Exposure to low-level metalaxyl impacts the cardiac development and function of zebrafish embryos
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摘要
Metalaxyl is an anilide pesticide that is widely used to control plant diseases caused by Peronosporales species. In order to study the toxic effects, zebrafish embryos were exposed to metalaxyl at nominal concentrations of 5, 50 and 500 ng/L for 72 hr, and the cardiac development and functioning of larvae were observed. The results showed that metalaxyl exposure resulted in increased rates of pericardial edema, heart hemorrhage and cardiac malformation. The distance between the sinus venosus and bulbus arteriosus, stroke volume, cardiac output and heart rate were significantly increased in larvae exposed to 50 and 500 ng/L metalaxyl compared to solvent control larvae. Significant upregulation in the transcription of tbx5, gata4 and myh6 was observed in the 50 and 500 ng/L treatments, and that of nkx2.5 and myl7 was observed in the 5, 50 and 500 ng/L groups. These disturbances may be related to cardiac developmental and functional defects in the larvae. The activity of Na~+/K~+-ATPase and Ca~(2+)-ATPase was significantly increased in zebrafish embryos exposed to 500 ng/L metalaxyl, and the mRNA levels of genes related to ATPase(atp2a11, atp1b2b,and atp1a3b)(in the 50 and 500 ng/L groups) and calcium channels(cacna1ab)(in the 500 ng/L group) were significantly downregulated; these changes might be associated with heart arrhythmia and functional failure.
Metalaxyl is an anilide pesticide that is widely used to control plant diseases caused by Peronosporales species. In order to study the toxic effects, zebrafish embryos were exposed to metalaxyl at nominal concentrations of 5, 50 and 500 ng/L for 72 hr, and the cardiac development and functioning of larvae were observed. The results showed that metalaxyl exposure resulted in increased rates of pericardial edema, heart hemorrhage and cardiac malformation. The distance between the sinus venosus and bulbus arteriosus, stroke volume, cardiac output and heart rate were significantly increased in larvae exposed to 50 and 500 ng/L metalaxyl compared to solvent control larvae. Significant upregulation in the transcription of tbx5, gata4 and myh6 was observed in the 50 and 500 ng/L treatments, and that of nkx2.5 and myl7 was observed in the 5, 50 and 500 ng/L groups. These disturbances may be related to cardiac developmental and functional defects in the larvae. The activity of Na~+/K~+-ATPase and Ca~(2+)-ATPase was significantly increased in zebrafish embryos exposed to 500 ng/L metalaxyl, and the mRNA levels of genes related to ATPase(atp2a11, atp1b2b,and atp1a3b)(in the 50 and 500 ng/L groups) and calcium channels(cacna1ab)(in the 500 ng/L group) were significantly downregulated; these changes might be associated with heart arrhythmia and functional failure.
Metalaxyl is an anilide pesticide that is widely used to control plant diseases caused by Peronosporales species. In order to study the toxic effects, zebrafish embryos were exposed to metalaxyl at nominal concentrations of 5, 50 and 500 ng/L for 72 hr, and the cardiac development and functioning of larvae were observed. The results showed that metalaxyl exposure resulted in increased rates of pericardial edema, heart hemorrhage and cardiac malformation. The distance between the sinus venosus and bulbus arteriosus, stroke volume, cardiac output and heart rate were significantly increased in larvae exposed to 50 and 500 ng/L metalaxyl compared to solvent control larvae. Significant upregulation in the transcription of tbx5, gata4 and myh6 was observed in the 50 and 500 ng/L treatments, and that of nkx2.5 and myl7 was observed in the 5, 50 and 500 ng/L groups. These disturbances may be related to cardiac developmental and functional defects in the larvae. The activity of Na~+/K~+-ATPase and Ca~(2+)-ATPase was significantly increased in zebrafish embryos exposed to 500 ng/L metalaxyl, and the mRNA levels of genes related to ATPase(atp2a11, atp1b2b,and atp1a3b)(in the 50 and 500 ng/L groups) and calcium channels(cacna1ab)(in the 500 ng/L group) were significantly downregulated; these changes might be associated with heart arrhythmia and functional failure.
引文
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Balci,M.M.,Akdemir,R.,2011.nkx2.5 mutations and congenital heart disease:is it a marker of cardiac anomalies?Int.J.Cardiol.147,44-45.
Barth,A.S.,Tomaselli,G.F.,2009.Cardiac metabolism and arrhythmias.Circ-Arrhythmia Elec.2,327-335.
Battaglin,W.A.,Sandstrom,M.W.,Kuivila,K.M.,Kolpin,D.W.,Meyer,M.T.,2011.Occurrence of azoxystrobin,propiconazole,and selected other fungicides in US streams,2005-2006.Water Air Soil Pollut.218,307-322.
Chen,Z.Y.,Huang,W.,Dahme,T.,Rottbauer,W.,Ackerman,M.J.,Xu,X.L.,2008.Depletion of zebrafish essential and regulatory myosin light chains reduces cardiac function through distinct mechanisms.Cardiovasc.Res.79,97-108.
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Du,G.,Xiao,Y.,Yang,H.R.,Wang,L.,Song,Y.L.,Wang,Y.T.,2012.Rapid determination of pesticide residues in herbs using selective pressurized liquid extraction and fast gas chromatography coupled with mass spectrometry.J.Sep.Sci.35,1922-1932.
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Fernández,I.,Gavaia,P.J.,Laizé,V.,Cancela,M.L.,2018.Fish as a model to assess chemical toxicity in bone.Aquat.Toxicol.194,208-226.
Hayes,T.B.,Stuart,A.A.,Mendoza,M.,Collins,A.,Noriega,N.,Vonk,A.,et al.,2006.Characterization of atrazine-induced gonadal malformations in African clawed frogs(Xenopus laevis)and comparisons with effects of an androgen antagonist(cyproterone acetate)and exogenous estrogen(17β-estradiol):support for the demasculinization/feminization hypothesis.Environ.Health Perspect.114(Suppl.1),134-141.
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Holtzinger,A.,Evans,T.,2005.Gata4 regulates the formation of multiple organs.Development 132,4005-4014.
Horie,Y.,Yamagishi,T.,Takahashi,H.,Shintaku,Y.,Iguchi,T.,Tatarazako,N.,2017.Assessment of the lethal and sublethal effects of 20 environmental chemicals in zebrafish embryos and larvae by using OECD TG 212.J.Appl.Toxicol.37,1245-1253.
Houbraken,M.,Habimana,V.,Senaeve,D.,López-Dávila,E.,Spanoghe,P.,2017.Multi-residue determination and ecological risk assessment of pesticides in the lakes of Rwanda.Sci.Total Environ.576,888-894.
Huang,L.X.,Wang,C.G.,Zhang,Y.Y.,Jian,L.,Zhong,Y.F.,Zhou,Y.L.,et al.,2012.Benzo[a]pyrene exposure influences the cardiac development and the expression of cardiovascular relative genes in zebrafish(Danio rerio)embryos.Chemosphere.87,369-375.
Incardona,J.P.,2017.Molecular mechanisms of crude oil developmental toxicity in fish.Arch.Environ.Contam.Toxicol.73,19-32.
Incardona,J.P.,Carls,M.G.,Day,H.L.,Sloan,C.A.,Bolton,J.L.,Collier,T.K.,et al.,2009.Cardiac arrhythmia is the primary response of embryonic pacific herring(Clupea pallasi)exposed to crude oil during weathering.Environ.Sci.Technol.43,201-207.
Jin,Y.,Liu,Z.,Peng,T.,Fu,Z.,2015.The toxicity of chlorpyrifos on the early life stage of zebrafish:a survey on the endpoints at development,locomotor behavior,oxidative stress and immunotoxicity.Fish Shellfish Immun.43,405-414.
Kathiriya,I.S.,Barnes,R.,Schluterman,M.K.,King,I.N.,Butler,C.A.,Rothrock,C.R.,et al.,2003.Gata4 mutations cause human congenital heart defects and reveal an interaction with Tbx5.Nature.424,443-447.
Kodde,I.F.,Van der Stok,J.,Smolenski,R.T.,Jong,J.W.,2007.Metabolic and genetic regulation of cardiac energy substrate preference.Comp.Biochem.Physiol.A.146,26-39.
Li,K.,Wu,J.Q.,Jiang,L.L.,Shen,L.Z.,Li,J.Y.,He,Z.H.,et al.,2017.Developmental toxicity of 2,4-dichlorophenoxyacetic acid in zebrafish embryos.Chemosphere 171,40-48.
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Liu,J.,Stainier,D.Y.,2012.Zebrafish in the study of early cardiac development.Circ.Res.110,870-874.
Liu,H.C.,Chu,T.Y.,Chen,L.L.,Gui,W.J.,Zhu,G.L.,2017.The cardiovascular toxicity of triadimefon in early life stage of zebrafish and potential implications to human health.Environ.Pollut.231,1093-1103.
Maharajan,K.,Muthulakshmi,S.,Nataraj,B.,Ramesh,M.,Kadirvelu,K.,2018.Toxicity assessment of pyriproxyfen in vertebrate model zebrafish embryos(Danio rerio):a multi biomarker study.Aquat.Toxicol.196,132-145.
Malhat,F.M.,2017.Persistence of metalaxyl residues on tomato fruit using high performance liquid chromatography and QuEChERS methodology.Arab.J.Chem.10,S765-S768.
Maves,L.,Tyler,A.,Moens,C.B.,Tapscott,S.J.,2009.Pbx acts with Hand2 in early myocardial differentiation.Dev.Biol.333,409-418.
Meite,F.,Alvarez-Zaldívar,P.,Crochet,A.,Wiegert,C.,Payraudeau,S.,Imfeld,G.,2018.Impact of rainfall patterns and frequency on the export of pesticides and heavy-metals from agricultural soils.Sci.Total Environ.616-617,500-509.
Moeder,M.,Carranza-Diaz,O.,López-Angulo,G.,Vega-Avi?a,R.,Chávez-Durán,F.A.,Jomaa,S.,et al.,2017.Potential of vegetated ditches to manage organic pollutants derived from agricultural runoff and domestic sewage:a case study in Sinaloa(Mexico).Sci.Total Environ.598,1106-1115.
Moskowitz,I.P.,Pizard,A.,Patel,V.V.,Bruneau,B.G.,Kim,J.B.,Kupershmidt,S.,et al.,2004.The T-box transcription factor Tbx5is required for the patterning and maturation of the murine cardiac conduction system.Development 131,4107-4116.
Pandey,M.R.,Guo,H.,2014.Evaluation of cytotoxicity,genotoxicity and embryotoxicity of insecticide propoxur using flounder gill(FG)cells and zebrafish embryos.Toxicol.in Vitro28,340-353.
Pfaffl,M.W.,Horgan,G.W.,Dempfle,L.,2002.Relative expression software tool(REST?)for group-wise comparison and statistical analysis of relative expression results in real-time PCR.Nucleic Acids Res.30(9),e36.
Phopin,K.,Wanwimolruk,S.,Prachayasittikul,V.,2017.Food safety in Thailand.3:Pesticide residues detected in mangosteen(Garcinia mangostana L.),queen of fruits.J.Sci.Food Agric.97,832-840.
Pott,A.,Rottbauer,W.,Just,S.,2014.Functional genomics in zebrafish as a tool to identify novel antiarrhythmic targets.Curr.Med.Chem.21,1320-1329.
Reiter,J.F.,Verkade,H.,Stainier,D.Y.R.,2001.Bmp2b and Oep promote early myocardial differentiation through their regulation of gata5.Dev.Biol.234,330-338.
Richards,J.G.,Semple,J.W.,Bystriansky,J.S.,Schulte,P.M.,2003.Na+/K+-ATPaseα-isoform switching in gills of rainbow trout(Oncorhynchus mykiss)during salinity transfer.J.Exp.Biol.206,4475-4486.
Sakr,S.,Lamfon,H.,Essawy,A.,2011.Ginger(Zingiber officinale)extract ameliorates metalaxyl fungicide induced nephrotoxicity in albino mice.Afr.J.Pharm.Pharmacol 5,104-112.
Schock,E.N.,Ford,W.C.,Midgley,K.J.,Fader,J.G.,Giavasis,M.N.,McWhorter,M.L.,2012.The effects of carbaryl on the development of zebrafish(Danio rerio)embryos.Zebrafish 9,169-178.
Struger,J.,Grabuski,J.,Cagampan,S.,Sverko,E.,Marvin,C.,2016.Occurrence and distribution of carbamate pesticides and metalaxyl in southern Ontario surface waters 2007-2010.Bull.Environ.Contam.Toxicol.96,423-431.
Takeuchi,J.K.,Bruneau,B.G.,2009.Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors.Nature459,708-711.
Targoff,K.L.,Colombo,S.,George,V.,Schell,T.,Kim,S.H.,SolnicaKrezel,L.,et al.,2013.Nkx genes are essential for maintenance of ventricular identity.Development 140,4203-4213.
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USEPA(United States Environmental Protection Agency),1995.Environmental Effects Database(EEDB);Office of Pesticide Programs.Environmental Fate and Effects Division,Washington,DC.
V?lim?ki,M.J.,T?lli,M.A.,Kinnunen,S.M.,Aro,J.,Serpi,R.,Pohjolainen,L.,et al.,2017.Discovery of small molecules targeting the synergy of cardiac transcription factors GATA4and NKX2-5.J.Med.Chem.60,7781-7798.
Wan,M.T.,Kuo,J.N.,Mcpherson,B.,Pasternak,J.,2006.Agricultural pesticide residues in farm ditches of the lower Fraser valley,British Columbia,Canada.J.Environ.Sci.Health B 41(5),647-669.
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Bagatto,B.,Francl,J.,Liu,B.,Liu,Q.,2006.Cadherin2(N-cadherin)plays an essential role in zebrafish cardiovascular development.BMC Dev.Biol.6,23.
Bakkers,J.,2011.Zebrafish as a model to study cardiac development and human cardiac disease.Cardiovasc.Res.91,279-288.
Balci,M.M.,Akdemir,R.,2011.nkx2.5 mutations and congenital heart disease:is it a marker of cardiac anomalies?Int.J.Cardiol.147,44-45.
Barth,A.S.,Tomaselli,G.F.,2009.Cardiac metabolism and arrhythmias.Circ-Arrhythmia Elec.2,327-335.
Battaglin,W.A.,Sandstrom,M.W.,Kuivila,K.M.,Kolpin,D.W.,Meyer,M.T.,2011.Occurrence of azoxystrobin,propiconazole,and selected other fungicides in US streams,2005-2006.Water Air Soil Pollut.218,307-322.
Chen,Z.Y.,Huang,W.,Dahme,T.,Rottbauer,W.,Ackerman,M.J.,Xu,X.L.,2008.Depletion of zebrafish essential and regulatory myosin light chains reduces cardiac function through distinct mechanisms.Cardiovasc.Res.79,97-108.
Demsia,G.,Vlastos,D.,Goumenou,M.,Matthopoulos,D.P.,2007.Assessment of the genotoxicity of imidacloprid and metalaxyl in cultured human lymphocytes and rat bone-marrow.Mutat.Res.634,32-39.
Du,G.,Xiao,Y.,Yang,H.R.,Wang,L.,Song,Y.L.,Wang,Y.T.,2012.Rapid determination of pesticide residues in herbs using selective pressurized liquid extraction and fast gas chromatography coupled with mass spectrometry.J.Sep.Sci.35,1922-1932.
Ebert,A.M.,Hume,G.L.,Warren,K.S.,Cook,N.P.,Burns,C.G.,Mohideen,M.A.,et al.,2005.Calcium extrusion is critical for cardiac morphogenesis and rhythm in embryonic zebrafish hearts.Proc.Natl.Acad.Sci.U.S.A.102,17705-17710.
Fernández,I.,Gavaia,P.J.,Laizé,V.,Cancela,M.L.,2018.Fish as a model to assess chemical toxicity in bone.Aquat.Toxicol.194,208-226.
Hayes,T.B.,Stuart,A.A.,Mendoza,M.,Collins,A.,Noriega,N.,Vonk,A.,et al.,2006.Characterization of atrazine-induced gonadal malformations in African clawed frogs(Xenopus laevis)and comparisons with effects of an androgen antagonist(cyproterone acetate)and exogenous estrogen(17β-estradiol):support for the demasculinization/feminization hypothesis.Environ.Health Perspect.114(Suppl.1),134-141.
He,J.H.,Gao,J.M.,Huang,C.J.,Li,C.Q.,2014.Zebrafish models for assessing developmental and reproductive toxicity.Neurotoxicol.Teratol.42,35-42.
Hiroi,Y.,Kudoh,S.,Monzen,K.,Ikeda,Y.,Yazaki,Y.,Nagai,R.,et al.,2001.Tbx5 associates with Nkx2.5 and synergistically promotes cardiomyocyte differentiation.Nat.Genet.28(3),276-280.
Holtzinger,A.,Evans,T.,2005.Gata4 regulates the formation of multiple organs.Development 132,4005-4014.
Horie,Y.,Yamagishi,T.,Takahashi,H.,Shintaku,Y.,Iguchi,T.,Tatarazako,N.,2017.Assessment of the lethal and sublethal effects of 20 environmental chemicals in zebrafish embryos and larvae by using OECD TG 212.J.Appl.Toxicol.37,1245-1253.
Houbraken,M.,Habimana,V.,Senaeve,D.,López-Dávila,E.,Spanoghe,P.,2017.Multi-residue determination and ecological risk assessment of pesticides in the lakes of Rwanda.Sci.Total Environ.576,888-894.
Huang,L.X.,Wang,C.G.,Zhang,Y.Y.,Jian,L.,Zhong,Y.F.,Zhou,Y.L.,et al.,2012.Benzo[a]pyrene exposure influences the cardiac development and the expression of cardiovascular relative genes in zebrafish(Danio rerio)embryos.Chemosphere.87,369-375.
Incardona,J.P.,2017.Molecular mechanisms of crude oil developmental toxicity in fish.Arch.Environ.Contam.Toxicol.73,19-32.
Incardona,J.P.,Carls,M.G.,Day,H.L.,Sloan,C.A.,Bolton,J.L.,Collier,T.K.,et al.,2009.Cardiac arrhythmia is the primary response of embryonic pacific herring(Clupea pallasi)exposed to crude oil during weathering.Environ.Sci.Technol.43,201-207.
Jin,Y.,Liu,Z.,Peng,T.,Fu,Z.,2015.The toxicity of chlorpyrifos on the early life stage of zebrafish:a survey on the endpoints at development,locomotor behavior,oxidative stress and immunotoxicity.Fish Shellfish Immun.43,405-414.
Kathiriya,I.S.,Barnes,R.,Schluterman,M.K.,King,I.N.,Butler,C.A.,Rothrock,C.R.,et al.,2003.Gata4 mutations cause human congenital heart defects and reveal an interaction with Tbx5.Nature.424,443-447.
Kodde,I.F.,Van der Stok,J.,Smolenski,R.T.,Jong,J.W.,2007.Metabolic and genetic regulation of cardiac energy substrate preference.Comp.Biochem.Physiol.A.146,26-39.
Li,K.,Wu,J.Q.,Jiang,L.L.,Shen,L.Z.,Li,J.Y.,He,Z.H.,et al.,2017.Developmental toxicity of 2,4-dichlorophenoxyacetic acid in zebrafish embryos.Chemosphere 171,40-48.
Lin,C.C.,Hui,M.N.,Cheng,S.H.,2007.Toxicity and cardiac effects of carbaryl in early developing zebrafish(Danio rerio)embryos.Toxicol.Appl.Pharmacol.222,159-168.
Liu,J.,Stainier,D.Y.,2012.Zebrafish in the study of early cardiac development.Circ.Res.110,870-874.
Liu,H.C.,Chu,T.Y.,Chen,L.L.,Gui,W.J.,Zhu,G.L.,2017.The cardiovascular toxicity of triadimefon in early life stage of zebrafish and potential implications to human health.Environ.Pollut.231,1093-1103.
Maharajan,K.,Muthulakshmi,S.,Nataraj,B.,Ramesh,M.,Kadirvelu,K.,2018.Toxicity assessment of pyriproxyfen in vertebrate model zebrafish embryos(Danio rerio):a multi biomarker study.Aquat.Toxicol.196,132-145.
Malhat,F.M.,2017.Persistence of metalaxyl residues on tomato fruit using high performance liquid chromatography and QuEChERS methodology.Arab.J.Chem.10,S765-S768.
Maves,L.,Tyler,A.,Moens,C.B.,Tapscott,S.J.,2009.Pbx acts with Hand2 in early myocardial differentiation.Dev.Biol.333,409-418.
Meite,F.,Alvarez-Zaldívar,P.,Crochet,A.,Wiegert,C.,Payraudeau,S.,Imfeld,G.,2018.Impact of rainfall patterns and frequency on the export of pesticides and heavy-metals from agricultural soils.Sci.Total Environ.616-617,500-509.
Moeder,M.,Carranza-Diaz,O.,López-Angulo,G.,Vega-Avi?a,R.,Chávez-Durán,F.A.,Jomaa,S.,et al.,2017.Potential of vegetated ditches to manage organic pollutants derived from agricultural runoff and domestic sewage:a case study in Sinaloa(Mexico).Sci.Total Environ.598,1106-1115.
Moskowitz,I.P.,Pizard,A.,Patel,V.V.,Bruneau,B.G.,Kim,J.B.,Kupershmidt,S.,et al.,2004.The T-box transcription factor Tbx5is required for the patterning and maturation of the murine cardiac conduction system.Development 131,4107-4116.
Pandey,M.R.,Guo,H.,2014.Evaluation of cytotoxicity,genotoxicity and embryotoxicity of insecticide propoxur using flounder gill(FG)cells and zebrafish embryos.Toxicol.in Vitro28,340-353.
Pfaffl,M.W.,Horgan,G.W.,Dempfle,L.,2002.Relative expression software tool(REST?)for group-wise comparison and statistical analysis of relative expression results in real-time PCR.Nucleic Acids Res.30(9),e36.
Phopin,K.,Wanwimolruk,S.,Prachayasittikul,V.,2017.Food safety in Thailand.3:Pesticide residues detected in mangosteen(Garcinia mangostana L.),queen of fruits.J.Sci.Food Agric.97,832-840.
Pott,A.,Rottbauer,W.,Just,S.,2014.Functional genomics in zebrafish as a tool to identify novel antiarrhythmic targets.Curr.Med.Chem.21,1320-1329.
Reiter,J.F.,Verkade,H.,Stainier,D.Y.R.,2001.Bmp2b and Oep promote early myocardial differentiation through their regulation of gata5.Dev.Biol.234,330-338.
Richards,J.G.,Semple,J.W.,Bystriansky,J.S.,Schulte,P.M.,2003.Na+/K+-ATPaseα-isoform switching in gills of rainbow trout(Oncorhynchus mykiss)during salinity transfer.J.Exp.Biol.206,4475-4486.
Sakr,S.,Lamfon,H.,Essawy,A.,2011.Ginger(Zingiber officinale)extract ameliorates metalaxyl fungicide induced nephrotoxicity in albino mice.Afr.J.Pharm.Pharmacol 5,104-112.
Schock,E.N.,Ford,W.C.,Midgley,K.J.,Fader,J.G.,Giavasis,M.N.,McWhorter,M.L.,2012.The effects of carbaryl on the development of zebrafish(Danio rerio)embryos.Zebrafish 9,169-178.
Struger,J.,Grabuski,J.,Cagampan,S.,Sverko,E.,Marvin,C.,2016.Occurrence and distribution of carbamate pesticides and metalaxyl in southern Ontario surface waters 2007-2010.Bull.Environ.Contam.Toxicol.96,423-431.
Takeuchi,J.K.,Bruneau,B.G.,2009.Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors.Nature459,708-711.
Targoff,K.L.,Colombo,S.,George,V.,Schell,T.,Kim,S.H.,SolnicaKrezel,L.,et al.,2013.Nkx genes are essential for maintenance of ventricular identity.Development 140,4203-4213.
Tomlin,C.,2006.The Pesticide Manual.14th Ed.British Crop Protection Council,Hampshire,UK.
USEPA(United States Environmental Protection Agency),1995.Environmental Effects Database(EEDB);Office of Pesticide Programs.Environmental Fate and Effects Division,Washington,DC.
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