草地贪夜蛾的天敌资源及其生物防治中的应用
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摘要
草地贪夜蛾Spodoptera frugiperda (Smith) (FAW)是一种能取食80多种作物、成虫每晚能迁飞100多公里的多食性、迁飞性害虫,自从2018年底入侵我国以来,在我国快速向北扩散,到目前已经在我国18省市区发生,将严重影响我国玉米等粮食安全和农民的收入,及时研发应急防控技术和今后的可持续控制技术已迫在眉睫。根据草地贪夜蛾在美洲原产地的生物学特性及在非洲的控制实践,我们总结了草地贪夜蛾的天敌昆虫(寄生性和捕食性昆虫)和昆虫病原微生物(病毒、细菌、真菌和线虫)种类、主要天敌类群的生物学、天敌昆虫的大量繁殖、昆虫病原微生物的规模化生产、淹没释放应用、生态调控及生物防治的情况,并讨论了我国草地贪夜蛾生物防治的可行性和前景。
The fall armyworm, Spodoptera frugiperda(Smith)(FAW), is an insect pest that feeds on more than 80 crop species with the adult moth able to move over 100 km per night. FAW was first detected in Yunnan, southwest part of China in early 2019, and rapidly spread to 18 provinces within China by May this year, which seriously threatens the food and income security of millions of farmers. The development of emergency prevention and control technology at present and sustainable management technology in the near future are extremely urgent. Based on the studies of the pest's biology in the Americas and the experiences of management for this pest in Africa, we summary the knowledge about the species of the natural enemies(biological control agents), including entomophagous insects(parasitoids and predators) and entomopathogens(viruses,bacteria, fungi and nematodes), the biology and characters of the main group of natural enemies, the mass rearing of entomophagous insects, the small-scale production of entomopathogens, and the biological control for fall armyworm management. We also discuss the prospects for using natural enemies against fall armyworm in China.
The fall armyworm, Spodoptera frugiperda(Smith)(FAW), is an insect pest that feeds on more than 80 crop species with the adult moth able to move over 100 km per night. FAW was first detected in Yunnan, southwest part of China in early 2019, and rapidly spread to 18 provinces within China by May this year, which seriously threatens the food and income security of millions of farmers. The development of emergency prevention and control technology at present and sustainable management technology in the near future are extremely urgent. Based on the studies of the pest's biology in the Americas and the experiences of management for this pest in Africa, we summary the knowledge about the species of the natural enemies(biological control agents), including entomophagous insects(parasitoids and predators) and entomopathogens(viruses,bacteria, fungi and nematodes), the biology and characters of the main group of natural enemies, the mass rearing of entomophagous insects, the small-scale production of entomopathogens, and the biological control for fall armyworm management. We also discuss the prospects for using natural enemies against fall armyworm in China.
引文
Barrera G,Simon O,Villamizar L,Williams T,Caballero P,2011.Spodoptera frugiperda multiple nucleopolyhedrovirus as a potential biological insecticide:Genetic and phenotypic comparison of field isolates from Colombia.Biological Control,58(2):113-120.
Barreto MR,Loguercio LL,Valicente FH,Paiva E,1999.Insecticidal activity of culture supernatants from Bacillus thuringiensis berliner strains against Spodoptera frugiperda Smith(Lepidoptera:Noctuidae)larvae.Anais da Sociedade Entomologica do Brasil,28(9):675-685.
Behle RW,Popham HJR,2012.Laboratory and field evaluations of the efficacy of a fast-killing baculovirus isolate from Spodoptera frugiperda.Journal of Invertebrate Pathology,109(2):194-200.
Beserra EB,Dias CTD,Parra JRP,2002.Distribution and natural parasitism of Spodoptera frugiperda(Lepidoptera:Noctuidae)eggs at different phenological stages of corn.Florida Entomologist,85(4):588-593.
Bratti A,1993.In vitro rearing of Lydella thompsoni Herting and Archytas marmoratus(Town.)(Dip.Tachinidae)larval stages:preliminary results.Istituto di Entomologia“Guido Grandi”Univsita di Bologna,48:93-100.
Bueno R,Bueno AD,Parra JRP,Vieira SS,de Oliveira LJ,2010a.Biological characteristics and parasitism capacity of Trichogramma pretiosum Riley(Hymenoptera,Trichogrammatidae)on eggs of Spodoptera frugiperda(J.E.Smith)(Lepidoptera,Noctuidae).Revista Brasileira de Entomologia,54(2):322-327.
Bueno R,Bueno AD,Xavier MFD,Carvalho MM,2014.Telenomus remus(Hymenoptera:Platygastridae)parasitism on eggs of Anticarsia gemmatalis(Lepidoptera:Eribidae)compared with its natural host Spodoptera frugiperda(Lepidoptera:Noctuidae).Annals of the Entomological Society of America,107(4):799-808.
Bueno R,Carneiro TR,Bueno AD,Pratissoli D,Fernandes OA,Vieira SS,2010b.Parasitism capacity of Telenomus remus Nixon(Hymenoptera:Scelionidae)on Spodoptera frugiperda(Smith)(Lepidoptera:Noctuidae)eggs.Brazilian Archives of Biology and Technology,53(1):133-139.
Carneiro TR,Fernandes OA,Cruz I,2009.Influence of females intraspecific competition and lack of host on Telenomus remus Nixon(Hymenoptera,Scelionidae)parasitism on Spodoptera frugiperda(J.E.Smith)(Lepidoptera,Noctuidae)eggs.Revista Brasileira de Entomologia,53(3):482-486.
Carneiro TR,Fernandes OA,Cruz I,Bueno R,2010.Functional response of Telenomus remus Nixon(Hymenoptera,Scelionidae)to Spodoptera frugiperda(J.E.Smith)(Lepidoptera,Noctuidae)eggs:effect of female age.Revista Brasileira de Entomologia,54(4):692-696.
Carpenter JE,Proshold FI,2000.Survival of Archytas marmoratus(Diptera:Tachinidae)from superparasitized corn earworm larvae(Lepidoptera:Noctuidae).Environmental Entomology,29(3):606-611.
Cave RD,2000.Biology,ecology and use in pest management of Telenomus remus.Biocontrol News and Information,21(1):21N-26N.
Chen L,Chen KW,Liang GW,2013.Antennal sensilla of female Telenomus remus observed with scanning electron microscopy.Journal of South China Agricultural University,34(1):72-75.[陈丽,陈科伟,梁广文,2013.夜蛾黑卵蜂雌蜂触角感器的扫描电镜观察.华南农业大学学报,34(1):72-75.]
Cisneros J,Perez JA,Penagos DI,Ruiz J,Goulson D,Caballero P,Cave RD,Williams T,2002.Formulation of a nucleopolyhedrovirus with boric acid for control of Spodoptera frugiperda(Lepidoptera:Noctuidae)in maize.Biological Control,23(1):87-95.
Correa Figueiredo MdL,Cruz I,da Silva RB,Foster JE,2015.Biological control with Trichogramma pretiosum increases organic maize productivity by 19.4%.Agronomy for Sustainable Development,35(3):1175-1183.
da Silva SMB,Silva-Werneck JO,Falcao R,Gomes AC,Fragoso RR,Quezado MT,Neto OBO,Aguiar JB,de Sa MFG,Bravo A,Monnerat RG,2004.Characterization of novel Brazilian Bacillus thuringiensis strains active against Spodoptera frugiperda and other insect pests.Journal of Applied Entomology,128(2):102-107.
Dequech STB,Camera C,Sturza VS,Ribeiro LD,Querino RB,Poncio S,2013.Population fluctuation of Spodoptera frugiperda eggs and natural parasitism by Trichogramma in maize.Acta Scientiarum-Agronomy,35(3):295-300.
Dequech STB,Da Silva RFP,Fiuza LM,2005.Interaction between Spodoptera frugiperda(J.E.Smith)(Lepidoptera:Noctuidae),Campoletis flavicincta(Ashmead)(Hymenoptera:Ichneumonidae)and Bacillus thuringiensis aizawai,in laboratory.Neotropical Entomology,34(6):937-944.
Desneux N,Ramirez-Romero R,Bokonon-Ganta AH,Bernal JS,2010.Attraction of the parasitoid Cotesia marginiventris to host(Spodoptera frugiperda)frass is affected by transgenic maize.Ecotoxicology,19(7):1183-1192.
Escribano A,Williams T,Goulson D,Cave RD,Chapman JW,Caballero P,2001.Consequences of interspecific competition on the virulence and genetic composition of a nucleopolyhedrovirus in Spodoptera frugiperda larvae parasitized by Chelonus insularis.Biocontrol Science and Technology,11(5):649-662.
FAO,2018.Integrated management of the fall armyworm on maize.A guide for Farmer Field Schools in Africa.Rome:Food and Agriculture Organization of the United Nations.1-139.
Feldmann F,Rieckmann U,Winter S,2019.The spread of the fall armyworm Spodoptera frugiperda in Africa:What should be done next?Journal of Plant Diseases and Protection,126(5):97-101.
Figueiredo MDLC,Della Lucia TMC,Cruz I,2010.Effect of Telenomus remus Nixon(Hymenoptera:Scelionidae)density on control of Spodoptera frugiperda(Smith)(Lepidoptera:Noctuidae)egg masses upon release in a maize field.Revista Brasileira de Milho e Sorgo,1(2):12-19.
Garcia LC,Raetano CG,Leite LG,2008.Application technology for the entomopathogenic nematodes Heterorhabditis indica and Steinernema sp.(Rhabditida:Heterorhabditidae and Steinernematidae)to control Spodoptera frugiperda(Smith)(Lepidoptera:Noctuidae)in corn.Neotropical Entomology,37(3):305-311.
Goergen G,Kumar PL,Sankung SB,Togola A,Tamo M,2016.First report of outbreaks of the fall armyworm Spodoptera frugiperda(JE Smith)(Lepidoptera,Noctuidae),a new alien invasive pest in west and central Africa.PLoS ONE,11(10):e0165632.
Gomez J,Guevara J,Cuartas P,Espinel C,Villamizar L,2013.Microencapsulated Spodoptera frugiperda nucleopolyhedrovirus:insecticidal activity and effect on arthropod populations in maize.Biocontrol Science and Technology,23(7):829-846.
Gross HR Jr,Johnson R,1985.Archytas marmoratus(Diptera:Tachinidae)advances in large-scale rearing and associated biological studies.Journal of Economic Entomology,78(6):1350-1353.
Haase S,Sciocco-Cap A,Romanowski V,2015.Baculovirus insecticides in Latin America:Historical overview,current status and future perspectives.Viruses-Basel,7(5):2230-2267.
Hamm JJ,Shapiro M,1992.Infectivity of fall armyworm(Lepidoptera,Noctuidae)nuclear polyhedrosis-virus enhanced by a fluorescent brightener.Journal of Economic Entomology,85(6):2149-2152.
Harrisona RD,Thierfelderb C,Baudronc F,Chinwadad P,Midegae C,Schaffnerf U,van den Bergg J,2019.Agro-ecological options for fall armyworm(Spodoptera frugiperda JE Smith)management:Providing low-cost,smallholder friendly solutions to an invasive pest.Journal of Environmental Management,243:318-330.
Jourdie V,Alvarez N,Molina-Ochoa J,Williams T,Bergvinson D,Benrey B,Turlings TCJ,Franck P,2010.Population genetic structure of two primary parasitoids of Spodoptera frugiperda(Lepidoptera),Chelonus insularis and Campoletis sonorensis(Hymenoptera):to what extent is the host plant important?Molecular Ecology,19(10):2168-2179.
Jourdie V,Alvarez N,Turlings TCJ,Franck P,2009.Isolation and characterization of polymorphic microsatellite loci in two primary parasitoids of the noctuid Spodoptera frugiperda:Chelonus insularis and Campoletis sonorensis(Hymenoptera).Molecular Ecology Resources,9(1):171-173.
Kaya HK,Aguillera MM,Alumai A,Choo HY,de la Torre M,Fodor A,Ganguly S,Hazir S,Lakatos T,Pye A,Wilsonk M,Yamanaka S,Yang HW,Ehlers RU,2006.Status of entomopathogenic nematodes and their symbiotic bacteria from selected countries or regions of the world.Biological Control,38(1):134-155.
Kenis M,du Plessis H,Van den Berg J,Ba MN,Goergen G,Kwadjo KE,Baoua I,Tefera T,Buddie A,Cafa G,Offord L,Rwomushana I,Polaszek A,2019.Telenomus remus,a candidate parasitoid for the biological control of Spodoptera frugiperda in Africa,is already present on the continent.Insects,10(4):92.
Lobo Lina M,van Harten A,1985.Luta biologica contra as pragas de cultures em Cabo Verde situa?ao actual a programas futuros.Revista Investiga?áo Agraria CEA,Sér A,1:3-11.
Matrangolo WJR,Martins-Dias AMP,Cruz I,2010.Aspectos biológicos de Campoletis flavicincta(Ashmead)(Hymenoptera:Ichneumonidae)e intera??es com o vírus da poliedrose nuclear de Spodoptera frugiperda.Revista Brasileira de Milho e Sorgo,6(1):207.
Molina-Ochoa J,Carpenter JE,Heinrichs EA,Foster JE,2003.Parasitoids and parasites of Spodoptera frugiperda(Lepidoptera:Noctuidae)in the Americas and Caribbean Basin:An inventory.Florida Entomologist,86(3):254-289.
Molina-Ochoa J,Carpenter JE,Lezama-Gutierrez R,Foster JE,Gonzalez-Ramirez M,Angel-Sahagun CA,Farias-Larios J,2004.Natural distribution of Hymenopteran parasitoids of Spodoptera frugiperda(Lepidoptera:Noctuidae)larvae in Mexico.Florida Entomologist,87(4):461-472.
Molina-Ochoa J,Lezama-Gutierrez R,Hamm JJ,Wiseman BR,Lopez-Edwards M,1999.Integrated control of fall armyworm(Lepidoptera:Noctuidae)using resistant plants and entomopathogenic nematodes(Rhabditida:Steinernematidae).Florida Entomologist,82(2):263-271.
Monnerat R,Martins E,Queiroz P,Orduz S,Jaramillo G,Benintende G,Cozzi J,Real MD,Martinez-Ramirez A,Rausell C,Cerón J,Ibarra JE,Del Rincon-Castro MC,Espinoza AM,Meza-Basso L,Cabrera L,Sánchez J,Soberon M,Bravo A,2006.Genetic variability of Spodoptera frugiperda Smith(Lepidoptera:Noctuidae)populations from Latin America is associated with variations in susceptibility to Bacillus thuringiensis cry toxins.Applied and Environmental Microbiology,72(11):7029-7035.
Montezano DG,Specht A,Sosa-Gómez DR,Roque-Specht VF,Sousa-Silva JC,Paula-Moraes SV,Peterson JA,Hunt TE,2018.Host plants of Spodoptera frugiperda(Lepidoptera:Noctuidae)in the Americas.African Entomology,26(2):286-301.
Moscardi F,1999.Assessment of the application of baculoviruses for control of Lepidoptera.Annual Review of Entomology,44:257-289.
Murua MG,Molina-Ochoa J,Fidalgo P,2009.Natural distribution of parasitoids of larvae of the fall armyworm,Spodoptera frugiperda,in Argentina.Journal of Insect Science,9(1):20.doi:10.1673/031.009.2001.
Neto FCM,Zanuncio JC,Cruz I,Guedes RNC,Picanco MC,2005.Progeny production and parasitism by Campoletis flavicincta(Hym.:Ichneumonidae)as affected by female ageing.Biological Agriculture&Horticulture,22(4):369-378.
Neto FDC,Cruz I,Zanuncio JC,Silva CHO,Picanco MC,2004.Parasitism by Campoletis flavicincta on Spodoptera frugiperda in corn.Pesquisa Agropecuaria Brasileira,39(11):1077-1081.
Nixon GEJ,1937.Some Asiatic Telenomin?(Hym.,Proctotrupoidea).Annals and Magazine of Natural History,20(10):444-475.
Noyes JS,2019.Universal chalcidoidea database.World Wide Web electronic publication.2019-03-15,http://www.nhm.ac.uk/chalcidoids.
Patel PN,Habib MEM,1987.Biological studies on Campoletis Flavicincta(Ashmead,1890)(Hym,Ichneumonidae),an endoparasite of the fall armyworm,Spodoptera frugiperda(Abbot And Smith,1797)(Lepid,Noctuidae).Journal of Applied Entomology-Zeitschrift fur Angewandte Entomologie,104(1):28-35.
Penaflor M,Sarmento MMD,da Silva CSB,Werneburg AG,Bento JMS,2012.Effect of host egg age on preference,development and arrestment of Telenomus remus(Hymenoptera:Scelionidae).European Journal of Entomology,109(1):15-20.
Polanczyk RA,da Silva RFP,Fiuza LM,2000.Effectiveness of Bacillus thuringiensis strains against Spodoptera frugiperda(Lepidoptera:Noctuidae).Brazilian Journal of Microbiology,31(3):165-167.
Pomari AF,Bueno AD,Bueno R,Menezes AD,Fonseca A,2013a.Releasing number of Telenomus remus(Nixon)(Hymenoptera:Platygastridae)against Spodoptera frugiperda Smith(Lepidoptera:Noctuidae)in corn,cotton and soybean.Ciência Rural,43(3):377-382.
Pomari AF,Bueno AdF,Bueno RCOdF,Junior M,de Oliveiras A,Fonseca ACPF,2013b.Releasing number of Telenomus remus(Nixon)(Hymenoptera:Platygastridae)against Spodoptera frugiperda Smith(Lepidoptera:Noctuidae)in corn,cotton and soybean.Ciência Rural,43(3):377-382.
Prasanna B,Huesing J,Eddy R,Peschke V,2018.Fall Armyworm in Africa:A Guide for Integrated Pest Management.Wallingford:CAB International.1-109.
Queiroz AP,Bueno AD,Pomari-Fernandes A,Grande MLM,Bortolotto OC,da Silva DM,2017.Quality control of Telenomus remus(Hymenoptera:Platygastridae)reared on the factitious host Corcyra cephalonica(Lepidoptera:Pyralidae)for successive generations.Bulletin of Entomological Research,107(6):791-798.
Rwomushana I,Bateman M,Beale T,Beseh P,Cameron K,Chiluba M,Clottey V,Davis T,Day R,Early R,Godwin J,Gonzalez-Moreno P,Kansiime M,Kenis M,Makale F,Mugambi I,Murphy S,Nunda W,Phiri N,Pratt C,Tambo J,2018.Fall armyworm:Impacts and implications for Africa.Evidence note update.Wallingford:CAB International.1-53.
Salas Araiza MD,2018.Natural enemies of the fall armyworm and the corn earworm in sorghum and maize in Irapuato,Guanajuato,Mexico.Southwestern Entomologist,43(3):715-722.
Shapiro-Ilan DI,Gouge DH,Piggott SJ,Fife JP,2006.Application technology and environmental considerations for use of entomopathogenic nematodes in biological control.Biological Control,38(1):124-133.
Shylesha AN,Jalali SK,Gupta A,Varshney R,Venkatesan T,Shetty P,Ojha R,Ganiger PC,Navik O,Subaharan K,Bakthavatsalam N,Ballal CR,Raghavendra A,2018.Studies on new invasive pest Spodoptera frugiperda(J.E.Smith)(Lepidoptera:Noctuidae)and its natural enemies.Journal of Biological Control,32(3):145-151.
Silva RB,Cruz I,Penteado-Dias AM,2014.First report of Dolichozele koebelei Viereck,1911(Hymenoptera:Braconidae)on larvae of Spodoptera frugiperda(J.E.Smith,1797)(Lepidoptera:Noctuidae)in maize(Zea mays L.)under different cropping systems.Brazilian Journal of Biology,74(3):218-222.
Tang YL,Chen KW,Xu ZF,2013.Study on ontogenesis of Telenomus remus Nixon(Hymenoptera:Scelionidae).Journal of Changjiang Vegetables,18:1-3.[唐雅丽,陈科伟,许再福,2010.夜蛾黑卵蜂(Telenomus remus Nixon)个体发育研究.长江蔬菜,18:1-3.]
Valicente FH,Tuelher ES,2009.Controle Biológico da Lagarta do Cartucho,Spodoptera frugiperda,com Baculovirus.Sete Lagoas:Embrapa Milho e Sorgo.1-14.
Valicente FH,Tuelher ES,Barros EC,2010.Processo de formula??o do Baculovirus spodoptera em pómolhável.Sete Lagoas:Embrapa Milho e Sorgo.1-5.
van Harten A,1991.Influence of parasitoids on the mortality of pests in vegetable cultivation in CapeVerde.Journal of Applied Entomology,111(5):521-525.
Vieira NF,Pomari-Fernandes A,Lemes AAF,Vacari AM,De Bortoli SA,Bueno AD,2017.Cost of production of Telenomus remus(Hymenoptera:Platygastridae)grown in natural and alternative hosts.Journal of Economic Entomology,110(6):2724-2726.
Wang ZY,He KL,Zhang F,Lu X,Babendreier D,2014.Mass rearing and release of Trichogramma for biological control of insect pests of corn in China.Biological Control,68:136-144.
Wraight SP,Ramos ME,Avery PB,Jaronski ST,Vandenberg JD,2010.Comparative virulence of Beauveria bassiana isolates against lepidopteran pests of vegetable crops.J.Invertebr.Pathol.,103(3):186-199.
Xiang YY,Zhang F,2011.Review of application research on Trichogramma westwood in biological control in China.Journal of Henan Agricultural Sciences,40(12):20-24.[向玉勇,张帆,2011.赤眼蜂在我国生物防治中的应用研究进展.河南农业科学,40(12):20-24.]
Yang Y,Han Y,Fang ZhH,Xu ZF,2012.Effect of host egg age and contact time on the parasitic capacity of Telenomus remus(Hymenoptera:Scelionidae).Chinese Journal of Applied Entomology,49(6):1490-1495.[杨莹,韩勇,方祝红,许再福,2012.寄主卵龄和接触时间对夜蛾黑卵蜂寄生能力的影响.应用昆虫学报,49(6):1490-1495.]
Yu DSK,van Achterberg C,Horstmann K,2016.Taxapad 2016,Ichneumonoidea 2015.Taxapad database on flash-drive,Ottawa,Can.2019-03-15.
Zenner I,Alvarez A,Barreto S,2006.Influence of parasitism by Chelonus insularis Cresson(Hymenoptera:Braconidae)on the susceptibility of Spodoptera frugiperda(J.E.Smith)(Lepidoptera:Noctuidae)to insecticides.Neotropical Entomology,35(6):818-822.
Barreto MR,Loguercio LL,Valicente FH,Paiva E,1999.Insecticidal activity of culture supernatants from Bacillus thuringiensis berliner strains against Spodoptera frugiperda Smith(Lepidoptera:Noctuidae)larvae.Anais da Sociedade Entomologica do Brasil,28(9):675-685.
Behle RW,Popham HJR,2012.Laboratory and field evaluations of the efficacy of a fast-killing baculovirus isolate from Spodoptera frugiperda.Journal of Invertebrate Pathology,109(2):194-200.
Beserra EB,Dias CTD,Parra JRP,2002.Distribution and natural parasitism of Spodoptera frugiperda(Lepidoptera:Noctuidae)eggs at different phenological stages of corn.Florida Entomologist,85(4):588-593.
Bratti A,1993.In vitro rearing of Lydella thompsoni Herting and Archytas marmoratus(Town.)(Dip.Tachinidae)larval stages:preliminary results.Istituto di Entomologia“Guido Grandi”Univsita di Bologna,48:93-100.
Bueno R,Bueno AD,Parra JRP,Vieira SS,de Oliveira LJ,2010a.Biological characteristics and parasitism capacity of Trichogramma pretiosum Riley(Hymenoptera,Trichogrammatidae)on eggs of Spodoptera frugiperda(J.E.Smith)(Lepidoptera,Noctuidae).Revista Brasileira de Entomologia,54(2):322-327.
Bueno R,Bueno AD,Xavier MFD,Carvalho MM,2014.Telenomus remus(Hymenoptera:Platygastridae)parasitism on eggs of Anticarsia gemmatalis(Lepidoptera:Eribidae)compared with its natural host Spodoptera frugiperda(Lepidoptera:Noctuidae).Annals of the Entomological Society of America,107(4):799-808.
Bueno R,Carneiro TR,Bueno AD,Pratissoli D,Fernandes OA,Vieira SS,2010b.Parasitism capacity of Telenomus remus Nixon(Hymenoptera:Scelionidae)on Spodoptera frugiperda(Smith)(Lepidoptera:Noctuidae)eggs.Brazilian Archives of Biology and Technology,53(1):133-139.
Carneiro TR,Fernandes OA,Cruz I,2009.Influence of females intraspecific competition and lack of host on Telenomus remus Nixon(Hymenoptera,Scelionidae)parasitism on Spodoptera frugiperda(J.E.Smith)(Lepidoptera,Noctuidae)eggs.Revista Brasileira de Entomologia,53(3):482-486.
Carneiro TR,Fernandes OA,Cruz I,Bueno R,2010.Functional response of Telenomus remus Nixon(Hymenoptera,Scelionidae)to Spodoptera frugiperda(J.E.Smith)(Lepidoptera,Noctuidae)eggs:effect of female age.Revista Brasileira de Entomologia,54(4):692-696.
Carpenter JE,Proshold FI,2000.Survival of Archytas marmoratus(Diptera:Tachinidae)from superparasitized corn earworm larvae(Lepidoptera:Noctuidae).Environmental Entomology,29(3):606-611.
Cave RD,2000.Biology,ecology and use in pest management of Telenomus remus.Biocontrol News and Information,21(1):21N-26N.
Chen L,Chen KW,Liang GW,2013.Antennal sensilla of female Telenomus remus observed with scanning electron microscopy.Journal of South China Agricultural University,34(1):72-75.[陈丽,陈科伟,梁广文,2013.夜蛾黑卵蜂雌蜂触角感器的扫描电镜观察.华南农业大学学报,34(1):72-75.]
Cisneros J,Perez JA,Penagos DI,Ruiz J,Goulson D,Caballero P,Cave RD,Williams T,2002.Formulation of a nucleopolyhedrovirus with boric acid for control of Spodoptera frugiperda(Lepidoptera:Noctuidae)in maize.Biological Control,23(1):87-95.
Correa Figueiredo MdL,Cruz I,da Silva RB,Foster JE,2015.Biological control with Trichogramma pretiosum increases organic maize productivity by 19.4%.Agronomy for Sustainable Development,35(3):1175-1183.
da Silva SMB,Silva-Werneck JO,Falcao R,Gomes AC,Fragoso RR,Quezado MT,Neto OBO,Aguiar JB,de Sa MFG,Bravo A,Monnerat RG,2004.Characterization of novel Brazilian Bacillus thuringiensis strains active against Spodoptera frugiperda and other insect pests.Journal of Applied Entomology,128(2):102-107.
Dequech STB,Camera C,Sturza VS,Ribeiro LD,Querino RB,Poncio S,2013.Population fluctuation of Spodoptera frugiperda eggs and natural parasitism by Trichogramma in maize.Acta Scientiarum-Agronomy,35(3):295-300.
Dequech STB,Da Silva RFP,Fiuza LM,2005.Interaction between Spodoptera frugiperda(J.E.Smith)(Lepidoptera:Noctuidae),Campoletis flavicincta(Ashmead)(Hymenoptera:Ichneumonidae)and Bacillus thuringiensis aizawai,in laboratory.Neotropical Entomology,34(6):937-944.
Desneux N,Ramirez-Romero R,Bokonon-Ganta AH,Bernal JS,2010.Attraction of the parasitoid Cotesia marginiventris to host(Spodoptera frugiperda)frass is affected by transgenic maize.Ecotoxicology,19(7):1183-1192.
Escribano A,Williams T,Goulson D,Cave RD,Chapman JW,Caballero P,2001.Consequences of interspecific competition on the virulence and genetic composition of a nucleopolyhedrovirus in Spodoptera frugiperda larvae parasitized by Chelonus insularis.Biocontrol Science and Technology,11(5):649-662.
FAO,2018.Integrated management of the fall armyworm on maize.A guide for Farmer Field Schools in Africa.Rome:Food and Agriculture Organization of the United Nations.1-139.
Feldmann F,Rieckmann U,Winter S,2019.The spread of the fall armyworm Spodoptera frugiperda in Africa:What should be done next?Journal of Plant Diseases and Protection,126(5):97-101.
Figueiredo MDLC,Della Lucia TMC,Cruz I,2010.Effect of Telenomus remus Nixon(Hymenoptera:Scelionidae)density on control of Spodoptera frugiperda(Smith)(Lepidoptera:Noctuidae)egg masses upon release in a maize field.Revista Brasileira de Milho e Sorgo,1(2):12-19.
Garcia LC,Raetano CG,Leite LG,2008.Application technology for the entomopathogenic nematodes Heterorhabditis indica and Steinernema sp.(Rhabditida:Heterorhabditidae and Steinernematidae)to control Spodoptera frugiperda(Smith)(Lepidoptera:Noctuidae)in corn.Neotropical Entomology,37(3):305-311.
Goergen G,Kumar PL,Sankung SB,Togola A,Tamo M,2016.First report of outbreaks of the fall armyworm Spodoptera frugiperda(JE Smith)(Lepidoptera,Noctuidae),a new alien invasive pest in west and central Africa.PLoS ONE,11(10):e0165632.
Gomez J,Guevara J,Cuartas P,Espinel C,Villamizar L,2013.Microencapsulated Spodoptera frugiperda nucleopolyhedrovirus:insecticidal activity and effect on arthropod populations in maize.Biocontrol Science and Technology,23(7):829-846.
Gross HR Jr,Johnson R,1985.Archytas marmoratus(Diptera:Tachinidae)advances in large-scale rearing and associated biological studies.Journal of Economic Entomology,78(6):1350-1353.
Haase S,Sciocco-Cap A,Romanowski V,2015.Baculovirus insecticides in Latin America:Historical overview,current status and future perspectives.Viruses-Basel,7(5):2230-2267.
Hamm JJ,Shapiro M,1992.Infectivity of fall armyworm(Lepidoptera,Noctuidae)nuclear polyhedrosis-virus enhanced by a fluorescent brightener.Journal of Economic Entomology,85(6):2149-2152.
Harrisona RD,Thierfelderb C,Baudronc F,Chinwadad P,Midegae C,Schaffnerf U,van den Bergg J,2019.Agro-ecological options for fall armyworm(Spodoptera frugiperda JE Smith)management:Providing low-cost,smallholder friendly solutions to an invasive pest.Journal of Environmental Management,243:318-330.
Jourdie V,Alvarez N,Molina-Ochoa J,Williams T,Bergvinson D,Benrey B,Turlings TCJ,Franck P,2010.Population genetic structure of two primary parasitoids of Spodoptera frugiperda(Lepidoptera),Chelonus insularis and Campoletis sonorensis(Hymenoptera):to what extent is the host plant important?Molecular Ecology,19(10):2168-2179.
Jourdie V,Alvarez N,Turlings TCJ,Franck P,2009.Isolation and characterization of polymorphic microsatellite loci in two primary parasitoids of the noctuid Spodoptera frugiperda:Chelonus insularis and Campoletis sonorensis(Hymenoptera).Molecular Ecology Resources,9(1):171-173.
Kaya HK,Aguillera MM,Alumai A,Choo HY,de la Torre M,Fodor A,Ganguly S,Hazir S,Lakatos T,Pye A,Wilsonk M,Yamanaka S,Yang HW,Ehlers RU,2006.Status of entomopathogenic nematodes and their symbiotic bacteria from selected countries or regions of the world.Biological Control,38(1):134-155.
Kenis M,du Plessis H,Van den Berg J,Ba MN,Goergen G,Kwadjo KE,Baoua I,Tefera T,Buddie A,Cafa G,Offord L,Rwomushana I,Polaszek A,2019.Telenomus remus,a candidate parasitoid for the biological control of Spodoptera frugiperda in Africa,is already present on the continent.Insects,10(4):92.
Lobo Lina M,van Harten A,1985.Luta biologica contra as pragas de cultures em Cabo Verde situa?ao actual a programas futuros.Revista Investiga?áo Agraria CEA,Sér A,1:3-11.
Matrangolo WJR,Martins-Dias AMP,Cruz I,2010.Aspectos biológicos de Campoletis flavicincta(Ashmead)(Hymenoptera:Ichneumonidae)e intera??es com o vírus da poliedrose nuclear de Spodoptera frugiperda.Revista Brasileira de Milho e Sorgo,6(1):207.
Molina-Ochoa J,Carpenter JE,Heinrichs EA,Foster JE,2003.Parasitoids and parasites of Spodoptera frugiperda(Lepidoptera:Noctuidae)in the Americas and Caribbean Basin:An inventory.Florida Entomologist,86(3):254-289.
Molina-Ochoa J,Carpenter JE,Lezama-Gutierrez R,Foster JE,Gonzalez-Ramirez M,Angel-Sahagun CA,Farias-Larios J,2004.Natural distribution of Hymenopteran parasitoids of Spodoptera frugiperda(Lepidoptera:Noctuidae)larvae in Mexico.Florida Entomologist,87(4):461-472.
Molina-Ochoa J,Lezama-Gutierrez R,Hamm JJ,Wiseman BR,Lopez-Edwards M,1999.Integrated control of fall armyworm(Lepidoptera:Noctuidae)using resistant plants and entomopathogenic nematodes(Rhabditida:Steinernematidae).Florida Entomologist,82(2):263-271.
Monnerat R,Martins E,Queiroz P,Orduz S,Jaramillo G,Benintende G,Cozzi J,Real MD,Martinez-Ramirez A,Rausell C,Cerón J,Ibarra JE,Del Rincon-Castro MC,Espinoza AM,Meza-Basso L,Cabrera L,Sánchez J,Soberon M,Bravo A,2006.Genetic variability of Spodoptera frugiperda Smith(Lepidoptera:Noctuidae)populations from Latin America is associated with variations in susceptibility to Bacillus thuringiensis cry toxins.Applied and Environmental Microbiology,72(11):7029-7035.
Montezano DG,Specht A,Sosa-Gómez DR,Roque-Specht VF,Sousa-Silva JC,Paula-Moraes SV,Peterson JA,Hunt TE,2018.Host plants of Spodoptera frugiperda(Lepidoptera:Noctuidae)in the Americas.African Entomology,26(2):286-301.
Moscardi F,1999.Assessment of the application of baculoviruses for control of Lepidoptera.Annual Review of Entomology,44:257-289.
Murua MG,Molina-Ochoa J,Fidalgo P,2009.Natural distribution of parasitoids of larvae of the fall armyworm,Spodoptera frugiperda,in Argentina.Journal of Insect Science,9(1):20.doi:10.1673/031.009.2001.
Neto FCM,Zanuncio JC,Cruz I,Guedes RNC,Picanco MC,2005.Progeny production and parasitism by Campoletis flavicincta(Hym.:Ichneumonidae)as affected by female ageing.Biological Agriculture&Horticulture,22(4):369-378.
Neto FDC,Cruz I,Zanuncio JC,Silva CHO,Picanco MC,2004.Parasitism by Campoletis flavicincta on Spodoptera frugiperda in corn.Pesquisa Agropecuaria Brasileira,39(11):1077-1081.
Nixon GEJ,1937.Some Asiatic Telenomin?(Hym.,Proctotrupoidea).Annals and Magazine of Natural History,20(10):444-475.
Noyes JS,2019.Universal chalcidoidea database.World Wide Web electronic publication.2019-03-15,http://www.nhm.ac.uk/chalcidoids.
Patel PN,Habib MEM,1987.Biological studies on Campoletis Flavicincta(Ashmead,1890)(Hym,Ichneumonidae),an endoparasite of the fall armyworm,Spodoptera frugiperda(Abbot And Smith,1797)(Lepid,Noctuidae).Journal of Applied Entomology-Zeitschrift fur Angewandte Entomologie,104(1):28-35.
Penaflor M,Sarmento MMD,da Silva CSB,Werneburg AG,Bento JMS,2012.Effect of host egg age on preference,development and arrestment of Telenomus remus(Hymenoptera:Scelionidae).European Journal of Entomology,109(1):15-20.
Polanczyk RA,da Silva RFP,Fiuza LM,2000.Effectiveness of Bacillus thuringiensis strains against Spodoptera frugiperda(Lepidoptera:Noctuidae).Brazilian Journal of Microbiology,31(3):165-167.
Pomari AF,Bueno AD,Bueno R,Menezes AD,Fonseca A,2013a.Releasing number of Telenomus remus(Nixon)(Hymenoptera:Platygastridae)against Spodoptera frugiperda Smith(Lepidoptera:Noctuidae)in corn,cotton and soybean.Ciência Rural,43(3):377-382.
Pomari AF,Bueno AdF,Bueno RCOdF,Junior M,de Oliveiras A,Fonseca ACPF,2013b.Releasing number of Telenomus remus(Nixon)(Hymenoptera:Platygastridae)against Spodoptera frugiperda Smith(Lepidoptera:Noctuidae)in corn,cotton and soybean.Ciência Rural,43(3):377-382.
Prasanna B,Huesing J,Eddy R,Peschke V,2018.Fall Armyworm in Africa:A Guide for Integrated Pest Management.Wallingford:CAB International.1-109.
Queiroz AP,Bueno AD,Pomari-Fernandes A,Grande MLM,Bortolotto OC,da Silva DM,2017.Quality control of Telenomus remus(Hymenoptera:Platygastridae)reared on the factitious host Corcyra cephalonica(Lepidoptera:Pyralidae)for successive generations.Bulletin of Entomological Research,107(6):791-798.
Rwomushana I,Bateman M,Beale T,Beseh P,Cameron K,Chiluba M,Clottey V,Davis T,Day R,Early R,Godwin J,Gonzalez-Moreno P,Kansiime M,Kenis M,Makale F,Mugambi I,Murphy S,Nunda W,Phiri N,Pratt C,Tambo J,2018.Fall armyworm:Impacts and implications for Africa.Evidence note update.Wallingford:CAB International.1-53.
Salas Araiza MD,2018.Natural enemies of the fall armyworm and the corn earworm in sorghum and maize in Irapuato,Guanajuato,Mexico.Southwestern Entomologist,43(3):715-722.
Shapiro-Ilan DI,Gouge DH,Piggott SJ,Fife JP,2006.Application technology and environmental considerations for use of entomopathogenic nematodes in biological control.Biological Control,38(1):124-133.
Shylesha AN,Jalali SK,Gupta A,Varshney R,Venkatesan T,Shetty P,Ojha R,Ganiger PC,Navik O,Subaharan K,Bakthavatsalam N,Ballal CR,Raghavendra A,2018.Studies on new invasive pest Spodoptera frugiperda(J.E.Smith)(Lepidoptera:Noctuidae)and its natural enemies.Journal of Biological Control,32(3):145-151.
Silva RB,Cruz I,Penteado-Dias AM,2014.First report of Dolichozele koebelei Viereck,1911(Hymenoptera:Braconidae)on larvae of Spodoptera frugiperda(J.E.Smith,1797)(Lepidoptera:Noctuidae)in maize(Zea mays L.)under different cropping systems.Brazilian Journal of Biology,74(3):218-222.
Tang YL,Chen KW,Xu ZF,2013.Study on ontogenesis of Telenomus remus Nixon(Hymenoptera:Scelionidae).Journal of Changjiang Vegetables,18:1-3.[唐雅丽,陈科伟,许再福,2010.夜蛾黑卵蜂(Telenomus remus Nixon)个体发育研究.长江蔬菜,18:1-3.]
Valicente FH,Tuelher ES,2009.Controle Biológico da Lagarta do Cartucho,Spodoptera frugiperda,com Baculovirus.Sete Lagoas:Embrapa Milho e Sorgo.1-14.
Valicente FH,Tuelher ES,Barros EC,2010.Processo de formula??o do Baculovirus spodoptera em pómolhável.Sete Lagoas:Embrapa Milho e Sorgo.1-5.
van Harten A,1991.Influence of parasitoids on the mortality of pests in vegetable cultivation in CapeVerde.Journal of Applied Entomology,111(5):521-525.
Vieira NF,Pomari-Fernandes A,Lemes AAF,Vacari AM,De Bortoli SA,Bueno AD,2017.Cost of production of Telenomus remus(Hymenoptera:Platygastridae)grown in natural and alternative hosts.Journal of Economic Entomology,110(6):2724-2726.
Wang ZY,He KL,Zhang F,Lu X,Babendreier D,2014.Mass rearing and release of Trichogramma for biological control of insect pests of corn in China.Biological Control,68:136-144.
Wraight SP,Ramos ME,Avery PB,Jaronski ST,Vandenberg JD,2010.Comparative virulence of Beauveria bassiana isolates against lepidopteran pests of vegetable crops.J.Invertebr.Pathol.,103(3):186-199.
Xiang YY,Zhang F,2011.Review of application research on Trichogramma westwood in biological control in China.Journal of Henan Agricultural Sciences,40(12):20-24.[向玉勇,张帆,2011.赤眼蜂在我国生物防治中的应用研究进展.河南农业科学,40(12):20-24.]
Yang Y,Han Y,Fang ZhH,Xu ZF,2012.Effect of host egg age and contact time on the parasitic capacity of Telenomus remus(Hymenoptera:Scelionidae).Chinese Journal of Applied Entomology,49(6):1490-1495.[杨莹,韩勇,方祝红,许再福,2012.寄主卵龄和接触时间对夜蛾黑卵蜂寄生能力的影响.应用昆虫学报,49(6):1490-1495.]
Yu DSK,van Achterberg C,Horstmann K,2016.Taxapad 2016,Ichneumonoidea 2015.Taxapad database on flash-drive,Ottawa,Can.2019-03-15.
Zenner I,Alvarez A,Barreto S,2006.Influence of parasitism by Chelonus insularis Cresson(Hymenoptera:Braconidae)on the susceptibility of Spodoptera frugiperda(J.E.Smith)(Lepidoptera:Noctuidae)to insecticides.Neotropical Entomology,35(6):818-822.