三种新烟碱农药对西方蜜蜂生存和生理的联合影响
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摘要
为探究亚致死浓度的3种常用新烟碱农药噻虫嗪、吡虫啉和噻虫胺两两混合对西方蜜蜂生存以及乙酰胆碱酯酶和谷胱甘肽S-转移酶活性的联合影响,本研究通过饲喂管法检测这3种新烟碱农药对西方蜜蜂的经口性急性毒性。用各农药的LD_(10)值作为处理剂量,检测LD_(10)的各农药及其两两混合处理西方蜜蜂后48 h蜜蜂的死亡率,并检测各处理组蜜蜂乙酰胆碱酯酶和谷胱甘肽S-转移酶活性变化。3种农药两两互混后与单一农药相比均能显著增加西方蜜蜂的死亡率(P<0.05);噻虫嗪和吡虫啉以及噻虫嗪和噻虫胺联合用药均对蜜蜂毒性具有协同增效作用(Q>1.15)。所有农药处理组蜜蜂的乙酰胆碱酯酶活性均显著高于对照组(P<0.05),其中噻虫嗪与噻虫胺混合组乙酰胆碱酯酶的活性最高;噻虫嗪和吡虫啉以及噻虫嗪和噻虫胺两两互混后与单一农药处理组相比均能显著增加蜜蜂乙酰胆碱酯酶活性(P<0.05)。除噻虫嗪与噻虫胺互混组对蜜蜂谷胱甘肽S-转移酶活性具有明显的抑制作用(P<0.05),其他农药组谷胱甘肽S-转移酶活性均没有明显变化。新烟碱类农药噻虫嗪和吡虫啉以及噻虫嗪和噻虫胺互混处理组能够协同增加对蜜蜂的毒性,而且农药混合与单一农药处理相比能引起蜜蜂不同的生理变化。本研究利于更深入了解和探究混合农药对蜜蜂健康的影响,并为保护蜜蜂提供一定理论基础。
To investigate combination effects of three common neonicotinoid pesticides thiamethoxam, imidacloprid and clothianidin on the activities of acetycholinesterase(AChE) and glutathione S-transferases(GSTs), and the survival in honey bees(Apis mellifera L.). The acute toxicity of three neonicotinoids pesticides to honey bees was tested by "oral-feeling tube" method; The mortalities, AChE and GSTs activities of honey bees was measure at 48 h after bees were exposed to LD_(10 ) of thiamethoxam, imidacloprid and clothianidin, and binary mixtures of these pesticides. The mortalities were significantly increased by binary mixtures of three pesticides(P<0.05). The synergistic effect of thiamethoxam and imidacloprid, or thiamethoxam and clothianidin could increase the toxicity to bees(Q>1.15). The activities of AChE in pesticide treatment groups were all significantly higher than control(P<0.05). Binary mixtures of thiamethoxam and imidacloprid, or thiamethoxam and clothianidin could significantly increased the activities of AChE(P<0.05). The activities of GSTs were distinctly inhibited by the mixture of thiamethoxam and clothianidin(P<0.05); however, there were no significant differences in the activities of GSTs in other pesticide groups. Combined toxicity was detected from mixtures of thiamethoxam and imidacloprid, or thiamethoxam and clothianidin showed synergistic interaction. Binary mixtures of neonicotinoids showed different physiology changes than single neonicotinoids in honeybees. These results are important for exploring impact of pesticides on the health of honey bees and provide theoretical basis in honey bees protection.
To investigate combination effects of three common neonicotinoid pesticides thiamethoxam, imidacloprid and clothianidin on the activities of acetycholinesterase(AChE) and glutathione S-transferases(GSTs), and the survival in honey bees(Apis mellifera L.). The acute toxicity of three neonicotinoids pesticides to honey bees was tested by "oral-feeling tube" method; The mortalities, AChE and GSTs activities of honey bees was measure at 48 h after bees were exposed to LD_(10 ) of thiamethoxam, imidacloprid and clothianidin, and binary mixtures of these pesticides. The mortalities were significantly increased by binary mixtures of three pesticides(P<0.05). The synergistic effect of thiamethoxam and imidacloprid, or thiamethoxam and clothianidin could increase the toxicity to bees(Q>1.15). The activities of AChE in pesticide treatment groups were all significantly higher than control(P<0.05). Binary mixtures of thiamethoxam and imidacloprid, or thiamethoxam and clothianidin could significantly increased the activities of AChE(P<0.05). The activities of GSTs were distinctly inhibited by the mixture of thiamethoxam and clothianidin(P<0.05); however, there were no significant differences in the activities of GSTs in other pesticide groups. Combined toxicity was detected from mixtures of thiamethoxam and imidacloprid, or thiamethoxam and clothianidin showed synergistic interaction. Binary mixtures of neonicotinoids showed different physiology changes than single neonicotinoids in honeybees. These results are important for exploring impact of pesticides on the health of honey bees and provide theoretical basis in honey bees protection.
引文
Alkassab AT,Kirchner WH.Impacts of chronic sublethal exposure to clothianidin on winterhoneybees [J].Ecotoxicology,2016,25 (5):1000-1010.
Aliouane Y,El Hassani AK,Gary V,et al.Subchronic exposure of honeybees to sublethal doses of pesticides:Effects on behavior [J].Environ.Toxicol.Chem.,2009,28 (1):113-122.
Badiou A,Meled M,Belzunces L.Honeybee (Apis mellifera) acetylcholinesterase-a biomarker to detect deltamethrin exposure [J].Ecotoxicol.Environ.Saf.,2008,69 (2):246-253.
Biddinger DJ,Robertson JL,Mullin C,et al.Comparative toxicities and synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia cornifrons (Radoszkowski) [J].PLoS ONE,2013,8 (9):e72587.
Brandt A,Gorenflo A,Siede R,et al.The neonicotinoids thiacloprid,imidacloprid,and clothianidin affect the immuncomperence of honey bees (Apis mellifera L.) [J].Insect Physiol.,2016,86:40-47.
Brown LA,Ihara M,Buckingham SD,et al.Neonicotinoid insecticides display partial and super agonist actions on native insect nicotinic acetylcholine receptors [J].J.Neurochem.,2006,99 (2):608-615.
Berenbaum MR,Johnson RM.Xenobiotic detoxification pathways in honey bees[J].Curr.Opin.Insect Sci.,2015,10:51-58.
Boily M,Sarrasin B,Deblois C,et al.Acetylcholinesterase in honey bees (Apis mellifera) exposed to neonicotinoids,atrazine and glyphosate:Laboratory and field experiments [J].Environ.Sci.and Pollut.Res.Int.,2013,20 (8):5603-5614.
Bielza P,Quinto V,Contreras J,et al.Resistance to spinosad in the western flower thrips,Frankliniella occidentalis (Pergande),in greenhouses of southeastern Spain [J].Pest Manag.Sci.,2007,63 (7):682-687.
Claudianos C,Ranson H,Johnson RM,et al.A deficit of detoxification enzymes:Pesticide sensitivity and environmental response in the honeybee [J].Insect Mol.Biol.,2006,15 (5):615-636.
Cresswell JE.A meta-analysis of experiments testing the effects of a neonicotinoid insecticide(imdacloprid) on honey bees [J].Ecotoxicology,2011,20 (1):149-157.
Casida JE,Durkin KA.Neuroactive insecticides:Targets,selectivity,resistance,and secondary effects [J].Annu.Rev.Entomol.,2013,58 (1):99-117
Cai QN,Zhang QW,Chen M.Contribution of indole alkaloids to Sitobion avenae (F.) resistance in wheat [J].Appl.Entomol.,2004,128 (8):517-521.
Fischer J,Muller T,Spatz AK,et al.Neonicotinoids interfere with specific components of navigation in honeybees [J].PLoS ONE,2014,9 (3):e91364.
Goulson D,Nicholls E,Botias C,et al.Bee decline driven by combined stress from parasites,pesticides,and lack of flowers [J].Science,2015,347 (6229):165-174.
Henry M,Beguin M,Requier F,et al.A common pesticide decreases foraging success and survival in honey bees [J].Science,2012,336 (6079):348-50.
Jia H,Sun R,Shi W,et al.Characterization of a mitochondrial manganese superoxide dismutase gene from Apis cerana cerana and its role in oxidative stress [J].J.Insect Physiol.,2014,60 (1):68-79.
Johnson RM.Honey bee toxicology [J].Annu.Rev.Entomol.,2015,60 (1):415-434.
Ji SM,Cheng CY,Yuan CW,et al.Acute toxicity and risk assessment of seven neonicotiniod insecticides on honeybee (Apis mellifera L.) [J].Agrochemicals,2015,54 (4):282-285.[季守民,程传英,袁传卫,等.7种新烟碱类杀虫剂对意大利蜜蜂的急性毒性及风险评价[J].农药,2015,54 (4):282-285]
Jin ZJ.Addition in drug combination [J].Acta Pharmacologica Sinica,1980,1 (2):70-76.[金正均.合并用药中的相加[J].中国药理学报,1980,1 (2):70-76]
Kim BM,El-Aty AA,Hwang TE,et al.Development of an acetylcholinesterase-based detection kit for the determination of organophosphorus and carbamate pesticideresidues in agricultural samples [J].Bull.Korean Chemical Soc.,2007,28 (6):929-935.
Mengoni GC,Farina WM.Effects of sublethal doses of imidacloprid on young adult honeybee behaviour [J].PLoS ONE,2015,10 (10):e0140814.
Millar NS,Denholm I.Nicotinic acetylcholine receptors:Targets for commercially important insecticides [J].Invert.Neurosci.,2007,7 (1):53-66.
Ma WH,Shen JS,Guo Y,et al.Effects of Zaohua disease on activities of digestive enzymes and detoxification enzymes in Apis mellifera ligustica [J].Acta Entomol.Sin.,2011,54 (9):1076-1081.
Nauen R,Ebbinghaus-Kintscher U,Salgado VL,et al.Thiamethoxam is a neonicotinoid precursor converted to clothianidin in insects and plants [J].Pesticide Biochem.Physiol.,2003,76 (2):55-69.
Nielsen SA,Brodsgaard CJ,Hansen H.Effects on detoxification enzymes in diferent life stages of honeybees (Apis mellifera L.,Hymenoptera:Apidae) treated with a synthetic pyrethroid (Flumethrin) [J].Altern.Lab.Anim.,2000,28 (3):437-443.
Peng YC,Yang EC.Sublethal dosage of imidacloprid reduces the microglomerular density of honeybee mushroom bodies [J].Sci.Rep.,2016,6:19298.
Spurgeon D,Hesketh H,Lahive E,et al.Chronic oral lethal and sublethal toxicities of different binary mixtures of pesticides and contaminants in bees (Apis mellifera,Osmia bicornis and Bombus terrestris) [J].Efsa Supporting Publications,2016,13 (9).
Thompson HM,Fryday SL,Harkin S,et al.Potential impacts of synergism in honeybees (Apis mellifera) of exposure to neonicotinoids and sprayed fungicides in crops [J].Apidologie,2014,45 (5):545-553.
Tison L,Hahn ML,Holtz S,et al.Honeybees' behavior is impaired by chronic exposure to the neonicotinoid thiacloprid in the field [J].Environ.Sci.Technol.,2016,50 (13):7218-7227.
Tsvetkov N,Samson-Robert O,Sood K,et al.Chronic exposure to neonicotinoids reduces honey bee health near corn crops [J].Science,2017,356 (6345):1395-1397.
Zhu YC,Yao JX,Adamczyk J,et al.Synergistic toxicity and physiological impact of imidacloprid alone and binary mixtures with seven representative pesticides on honey bee (Apis mellifera) [J].PLoS ONE,2017,12 (5):e0176837.
Aliouane Y,El Hassani AK,Gary V,et al.Subchronic exposure of honeybees to sublethal doses of pesticides:Effects on behavior [J].Environ.Toxicol.Chem.,2009,28 (1):113-122.
Badiou A,Meled M,Belzunces L.Honeybee (Apis mellifera) acetylcholinesterase-a biomarker to detect deltamethrin exposure [J].Ecotoxicol.Environ.Saf.,2008,69 (2):246-253.
Biddinger DJ,Robertson JL,Mullin C,et al.Comparative toxicities and synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia cornifrons (Radoszkowski) [J].PLoS ONE,2013,8 (9):e72587.
Brandt A,Gorenflo A,Siede R,et al.The neonicotinoids thiacloprid,imidacloprid,and clothianidin affect the immuncomperence of honey bees (Apis mellifera L.) [J].Insect Physiol.,2016,86:40-47.
Brown LA,Ihara M,Buckingham SD,et al.Neonicotinoid insecticides display partial and super agonist actions on native insect nicotinic acetylcholine receptors [J].J.Neurochem.,2006,99 (2):608-615.
Berenbaum MR,Johnson RM.Xenobiotic detoxification pathways in honey bees[J].Curr.Opin.Insect Sci.,2015,10:51-58.
Boily M,Sarrasin B,Deblois C,et al.Acetylcholinesterase in honey bees (Apis mellifera) exposed to neonicotinoids,atrazine and glyphosate:Laboratory and field experiments [J].Environ.Sci.and Pollut.Res.Int.,2013,20 (8):5603-5614.
Bielza P,Quinto V,Contreras J,et al.Resistance to spinosad in the western flower thrips,Frankliniella occidentalis (Pergande),in greenhouses of southeastern Spain [J].Pest Manag.Sci.,2007,63 (7):682-687.
Claudianos C,Ranson H,Johnson RM,et al.A deficit of detoxification enzymes:Pesticide sensitivity and environmental response in the honeybee [J].Insect Mol.Biol.,2006,15 (5):615-636.
Cresswell JE.A meta-analysis of experiments testing the effects of a neonicotinoid insecticide(imdacloprid) on honey bees [J].Ecotoxicology,2011,20 (1):149-157.
Casida JE,Durkin KA.Neuroactive insecticides:Targets,selectivity,resistance,and secondary effects [J].Annu.Rev.Entomol.,2013,58 (1):99-117
Cai QN,Zhang QW,Chen M.Contribution of indole alkaloids to Sitobion avenae (F.) resistance in wheat [J].Appl.Entomol.,2004,128 (8):517-521.
Fischer J,Muller T,Spatz AK,et al.Neonicotinoids interfere with specific components of navigation in honeybees [J].PLoS ONE,2014,9 (3):e91364.
Goulson D,Nicholls E,Botias C,et al.Bee decline driven by combined stress from parasites,pesticides,and lack of flowers [J].Science,2015,347 (6229):165-174.
Henry M,Beguin M,Requier F,et al.A common pesticide decreases foraging success and survival in honey bees [J].Science,2012,336 (6079):348-50.
Jia H,Sun R,Shi W,et al.Characterization of a mitochondrial manganese superoxide dismutase gene from Apis cerana cerana and its role in oxidative stress [J].J.Insect Physiol.,2014,60 (1):68-79.
Johnson RM.Honey bee toxicology [J].Annu.Rev.Entomol.,2015,60 (1):415-434.
Ji SM,Cheng CY,Yuan CW,et al.Acute toxicity and risk assessment of seven neonicotiniod insecticides on honeybee (Apis mellifera L.) [J].Agrochemicals,2015,54 (4):282-285.[季守民,程传英,袁传卫,等.7种新烟碱类杀虫剂对意大利蜜蜂的急性毒性及风险评价[J].农药,2015,54 (4):282-285]
Jin ZJ.Addition in drug combination [J].Acta Pharmacologica Sinica,1980,1 (2):70-76.[金正均.合并用药中的相加[J].中国药理学报,1980,1 (2):70-76]
Kim BM,El-Aty AA,Hwang TE,et al.Development of an acetylcholinesterase-based detection kit for the determination of organophosphorus and carbamate pesticideresidues in agricultural samples [J].Bull.Korean Chemical Soc.,2007,28 (6):929-935.
Mengoni GC,Farina WM.Effects of sublethal doses of imidacloprid on young adult honeybee behaviour [J].PLoS ONE,2015,10 (10):e0140814.
Millar NS,Denholm I.Nicotinic acetylcholine receptors:Targets for commercially important insecticides [J].Invert.Neurosci.,2007,7 (1):53-66.
Ma WH,Shen JS,Guo Y,et al.Effects of Zaohua disease on activities of digestive enzymes and detoxification enzymes in Apis mellifera ligustica [J].Acta Entomol.Sin.,2011,54 (9):1076-1081.
Nauen R,Ebbinghaus-Kintscher U,Salgado VL,et al.Thiamethoxam is a neonicotinoid precursor converted to clothianidin in insects and plants [J].Pesticide Biochem.Physiol.,2003,76 (2):55-69.
Nielsen SA,Brodsgaard CJ,Hansen H.Effects on detoxification enzymes in diferent life stages of honeybees (Apis mellifera L.,Hymenoptera:Apidae) treated with a synthetic pyrethroid (Flumethrin) [J].Altern.Lab.Anim.,2000,28 (3):437-443.
Peng YC,Yang EC.Sublethal dosage of imidacloprid reduces the microglomerular density of honeybee mushroom bodies [J].Sci.Rep.,2016,6:19298.
Spurgeon D,Hesketh H,Lahive E,et al.Chronic oral lethal and sublethal toxicities of different binary mixtures of pesticides and contaminants in bees (Apis mellifera,Osmia bicornis and Bombus terrestris) [J].Efsa Supporting Publications,2016,13 (9).
Thompson HM,Fryday SL,Harkin S,et al.Potential impacts of synergism in honeybees (Apis mellifera) of exposure to neonicotinoids and sprayed fungicides in crops [J].Apidologie,2014,45 (5):545-553.
Tison L,Hahn ML,Holtz S,et al.Honeybees' behavior is impaired by chronic exposure to the neonicotinoid thiacloprid in the field [J].Environ.Sci.Technol.,2016,50 (13):7218-7227.
Tsvetkov N,Samson-Robert O,Sood K,et al.Chronic exposure to neonicotinoids reduces honey bee health near corn crops [J].Science,2017,356 (6345):1395-1397.
Zhu YC,Yao JX,Adamczyk J,et al.Synergistic toxicity and physiological impact of imidacloprid alone and binary mixtures with seven representative pesticides on honey bee (Apis mellifera) [J].PLoS ONE,2017,12 (5):e0176837.