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Sudden and Prevalent Deaths of Foraging Honey Bees in Early Spring During Sowing of Clothianidin Coated Maize Seeds Between 2013 and 2018 in Turkey


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ADFAL (Adana Directorate of Food, Agriculture and Livestock) Report, (2017). Adana ilinde yaşanan arı ölümlerinin nedenleri, yapılan çalışmalar ve çözüm önerileri raporu (English: Report of bee losses reasons, background studies and suggested solutions in Adana city). Ministry of Agriculture and Forestry in Republic of Turkey (pp:1–10).ADFAL (Adana Directorate of Food, Agriculture and Livestock) Report2017Adana ilinde yaşanan arı ölümlerinin nedenleri, yapılan çalışmalar ve çözüm önerileri raporu(English: Report of bee losses reasons, background studies and suggested solutions in Adana city).Ministry of Agriculture and Forestry in Republic of Turkey110Search in Google Scholar

Albero, B., Sánchez-Brunete, C., & Tadeo, J.L. (2004). Analysis of Pesticides in Honey by Solid-Phase Extraction and Gas Chromatography-Mass Spectrometry. The Journal of Agricultural and Food Chemistry, 52(19), 5828–5835. DOI: 10.1021/jf049470tAlberoB.Sánchez-BruneteC.TadeoJ.L.2004Analysis of Pesticides in Honey by Solid-Phase Extraction and Gas Chromatography-Mass SpectrometryThe Journal of Agricultural and Food Chemistry52195828583510.1021/jf049470t15366828Open DOISearch in Google Scholar

Bacandritsos, N., Granato, A., Budge, G., Papanastasiou, I., Roinioti, E., Caldon, M., … Mutinelli, F. (2010). Sudden deaths and colony population decline in Greek honey bee colonies. Journal of Invertebrate Pathology, 105(3), 335–340. DOI: 10.1016/j.jip.2010.08.004BacandritsosN.GranatoA.BudgeG.PapanastasiouI.RoiniotiE.CaldonM.MutinelliF.2010Sudden deaths and colony population decline in Greek honey bee coloniesJournal of Invertebrate Pathology105333534010.1016/j.jip.2010.08.00420804765Open DOISearch in Google Scholar

Bortolotti, L., Sabatini, A. G., Mutinelli, F., Astuti, M., Lavazza, A., Piro, R., … Porrini, C. (2009). Spring honey bee losses in Italy. Julius-Kühn Archiv, 423, 148–152.BortolottiL.SabatiniA. G.MutinelliF.AstutiM.LavazzaA.PiroR.PorriniC.2009Spring honey bee losses in ItalyJulius-Kühn Archiv423148152Search in Google Scholar

Chauzat, M. P., & Faucon, J. P. (2007). Pesticide residues in beeswax samples collected from honey bee colonies (Apis mellifera L.) in France. Pest Management Science, 63(11), 1100–1106. DOI: 10.1002/ps.1451ChauzatM. P.FauconJ. P.2007Pesticide residues in beeswax samples collected from honey bee colonies (Apis mellifera L.) in FrancePest Management Science63111100110610.1002/ps.145117879980Open DOISearch in Google Scholar

Chauzat, M. P., Faucon, J. P., Martel, A. C., Lachaize, J., Cougoule, N., Aubert, M. (2006). A survey of pesticide residues in pollen loads collected by honey bees in France. Journal of Economic Entomology, 99(2), 253–262. DOI: 10.1603/0022-0493-99.2.253ChauzatM. P.FauconJ. P.MartelA. C.LachaizeJ.CougouleN.AubertM.2006A survey of pesticide residues in pollen loads collected by honey bees in FranceJournal of Economic Entomology99225326210.1603/0022-0493-99.2.25316686121Open DOISearch in Google Scholar

Chauzat, M. P., Martel, A. C., Blanchard, P., Clément, M. C., Schurr, F., Lair, C., … Faucon, J. P. (2010). A case report of a honey bee colony poisoning incident in France. Journal of Apicultural Research, 49(1), 113–115. DOI: 10.3896/IBRA.1.49.1.22ChauzatM. P.MartelA. C.BlanchardP.ClémentM. C.SchurrF.LairC.FauconJ. P.2010A case report of a honey bee colony poisoning incident in FranceJournal of Apicultural Research49111311510.3896/IBRA.1.49.1.22Open DOISearch in Google Scholar

Claudianos, C., Ranson, H., Johnson, R. M., Biswas, S., Schuler, M. A., Barenbaum, M. R., … Oakeshott, J. G. (2006). A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Molecular Biology, 15(5), 615–636. DOI: 10.1111/j.1365-2583.2006.00672.xClaudianosC.RansonH.JohnsonR. M.BiswasS.SchulerM. A.BarenbaumM. R.OakeshottJ. G.2006A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybeeInsect Molecular Biology15561563610.1111/j.1365-2583.2006.00672.x176113617069637Open DOISearch in Google Scholar

EC (European Commission), (2013). Commission Implementing Regulation (EU) No 485/2013. Amending Implementing Regulation (EU) No 540/2011, as regards the conditions of approval of the active substances clothianidin, thiamethoxam and imidacloprid, and prohibiting the use and sale of seeds treated with plant protection products containing those active substances. Official Journal of the European Union, L 139/12–26.EC (European Commission)2013Commission Implementing Regulation (EU) No 485/2013. Amending Implementing Regulation (EU) No 540/2011, as regards the conditions of approval of the active substances clothianidin, thiamethoxam and imidacloprid, and prohibiting the use and sale of seeds treated with plant protection products containing those active substancesOfficial Journal of the European UnionL 139/12–26.Search in Google Scholar

EFSA (European Food Safety Authority), (2013). Conclusion on the peer review of the pesticide risk assessment for bees for the active substance imidacloprid. European Food Safety Authority Journal, 11(1), 3068. DOI: 10.2903/j.efsa.2013.3068EFSA (European Food Safety Authority)2013Conclusion on the peer review of the pesticide risk assessment for bees for the active substance imidaclopridEuropean Food Safety Authority Journal111306810.2903/j.efsa.2013.3068Open DOISearch in Google Scholar

EFSA (European Food Safety Authority), (2018). Conclusion on the peer review of the pesticide risk assessment for bees for the active substance clothianidin considering the uses as seed treatments and granules. EFSA Journal, 16(2), 5177, 86 pp. DOI: 10.2903/j.efsa.2018.5177EFSA (European Food Safety Authority)2018Conclusion on the peer review of the pesticide risk assessment for bees for the active substance clothianidin considering the uses as seed treatments and granulesEFSA Journal16251778610.2903/j.efsa.2018.5177700945132625812Open DOISearch in Google Scholar

EFSA (European Food Safety Authority), Technical Report, (2018). Evaluation of the data on clothianidin, imidacloprid and thiamethoxam for the updated risk assessment to bees for seed treatments and granules in the EU. EFSA Supporting publication. DOI: 10.2903/sp.efsa.2018.EN-1378EFSA (European Food Safety Authority), Technical Report2018Evaluation of the data on clothianidin, imidacloprid and thiamethoxam for the updated risk assessment to bees for seed treatments and granules in the EUEFSA Supporting publication.10.2903/sp.efsa.2018.EN-1378Open DOISearch in Google Scholar

FAO (2018). A. Bee-poisoning symptoms, Chapter 7, pesticides and beekeeping. Retrieved March 26, 2018, from http://www.fao.org/docrep/x0083e/X0083E09.htmFAO2018A. Bee-poisoning symptoms, Chapter 7, pesticides and beekeepingRetrieved March 26, 2018, from http://www.fao.org/docrep/x0083e/X0083E09.htmSearch in Google Scholar

Ferrer, I., García-Reyes, J.F., Mezcua, M., Thurman, E.M., Fernánndez-Alba, A.R. (2005). Multi-residue pesticide analysis in fruits and vegetables by liquid chromatography-time-of-flight mass spectrometry. Journal of Chromatography A, 1082(1), 81–90. DOI: 10.1016/j.chroma.2005.03.040FerrerI.García-ReyesJ.F.MezcuaM.ThurmanE.M.Fernánndez-AlbaA.R.2005Multi-residue pesticide analysis in fruits and vegetables by liquid chromatography-time-of-flight mass spectrometryJournal of Chromatography A10821819010.1016/j.chroma.2005.03.04016038197Open DOISearch in Google Scholar

Girolami, V., Marzaro, M., Vivan, L., Giorio, C., Marton, D., Tapparo, A. (2012a). Aerial powdering of bees inside mobile cages and the extent of the toxic neonicotinoid cloud surrounding corn drillers. Journal of Applied Entomology, 137, 35–44. DOI: 10.1111/j.1439-0418.2012.01718.xGirolamiV.MarzaroM.VivanL.GiorioC.MartonD.TapparoA.2012aAerial powdering of bees inside mobile cages and the extent of the toxic neonicotinoid cloud surrounding corn drillersJournal of Applied Entomology137354410.1111/j.1439-0418.2012.01718.xOpen DOISearch in Google Scholar

Girolami, V., Marzaro, M., Vivan, L., Mazzon, L., Greatti, M., Giorio, C., … Tapparo, A. (2012b). Fatal powdering of bees in flight with particulates of neonicotinoids seed coating and humidity implication. Journal of Applied Entomology, 136(1–2), 17–26. DOI: 10.1111/j.1439-0418.2011.01648.xGirolamiV.MarzaroM.VivanL.MazzonL.GreattiM.GiorioC.TapparoA.2012bFatal powdering of bees in flight with particulates of neonicotinoids seed coating and humidity implicationJournal of Applied Entomology1361–2172610.1111/j.1439-0418.2011.01648.xOpen DOISearch in Google Scholar

Girolami, V., Mazzon, L., Squartini, A., Mori, N., Marzaro, M., Di Bernardo, A., … Tapparo, A. (2009). Translocation of neonicotinoid insecticides from coated seeds to seedling guttation drops: A novel way of intoxication for bees. Journal of Economic Entomology, 102(5), 1808–1815. DOI: 10.1603/029.102.0511GirolamiV.MazzonL.SquartiniA.MoriN.MarzaroM.Di BernardoA.TapparoA.2009Translocation of neonicotinoid insecticides from coated seeds to seedling guttation drops: A novel way of intoxication for beesJournal of Economic Entomology10251808181510.1603/029.102.051119886445Open DOISearch in Google Scholar

Greatti, M., Sabatini, A. G., Barbattini, R., Rossi, S., Stravisi, A. (2003). Risk of environmental contamination by the active ingredient imidacloprid used for corn seed dressing. Preliminary results. Bulletin of Insectology, 56(1), 69–72.GreattiM.SabatiniA. G.BarbattiniR.RossiS.StravisiA.2003Risk of environmental contamination by the active ingredient imidacloprid used for corn seed dressing. Preliminary resultsBulletin of Insectology5616972Search in Google Scholar

Han, S.H., Lee, D.B., Lee, D.W., Kim, E.H., Yoon, B.S. (2008). Ultra-rapid real-time PCR for the detection of Paenibacillus larvae, the causative agent of American Foulbrood (AFB). Journal of Invertebrate Pathology, 99(1), 8–13. DOI: org/10.1016/j.jip.2008.04.010HanS.H.LeeD.B.LeeD.W.KimE.H.YoonB.S.2008Ultra-rapid real-time PCR for the detection of Paenibacillus larvae, the causative agent of American Foulbrood (AFB)Journal of Invertebrate Pathology991813org/10.1016/j.jip.2008.04.010Open DOISearch in Google Scholar

Higes, M., Martín-Hernández, R., Botías, C., Bailón, E., González-Porto, A., Barrios, L., … Meana, A. (2008). How natural infection by Nosema ceranae causes honey bee colony collapse. Environmental Microbiology, 10(10), 2659–2669. DOI: 10.1111/j.1462-2920.2008.01687.xHigesM.Martín-HernándezR.BotíasC.BailónE.González-PortoA.BarriosL.MeanaA.2008How natural infection by Nosema ceranae causes honey bee colony collapseEnvironmental Microbiology10102659266910.1111/j.1462-2920.2008.01687.x18647336Open DOISearch in Google Scholar

Jeschke, P., Nauen, R., Schindler, M., Elbert, A. (2011). Overview of the status and global strategy for neonicotinoids. Journal of Agricultural and Food Chemistry, 59(7), 2897–2908. DOI: 10.1021/jf101303gJeschkeP.NauenR.SchindlerM.ElbertA.2011Overview of the status and global strategy for neonicotinoidsJournal of Agricultural and Food Chemistry5972897290810.1021/jf101303g20565065Open DOISearch in Google Scholar

Johnson, R. M., Ellis, M. D., Mullin, C. A., Frazier, M. (2010). Pesticides and honey bee toxicity-USA. Apidologie, 41(3), 312–31. DOI: 10.1051/apido/2010018JohnsonR. M.EllisM. D.MullinC. A.FrazierM.2010Pesticides and honey bee toxicity-USAApidologie4133123110.1051/apido/2010018Open DOISearch in Google Scholar

Kasiotis, K.M., Anagnostopoulos, C., Anastasiadou, P., Machera, K. (2014). Pesticide residues in honeybees, honey and bee pollen by LC-MS/MS screening: reported death incidents in honeybees. Scince of the Total Environment, 1(485–486), 633–642. DOI: 10.1016/j.scitotenv.2014.03.042KasiotisK.M.AnagnostopoulosC.AnastasiadouP.MacheraK.2014Pesticide residues in honeybees, honey and bee pollen by LC-MS/MS screening: reported death incidents in honeybeesScince of the Total Environment1485–48663364210.1016/j.scitotenv.2014.03.04224747255Open DOISearch in Google Scholar

Kiljanek, T., Niewiadowska, A. & Posyniak, A. (2016). Pesticide Poisoning of Honeybees: A Review of Symptoms, Incident Classification, and Causes of Poisoning. Journal of Apicultural Science, 60(2), 5–24. DOI: 10.1515/JAS-2016-0024KiljanekT.NiewiadowskaA.PosyniakA.2016Pesticide Poisoning of Honeybees: A Review of Symptoms, Incident Classification, and Causes of PoisoningJournal of Apicultural Science60252410.1515/JAS-2016-0024Open DOISearch in Google Scholar

Klein, A. M., Vaissile, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C., Tscharntke, T. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences, 274, 303–313. DOI: 10.1098/rspb.2006.3721KleinA. M.VaissileB. E.CaneJ. H.Steffan-DewenterI.CunninghamS. A.KremenC.TscharntkeT.2007Importance of pollinators in changing landscapes for world cropsProceedings of the Royal Society B: Biological Sciences27430331310.1098/rspb.2006.3721170237717164193Open DOISearch in Google Scholar

Lundin, O., Rundlöf, M., Smith, H. G., Fries, I., Bommarco, R. (2015). Neonicotinoid Insecticides and Their Impacts on Bees: A Systematic Review of Research Approaches and Identification of Knowledge Gaps. PLoS ONE, 10(8): e0136928. DOI: 10.1371/journal.pone.0136928LundinO.RundlöfM.SmithH. G.FriesI.BommarcoR.2015Neonicotinoid Insecticides and Their Impacts on Bees: A Systematic Review of Research Approaches and Identification of Knowledge GapsPLoS ONE108e013692810.1371/journal.pone.0136928455254826313444Open DOISearch in Google Scholar

Martin, S.J., Highfield, A.C., Brettel, L., Villalobos, E.M., Budge, G.E., Powell, M.,… Schroeder, D.C. (2012). Global honey bee viral landscape altered by a parasitic mite. Science, (336), 1034–1036. DOI: 10.1126/science.1220941MartinS.J.HighfieldA.C.BrettelL.VillalobosE.M.BudgeG.E.PowellM.SchroederD.C.2012Global honey bee viral landscape altered by a parasitic miteScience3361034103610.1126/science.122094122679096Open DOISearch in Google Scholar

Marzaro, M., Vivan, L., Targa, A., Mazzon, L., Mori, N., Greatti, M., … Girolami, V. (2011). Lethal aerial powdering of honey bees with neonicotinoids from fragments of maize seed coat. Bulletin of Insectology, 64(1), 119–126.MarzaroM.VivanL.TargaA.MazzonL.MoriN.GreattiM.GirolamiV.2011Lethal aerial powdering of honey bees with neonicotinoids from fragments of maize seed coatBulletin of Insectology641119126Search in Google Scholar

Naug, D. (2009). Nutritional stress due to habitat loss may explain recent honey colony collapses. Biological Conservation, 142(10), 2369–2372. DOI: 10.1016/j.biocon.2009.04.007NaugD.2009Nutritional stress due to habitat loss may explain recent honey colony collapsesBiological Conservation142102369237210.1016/j.biocon.2009.04.007Open DOISearch in Google Scholar

Official Decision (2018). Neonicotinoid Grubu Aktif Maddelerin Yasaklanması ve Kısıtlanması Hk. (English: As regards the conditions of prohibition and restrict of the active substances of neonicotinoid group). General Directorate of Food and Control, Ministry of Agriculture and Forestry in Republic of Turkey. Retrieved April 17, 2019, from https://bku.tarim.gov.tr/Duyuru/DuyuruDetay/32Official Decision2018Neonicotinoid Grubu Aktif Maddelerin Yasaklanması ve Kısıtlanması Hk(English: As regards the conditions of prohibition and restrict of the active substances of neonicotinoid group). General Directorate of Food and Control, Ministry of Agriculture and Forestry in Republic of Turkey. Retrieved April 17, 2019, from https://bku.tarim.gov.tr/Duyuru/DuyuruDetay/32Search in Google Scholar

OIE (All World Organisation for Animal Health) (2008). Nosemosis of honey bees. Chapter 2.2.4. In Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. (pp. 410–414). Paris: OIE Terrestrial Manual.OIE (All World Organisation for Animal Health)2008Nosemosis of honey beesChapter 2.2.4. In Manual of Diagnostic Tests and Vaccines for Terrestrial Animals.410414ParisOIE Terrestrial ManualSearch in Google Scholar

Pistorius, J., Bischoff, G., Heimbach, U., Stähler, M. (2009). Bee poisoning incidents in Germany in spring 2008 caused by abrasion of active substance from treated seeds during sowing of maize. Julius Kühn Archiv, 423, 118–126.PistoriusJ.BischoffG.HeimbachU.StählerM.2009Bee poisoning incidents in Germany in spring 2008 caused by abrasion of active substance from treated seeds during sowing of maizeJulius Kühn Archiv423118126Search in Google Scholar

Pistorius, J., Wehner, A., Kriszan, M., Bargen, H., Knäbe, S., Klein, O., … Heimbach, U. (2015). Application of predefined doses of neonicotinoid containing dusts in field trials and acute effects on honey bees. Bulletin of Insectology, 68(2), 161–172.PistoriusJ.WehnerA.KriszanM.BargenH.KnäbeS.KleinO.HeimbachU.2015Application of predefined doses of neonicotinoid containing dusts in field trials and acute effects on honey beesBulletin of Insectology682161172Search in Google Scholar

Public report (2011). Bee poisoning incidents in the Pomurje region of Eastern Slovenia in 2011. Based on the public report by the Inspectorate of the Republic Slovenia for Agriculture Forestry and Food. Retrieved April 16, 2019, from www.nationalbeeunit.com/downloadDocument.cfm?id=639Public report2011Bee poisoning incidents in the Pomurje region of Eastern Slovenia in 2011Based on the public report by the Inspectorate of the Republic Slovenia for Agriculture Forestry and Food. Retrieved April 16, 2019, from www.nationalbeeunit.com/downloadDocument.cfm?id=639Search in Google Scholar

Ratnieks, F. L. W., & Carreck, N. L. (2010). Clarity on honey bee collapse? Science, 327(5962), 152–153. DOI: 10.1126/science.1185563RatnieksF. L. W.CarreckN. L.2010Clarity on honey bee collapse?Science327596215215310.1126/science.118556320056879Open DOISearch in Google Scholar

Rortais, A., Arnold, G., Halm, M. P., Touffet-Briens, F. (2005). Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees. Apidologie, 36(1), 71–83. DOI: 10.1051/apido:2004071RortaisA.ArnoldG.HalmM. P.Touffet-BriensF.2005Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of beesApidologie361718310.1051/apido:2004071Open DOISearch in Google Scholar

Sharpe, J. R., & Heyden, L. C. (2009). Honey bee colony collapse disorder is possibly caused by a dietary pyrethrum deficiency. Bioscience Hypotheses, 2(6), 439–440. DOI: 10.1016/j.bihy.2009.01.004SharpeJ. R.HeydenL. C.2009Honey bee colony collapse disorder is possibly caused by a dietary pyrethrum deficiencyBioscience Hypotheses2643944010.1016/j.bihy.2009.01.004Open DOISearch in Google Scholar

Suchail, S., Guez, D., & Belzunces, L. P. (2001). Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environmental Toxicology and Chemistry, 20(11), 2482–2486. DOI: 10.1002/etc.5620201113SuchailS.GuezD.BelzuncesL. P.2001Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis melliferaEnvironmental Toxicology and Chemistry20112482248610.1002/etc.5620201113Open DOISearch in Google Scholar

Tapparo, A., Marton, D., Giorio, C., Zanella, A., Soldà, L., Marzaro, M., … Girolami, V. (2012). Assessment of the environmental exposure of honeybees to particulate matter containing neonicotinoid insecticides coming from corn coated seeds. Environmental Science Technology, 46(5), 2592–9. DOI: 10.1021/es2035152TapparoA.MartonD.GiorioC.ZanellaA.SoldàL.MarzaroM.GirolamiV.2012Assessment of the environmental exposure of honeybees to particulate matter containing neonicotinoid insecticides coming from corn coated seedsEnvironmental Science Technology4652592910.1021/es203515222292570Open DOISearch in Google Scholar

van der Geest, B. (2012). Bee poisoning incidents in the Pomurje region of Eastern Slovenia in 2011. Hazards of pesticides to bees. Julius-Kühn-Archiv, 437, 124. DOI: 10.5073/jka.2012.437.036van der GeestB.2012Bee poisoning incidents in the Pomurje region of Eastern Slovenia in 2011. Hazards of pesticides to beesJulius-Kühn-Archiv43712410.5073/jka.2012.437.036Open DOISearch in Google Scholar

van Dijk, T. (2010). Effects of neonicotinoid pesticide pollution of Dutch surface water on nontarget species abundance [MSc Thesis] Utrecht University.van DijkT.2010Effects of neonicotinoid pesticide pollution of Dutch surface water on nontarget species abundance[MSc Thesis] Utrecht University.Search in Google Scholar

van Engelsdorp, D., Evans, J. D., Saegerman, C., Mullin, C., Haubruge, E., Nguyen, B. K., … Pettis, J. S. (2009). Colony collapse disorder: a descriptive study. PLoS ONE, 4(8), e6481. DOI: 10.1371/journal.pone.0006481van EngelsdorpD.EvansJ. D.SaegermanC.MullinC.HaubrugeE.NguyenB. K.PettisJ. S.2009Colony collapse disorder: a descriptive studyPLoS ONE48e648110.1371/journal.pone.0006481271589419649264Open DOISearch in Google Scholar

Wood, T. J., & Goulson, D. (2017). The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013. Environmental Science and Pollution Research, 24(21), 17285–17325. DOI: 10.1007/s11356-017-9240-xWoodT. J.GoulsonD.2017The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013Environmental Science and Pollution Research2421172851732510.1007/s11356-017-9240-x553382928593544Open DOISearch in Google Scholar

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