pollination in oil crops: Recent advances and future strategies","volume":"Volume 2","author":"Abrol","year":"2012","journal-title":"Technological Innovations in Major World Oil Crops"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1007\/s10311-013-0412-8","article-title":"Higher soybean production using honeybee and wild pollinators, a sustainable alternative to pesticides and autopollination","volume":"11","author":"Milfont","year":"2013","journal-title":"Environ. Chem. Lett."},{"key":"ref_22","unstructured":"Coy, R. Personal communications."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Smith, T., Catchot, A.L., Harris, J.W., Gore, J., Krishnan, N., and Cook, D. (2017, January 8). Influence of cultural practices on soybean nectar production. Proceedings of the Entomological Society of America Conference, Denver, CO, USA.","DOI":"10.1603\/ICE.2016.109936"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1104\/pp.27.1.95","article-title":"Some Factors Affecting Nectar Secretion in Red Clover","volume":"27","author":"Shuel","year":"1952","journal-title":"Plant. Physiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"881","DOI":"10.1890\/14-1011.1","article-title":"Honey bee diet in intensive farmland habitats reveals an unexpectedly high flower richness and a major role of weeds","volume":"25","author":"Requier","year":"2015","journal-title":"Ecol. Appl."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Di Pasquale, G., Salignon, M., Le Conte, Y., Belzunces, L.P., Decourtye, A., Kretzschmar, A., Suchail, S., Brunet, J.L., and Alaux, C. (2013). Influence of pollen nutrition on honey bee health: Do pollen quality and diversity matter?. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0072016"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"838","DOI":"10.7717\/peerj.838","article-title":"Honey bee success predicted by landscape composition in Ohio, USA","volume":"3","author":"Sponsler","year":"2015","journal-title":"PeerJ"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1146\/annurev.ento.52.110405.091440","article-title":"The Sublethal Effects of Pesticides on Beneficial Arthropods","volume":"52","author":"Desneux","year":"2007","journal-title":"Annu. Rev. Entomol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1051\/apido\/2010018","article-title":"Pesticides and honey bee toxicity\u2014USA","volume":"41","author":"Johnson","year":"2010","journal-title":"Apidologie"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"973","DOI":"10.1007\/s10646-012-0863-x","article-title":"Neonicotinoids in bees: A review on concentrations, side-effects and risk assessment","volume":"21","author":"Smagghe","year":"2012","journal-title":"Ecotoxicology"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Lundin, O., Rundl\u00f6f, M., Smith, H.G., Fries, I., and Bommarco, R. (2015). Neonicotinoid Insecticides and Their Impacts on Bees: A Systematic Review of Research Approaches and Identification of Knowledge Gaps. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0136928"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1051\/apido:2004071","article-title":"Modes of honeybees exposure to systemic insecticides: Estimated amounts of contaminated pollen and nectar consumed by different categories of bees","volume":"36","author":"Rortais","year":"2005","journal-title":"Apidologie"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Dively, G.P., Embrey, M.S., Kamel, A., Hawthorne, D.J., and Pettis, J.S. (2015). Correction: Assessment of Chronic Sublethal Effects of Imidacloprid on Honey Bee Colony Health. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0126043"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1937","DOI":"10.1007\/s10646-012-0927-y","article-title":"Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris)","volume":"21","author":"Laycock","year":"2012","journal-title":"Ecotoxicology"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1126\/science.1215025","article-title":"Neonicotinoid Pesticide Reduces Bumble Bee Colony Growth and Queen Production","volume":"336","author":"Whitehorn","year":"2012","journal-title":"Science"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1016\/j.biocon.2006.02.025","article-title":"Regional problems need integrated solutions: Pest management and conservation biology in agroecosystems","volume":"131","author":"Cumming","year":"2006","journal-title":"Boil. Conserv."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1093\/jee\/99.2.253","article-title":"A Survey of Pesticide Residues in Pollen Loads Collected by Honey Bees in France","volume":"99","author":"Chauzat","year":"2006","journal-title":"J. Econ. Entomol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1964","DOI":"10.1603\/EC10235","article-title":"Overview of Pesticide Residues in Stored Pollen and Their Potential Effect on Bee Colony (Apis mellifera) Losses in Spain","volume":"103","author":"Bernal","year":"2010","journal-title":"J. Econ. Entomol."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Mullin, C.A., Frazier, M., Frazier, J.L., Ashcraft, S., Simonds, R., and Pettis, J.S. (2010). High levels of miticides and agrochemicals in North American apiaries: Implications for honey bee health. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0009754"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"2321","DOI":"10.1016\/j.chemosphere.2015.10.135","article-title":"Concentrations of neonicotinoid insecticides in honey, pollen and honey bees (Apis mellifera L.) in central Saskatchewan, Canada","volume":"144","author":"Codling","year":"2016","journal-title":"Chemosphere"},{"key":"ref_41","unstructured":"(2018). Pasture, Fall Armyworm. Insecticide Recommendations for Arkansas, MP-144, University of Arkansas Systems Division of Agriculture. Available online: https:\/\/www.uaex.edu\/publications\/pdf\/mp144\/mp144.pdf."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"9762","DOI":"10.1021\/es501657w","article-title":"Potential Exposure of Pollinators to Neonicotinoid Insecticides from the Use of Insecticide Seed Treatments in the Mid-Southern United States","volume":"48","author":"Stewart","year":"2014","journal-title":"Environ. Sci. Technol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"164","DOI":"10.3896\/IBRA.1.51.2.03","article-title":"The concentration effect of selected acaricides present in beeswax foundation on the survival of Apis mellifera colonies","volume":"51","author":"Medici","year":"2012","journal-title":"J. Apic. Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"5835","DOI":"10.1021\/jf010787s","article-title":"Study of Acaricide Stability in Honey. Characterization of Amitraz Degradation Products in Honey and Beeswax","volume":"49","author":"Korta","year":"2001","journal-title":"J. Agric. Food Chem."},{"key":"ref_45","first-page":"57","article-title":"Coumaphos residues in honey, bee brood, and beeswax after Varroa treatment","volume":"37","author":"Bajuk","year":"2017","journal-title":"Apidologie"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1719","DOI":"10.1016\/j.foodchem.2005.10.034","article-title":"Multiresidue determination of pesticides in honey samples by gas chromatography\u2013mass spectrometry and application in environmental contamination","volume":"101","author":"Rissato","year":"2007","journal-title":"Food Chem."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Alburaki, M., Chen, D., Skinner, J.A., Meikle, W.G., Tarpy, D.R., Adamczyk, J., and Stewart, S.D. (2018). Honey Bee Survival and Pathogen Prevalence: From the Perspective of Landscape and Exposure to Pesticides. Insects, 9.","DOI":"10.3390\/insects9020065"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1051\/apido:2005043","article-title":"Contaminants of bee products","volume":"37","author":"Bogdanov","year":"2006","journal-title":"Apidologie"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1007\/s13592-014-0273-6","article-title":"Potential impacts of synergism in honeybees (Apis mellifera) of exposure to neonicotinoids and sprayed fungicides in crops","volume":"45","author":"Thompson","year":"2014","journal-title":"Apidologie"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Johnson, R.M., Dahlgren, L., Siegfried, B.D., and Ellis, M.D. (2013). Acaricide, Fungicide and Drug Interactions in Honey Bees (Apis mellifera). PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0054092"},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Pettis, J.S., Lichtenberg, E.M., Andree, M., Stitzinger, J., and Rose, R. (2013). Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0070182"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1743","DOI":"10.1603\/0022-0493-101.6.1743","article-title":"Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae)","volume":"101","author":"Yang","year":"2008","journal-title":"J. Econ. Entomol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1463","DOI":"10.1111\/ele.12188","article-title":"Chronic sublethal stress causes bee colony failure","volume":"16","author":"Bryden","year":"2013","journal-title":"Ecol. Lett."},{"key":"ref_54","first-page":"303","article-title":"A common neonicotinoid pesticide, thiamethoxam, impairs honey bee flight ability","volume":"7","author":"Tosi","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Wu, J.Y., Anelli, C.M., and Sheppard, W.S. (2011). Sub-Lethal Effects of Pesticide Residues in Brood Comb on Worker Honey Bee (Apis mellifera) Development and Longevity. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0014720"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/S0039-9140(98)00237-9","article-title":"Kinetics and mechanism of amitraz hydrolysis in aqueous media by HPLC and GC-MS","volume":"48","author":"Corta","year":"1999","journal-title":"Talanta"},{"key":"ref_57","unstructured":"Vita Bee Health (2018, June 18). Apiguard Product Label. Valdosta, GA 31603, Available online: https:\/\/www3.epa.gov\/pesticides\/chem_search\/ppls\/079671-00001-20141007.pdf."},{"key":"ref_58","unstructured":"V\u00e9to-pharma, Inc. (2018, June 18). ApiLifeVar Product Label. Palaiseau, France 91120, Available online: https:\/\/www3.epa.gov\/pesticides\/chem_search\/ppls\/073291-00001-20190521.pdf."},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Krupke, C.H., Hunt, G.J., Eitzer, B.D., Andino, G., and Given, K. (2012). Multiple Routes of Pesticide Exposure for Honey Bees Living Near Agricultural Fields. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0029268"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"4449","DOI":"10.1021\/jf205393x","article-title":"Insecticide Residues in Pollen and Nectar of a Cucurbit Crop and Their Potential Exposure to Pollinators","volume":"60","author":"Dively","year":"2012","journal-title":"J. Agric. Food Chem."},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Meikle, W.G., Adamczyk, J.J., Weiss, M., Gregorc, A., Johnson, D.R., Stewart, S.D., Zawislak, J., Carroll, M.J., and Lorenz, G.M. (2016). Sublethal Effects of Imidacloprid on Honey Bee Colony Growth and Activity at Three Sites in the US. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0168603"},{"key":"ref_62","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_63","doi-asserted-by":"crossref","first-page":"961","DOI":"10.1046\/j.1461-0248.2003.00523.x","article-title":"Mass flowering crops enhance pollinator densities at a landscape scale","volume":"6","author":"Westphal","year":"2003","journal-title":"Ecol. Lett."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/j.agee.2010.01.015","article-title":"Intensification of agriculture, landscape composition and wild bee communities: A large scale study in four European countries","volume":"137","author":"Delettre","year":"2010","journal-title":"Agric. Ecosyst. Environ."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1007\/s00442-012-2515-5","article-title":"Mass-flowering crops enhance wild bee abundance","volume":"172","author":"Holzschuh","year":"2013","journal-title":"Oecologia"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1002\/ps.2780390407","article-title":"Synergism between EBI fungicides and a pyrethroid insecticide in the honeybee (Apis mellifera)","volume":"39","author":"Pilling","year":"1993","journal-title":"Pestic. Sci."},{"key":"ref_67","first-page":"131","article-title":"Assessment of the synergy and repellency of pyrethroid\/fungicide mixtures","volume":"56","author":"Thompson","year":"2003","journal-title":"Bull. Insectol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1603\/0022-0493-95.1.28","article-title":"Effects of Fluvalinate and Coumaphos on Queen Honey Bees (Hymenoptera: Apidae) in Two Commercial Queen Rearing Operations","volume":"95","author":"Haarmann","year":"2002","journal-title":"J. Econ. Entomol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"18466","DOI":"10.1073\/pnas.1314923110","article-title":"Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees","volume":"110","author":"Cavaliere","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Zhu, W., Schmehl, D.R., Mullin, C.A., and Frazier, J.L. (2014). Four Common Pesticides, Their Mixtures and a Formulation Solvent in the Hive Environment Have High Oral Toxicity to Honey Bee Larvae. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0077547"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1146\/annurev-ento-011613-162005","article-title":"Honey Bee Toxicology","volume":"60","author":"Johnson","year":"2015","journal-title":"Annu. Rev. Entomol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"S96","DOI":"10.1016\/j.jip.2009.07.016","article-title":"Biology and control of Varroa destructor","volume":"103","author":"Rosenkranz","year":"2010","journal-title":"J. Invertebr. Pathol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1051\/apido\/2009076","article-title":"Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada","volume":"41","author":"Eccles","year":"2010","journal-title":"Apidologie"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1016\/j.jip.2007.07.010","article-title":"Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States","volume":"97","author":"Chen","year":"2008","journal-title":"J. Invertebr. Pathol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1098\/rsbl.2009.0986","article-title":"Diet effects on honeybee immunocompetence","volume":"6","author":"Alaux","year":"2010","journal-title":"Boil. Lett."},{"key":"ref_76","doi-asserted-by":"crossref","unstructured":"Vanengelsdorp, D., Evans, J.D., Saegerman, C., Mullin, C., Haubruge, E., Nguyen, B.K., Frazier, M., Frazier, J., Cox-Foster, D., and Chen, Y. (2009). Colony Collapse Disorder: A Descriptive Study. 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