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Prospects for microbial control of the fall armyworm Spodoptera frugiperda: a review

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Abstract

The fall armyworm (FAW, Spodoptera frugiperda) is an important polyphagous insect pest in many crops. This highly invasive pest species originates from the Americas and recently spread rapidly across more than 100 countries worldwide. It poses a major threat to food security in a number of developing countries due to its rapid spread and distinctive ability to inflict widespread damage across multiple crops. Chemical insecticides are used as the main management strategy to control FAW in many parts of the world, particularly in the recently invaded areas in Africa and Asia. However, concerns over the adverse effects on environment and humans, and the development of resistance against insecticides have intensified efforts to develop alternatives that are effective and low-risk, while at the same time cost effective. Given that microbials are generally considered desirable options for pest management, this review compiles information on microbials in all phases of their development including entomopathogenic fungi, entomopathogenic nematodes, bacteria and baculoviruses, with a special focus on their efficacy against FAW. In addition, combinations of microbial agents and also mixtures with compatible insecticides for improved control of FAW are reviewed. The findings are discussed in light of improving management programs of FAW

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References

  • Akutse KS, Kimemia JW, Ekesi S, Khamis FM, Ombura OL, Subramanian S (2019) Ovicidal effects of entomopathogenic fungal isolates on the invasive Fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). J Appl Entomol 143(6):626–634

    CAS  Google Scholar 

  • Alonso A, Alama A, Noriega Mejía MR (2018) Efecto de tres concentraciones de Heterorhabditis bacteriophora Poinar en la mortalidad de prepupas y pupas de Spodoptera frugiperda (Smith & Abbot), en laboratorio e invernadero. https://dspace.unitru.edu.pe/handle/UNITRU/10908

  • Altre JA, Vandenberg JD (2001a) Penetration of cuticle and proliferation in hemolymph by Paecilomyces fumosoroseus isolates that differ in virulence against lepidopteran larvae. J Invertebr Pathol 78:81–86

    CAS  PubMed  Google Scholar 

  • Altre JA, Vandenberg JD (2001b) Comparison of blastospores of two Paecilomyces fumosoroseus isolates: in vitro traits and virulence when injected into fall armyworm, Spodoptera frugiperda. J Invertebr Pathol 78:170–175

    CAS  PubMed  Google Scholar 

  • Andaló V, Santos V, Moreira GF, Moreira CC, Moino JA (2012a) Evaluation of entomopathogenic nematodes under laboratory and greenhouses conditions for the control of Spodoptera frugiperda. Cienc Rural 40:1860–1866

    Google Scholar 

  • Andaló V, Santos V, Moreira GF, Moreira C, Freire M, Moino A (2012b) Movement of Heterorhabditis amazonensis and Steinernema arenarium in search of maize fall armyworm larvae in artificial conditions. Sci Agric 69:226–230

    Google Scholar 

  • Ansari MA, Shah FA, Butt TM (2008) Combined use of entomopathogenic nematodes and Metarhizium anisopliae as a new approach for black vine weevil, Otiorhynchus sulcatus, control. Entomol Exp Appl 129:340–347

    Google Scholar 

  • Arango JA, Romero M, Orduz S (2002) Diversity of Bacillus thuringiensis strains from Colombia with insecticidal activity against Spodoptera frugiperda (Lepidoptera: Noctuidae). J Appl Microbiol 92(3):466–474

    CAS  PubMed  Google Scholar 

  • Ayala OR, Navarro F, Virla EG (2013) Evaluation of the attack rates and level of damages by the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), affecting corn-crops in the northeast of Argentina. Rev Fac Cienc Agrar 45:1–12

    Google Scholar 

  • Ayala-Zermeño MA, Gallou A, Berlanga-Padilla AM, Andrade-Michel GY, Rodríguez-Rodríguez JC, Arredondo-Bernal HC, Montesinos-Matias R (2017) Viability, purity, and genetic stability of entomopathogenic fungi species using different preservation methods. Fungal Biol 121:920–928

    PubMed  Google Scholar 

  • Baradaran E, Moharramipour S, Asgari S, Mehrabadi M (2019) Upregulation of Helicoverpa armigera core RNA interference genes by bacterial infections and its effect on the insect–bacteria interaction. Insect Mole Biol 28(2):290–299

    CAS  Google Scholar 

  • Barrera G, Simón 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. Biol Control 58:113–120

    CAS  Google Scholar 

  • Barrera-Cubillos GP, Gómez-Valderrama JA, Rivero LFV (2017) Efficacy of microencapsulated nucleopolyhedroviruses from Colombia as biological insecticides against Spodoptera frugiperda (Lepidoptera: Noctuidae). Acta Agronómica 66(2):267–274

    Google Scholar 

  • Bateman ML, Day RK, Luke B, Edgington S, Kuhlmann U, Cock MJ (2018) Assessment of potential biopesticide options for managing fall armyworm (Spodoptera frugiperda) in Africa. J Appl Entomol 142:805–819

    Google Scholar 

  • Bentivenha JP, Rodrigues JG, Lima MF, Marçon P, Popham HJ, Omoto C (2018) Baseline susceptibility of Spodoptera frugiperda (Lepidoptera: Noctuidae) to SfMNPV and evaluation of cross-resistance to major insecticides and Bt Proteins. J Econ Enromol 112:91–98

    Google Scholar 

  • Bernhard K, Jarrett P, Meadows M, Butt J, Ellis DJ, Roberts GM, Pauli S, Rodgers P, Burges HD (1997) Natural isolates of Bacillus thuringiensis: worldwide distribution, characterization, and activity against insect pests. J Invertebr Pathol 70:59–68

    Google Scholar 

  • Burtet LM, Bernardi O, Melo A, Pes A, Strahl TT, Guedes JV (2017) Managing fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), with Bt maize and insecticides in southern Brazil. Pest Manag Sci 73:2569–2577

    CAS  PubMed  Google Scholar 

  • Butt T, Dudley E, Lord A, Greenfeild B (2014) Conidia of the insect pathogenic fungus, Metarhizium anisopliae, fail to adhere to mosquito larval cuticle. R Soc Open Sci 1:140193

    PubMed  PubMed Central  Google Scholar 

  • CABI (2018) Fall armyworm: Impacts and implications for Africa. https://www.invasive-species.org/wp-content/uploads/sites/2/2019/02/FAW-Evidence-Note-October-2018.pdf. Accessed 13 Mar 2019

  • CABI (2019) Datasheet Spodoptera frugiperda (fall armyworm). Invasive Species Compendium. https://www.cabi.org/isc/datasheet/29810#94987198-9f50-4173-8bbd-30bd93840e73?tdsourcetag=s_pcqq_aiomsg. Accessed 19 Oct 2019

  • Céspedes Y, Pozo ED, García I, Méndez A (2008) Effect of temperature on the entomopathogenic fungus Nomuraea rileyi (Farlow) Samson and its effectiveness on Spodoptera frugiperda JE Smith. Revista de Protección Vegetal 23:176–182

    Google Scholar 

  • Chávez D, Torres L, París A, Villamizar L, Cotes A (2004) Evaluation of natíve isolates of Nomuraea rileyi for the control of Spodoptera frugiperda (Lepidoptera: Noctuidae). Rev Colomb Entomol 30:93–97

    Google Scholar 

  • Cory JS, Myers JH (2003) The ecology and evolution of insect baculoviruses. Annu Rev Ecol Evol Syst 34:239–272

    Google Scholar 

  • Cubillos GPB (2013) Spodoptera frugiperda nucleopolyhedrovirus: the basis for a biopesticide product in Colombia. Diss Universidad Pública de Navarra.

  • Cruz I, Figueiredo ML, Valicente FH, Oliveira AC (1997) Application rate trials with a nuclear polyhedrosis virus to control Spodoptera frugiperda (Smith) on maize. Anais da Sociedade Entomológica do Brasil 26:145–152

    Google Scholar 

  • Cruz-Avalos AM, Bivián-Hernández MDLÁ, Ibarra JE, Del Rincón-Castro MC (2019) High virulence of Mexican entomopathogenic fungi against fall armyworm, (lepidoptera: noctuidae). J Econ Entomol 112:99–107

    CAS  PubMed  Google Scholar 

  • Day R, Abrahams P, Bateman M, Beale T, Clottey V, Cock M, Colmenarez Y, Corniani N, Early R, Godwin J, Gomez J, Moreno PJ, Murphy ST, Oppong-Mensah B, Phiri N, Pratt C, Silvestri S, Witt A (2017) Fall armyworm: impacts and implications for Africa. Outlooks on Pest Manag 28:196–201

    Google Scholar 

  • De Maagd RA, Bravo A, Crickmore N (2001) How Bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Genet 17:193–199

    PubMed  Google Scholar 

  • De Souza LM, Moino J, Mertz NR, da Silva MAT, Soares FM, Bonete Filho RZ (2012) Entomopathogenic nematodes and their compatibility with imidacloprid in the control of Spodoptera frugiperda in a forest nursery. Nematol Bras 36:32–41

    Google Scholar 

  • dos Santos KB, Neves P, Meneguim AM, dos Santos RB, dos Santos WJ, Boas GV, Dumas V, Martins E, Praça LB, Queiroz P, Berry C, Monnerat R (2009) Selection and characterization of the Bacillus thuringiensis strains toxic to Spodoptera eridania (Cramer), Spodoptera cosmioides (Walker) and Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae). Biol Control 50:157–163

    Google Scholar 

  • El-Sheikh EA (2015) Efficacy of Spodoptera littoralis nucleopolyherdovirus on Spodoptera frugiperda (J.E. Smith) and Spodoptera exigua (Hübner): virulence, biological effects, and inhibition of juvenile hormone esterase. J Biol Pest Control 25:587–595

    Google Scholar 

  • Escribano A, Williams T, Goulson D, Cave RD, Chapman JW, Caballero P (1999) Selection of a nucleopolyhedrovirus for control of Spodoptera frugiperda (Lepidoptera: Noctuidae): structural, genetic, and biological comparison of four isolates from the Americas. J Econ Entomol 92:1079–1085

    CAS  PubMed  Google Scholar 

  • Espky ND, Capinera JL (1994) Invasion efficiency as a measure of efficacy of the entomogenous nematode Steinernema carpocapsae (Rhabditida: Steinernematidae). J Econ Enromol 87:366–370

    Google Scholar 

  • Fallet P, Gianni L, Kajuga J, Waithira B, Machado R, Glauser G, Toepfer S, Turlings T (2019) Novel approaches to control the fall armyworm with entomopathogenic nematodes. In: IOBC IWGO conference, Engelberg, Switzerland, 14 to 17 October 2019, p 52

  • FAO (2019) Briefing note on FAO actions on fall armyworm. FAO, Rome. https://www.fao.org/3/a-bs183e.pdf. Accessed 15 Oct 2019

  • Fargues J, Maniania NK, Delmas JC (1994) Infectivity of propagules of Paecilomyces fumosoroseus during in Vitro development to Spodoptera frugiperda. J Invertebr Pathol 64:173–178

    Google Scholar 

  • Faria M, Lopes RB, Souza DA, Wraight SP (2015) Conidial vigor vs. viability as predictors of virulence of entomopathogenic fungi. J Invertebr Pathol 125:68–72

    PubMed  Google Scholar 

  • Farmer B (2019) Fall armyworm marches on as pest that devastated African crops spreads in Asia. https://www.telegraph.co.uk/news/2019/01/09/fall-armyworm-marches-pest-devastated-african-crops-spreads/. Accessed 10 Oct 2019

  • Feldmann F, Rieckmann U, Winter S (2019) The spread of the fall armyworm Spodoptera frugiperda in Africa—what should be done next? J Plant Dis Protect 126:97–101

    Google Scholar 

  • Figueiredo CS, Lemes ARN, Sebastião I, Desidério JA (2019) Synergism of the Bacillus thuringiensis Cry1, Cry2, and Vip3 proteins in Spodoptera frugiperda control. Appl Biochem Biotechnol 188:798–809

    Google Scholar 

  • France A, Yañez M (2010) Effects of fungicides on the development of the entomopathogenicfungus Metarhizium anisopliae VAR anisopliae. Instututo de investigaciones Agropecuarias INIA. Chil J Agric Res 70:390–398

    Google Scholar 

  • Fronza E, Specht A, Heinzen H, De Barros NM (2017) Metarhizium (Nomuraea) rileyi as biological control agent. Biocontrol Sci Technol 27:1243–1264

    Google Scholar 

  • Fuxa JR (1982) Prevalence of viral infections in populations of fall armyworm, Spodoptera frugiperda, in southeastern Louisiana. Environ Entomol 11:239–242

    Google Scholar 

  • García C, Bautista AN (2011) Pathogenicity of isolates of entomopathogenic fungi against Spodoptera frugiperda (Lepidoptera: Noctuidae) and Epilachna varivestis (Coleoptera: Coccinellidae). Colomb Entomol Rev 37:217–222

    Google Scholar 

  • Gardner WA, Sutton RM, Noblet R (1977) Persistence of Beauveria bassiana, Nomuraea rileyi, and Nosema necatrix on soyhean foliage. Environ Entomol 6:616–618

    Google Scholar 

  • Gardner WA, Noblet R, Schwehr RD (1984) The potential of microbial agents in managing populations of the fall armyworm (Lepidoptera: Noctuidae). Fla Entomol 67:325–332

    Google Scholar 

  • Goergen G, Kumar PL, Sankung SB, Togola A, Tamò M (2016) First report of outbreaks of the fall armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera, Noctuidae), a new alien onvasive pest in west and central africa. PLoS ONE 11(10):e0165632

    PubMed  PubMed Central  Google Scholar 

  • Gosselin ME, Bélair G, Simard L, Brodeur J (2009) Toxicity of spinosad and Beauveria bassiana to the black cutworm, and the additivity of subletal doses. Biocontrol Sci Technol 19:201–217

    Google Scholar 

  • Grewal PS, Koppenhöfer AM, Choo HY (2005) Lawn, turfgrass and pasture applications. In: Grewal PS, Ehlers RU, Shapiro-Ilan DI (eds) Nematodes as biocontrol agents. CABI, Wallingford, pp 115–146

    Google Scholar 

  • Grijalba EP, Espinel C, Cuartas PE, Chaparro ML, Villamizar LF (2018) Metarhizium rileyi biopesticide to control Spodoptera frugiperda: stability and insecticidal activity under glasshouse conditions. Fungal Biol 122:1069–1076

    PubMed  Google Scholar 

  • Guo JF, Zhao JZ, He KL, Zhang F, Wang ZY (2018) Potential invasion of the crop-devasting insect pest fall armyworm Spodoptera frugiperda to China. Chin Plant Prot 44:1–10

    Google Scholar 

  • Gutiérrez-Cárdenas OG, Cortez-Madrigal H, Malo EA, Gómez-Ruíz J, Nord R (2019) Physiological and pathogenical characterization of Beauveria bassiana and Metarhizium anisopliae isolates for management of adult Spodoptera frugiperda. Southwest Entomol 44(2):409–421

    Google Scholar 

  • Habib MEM, Patel PN (1990) Pathogenicity of Nomuraea rileyi (Farlow) Samson to larvae of Spodoptera frugiperda (JE Smith, 1797), a pest of corn. Revista de Agr (Piracicaba) 65:83–90

    Google Scholar 

  • Hernandez-Trejo A, Estrada-Drouaillet B, López-Santillán JA, Rios-Velasco C, Varela-Fuentes SE, Rodríguez-Herrera R, Osorio-Hernández E (2019a) In vitro evaluation of native entomopathogenic fungi and neem (Azadiractha indica) extracts on Spodoptera frugiperda. Int J Exp Bot 88:47–54

    Google Scholar 

  • Hernandez-Trejo A, Estrada-Drouaillet B, López-Santillán J, Rios-Velasco A, Rios-Velasco C, Rodríguez-Herrera R, Osorio-Hernández E (2019b) Effects of native entomopathogenic fungal strains and neem extract on Spodoptera frugiperda on maize. Southwest Entomol 44:117–124

    Google Scholar 

  • Hoffmann C, Vanderbruggen H, Höfte H, van Rie J, Jansens S, Van Mellaert H (1998) Specificity of Bacillus thuringiensis deltaendotoxins is correlated with the presence of high-affinity binding sites in the brush border membrane of target insect midguts. Proc Natl Am Sci 85:7844–7848

    Google Scholar 

  • Hoverman JT, Mihaljevic JR, Richgels KL, Kerby JL, Johnson PT (2012) Widespread co-occurrence of virulent pathogens within California amphibian communities. EcoHealth 9(3):288–292

    PubMed  Google Scholar 

  • Hruska AJ (2019) Fall armyworm (Spodoptera frugiperda) management by smallholders. CAB Rev 14:1–11

    Google Scholar 

  • Kaur G, Padmaja V (2009) Relationships among activities of extracellular enzyme production and virulence against Helicoverpa armigera in Beauveria bassiana. J Basic Microb 49:264–274

    CAS  Google Scholar 

  • Jiang YY, Liu J, Xie MC, Li YH, Yang JJ, Zhang ML, Qiu K (2019) Observation on law of diffusion damage of Spodoptera frugiperda in China in 2019. Chin Plant Prot 45(6):10–19

    Google Scholar 

  • Karabörklü S, Azizoglu U, Azizoglu ZB (2018) Recombinant entomopathogenic agents: a review of biotechnological approaches to pest insect control. World J Microbiol Biotechnol 34:14

    Google Scholar 

  • Kebede M, Shimalis T (2018) Out-break, distribution and management of fall armyworm, Spodoptera frugiperda JE smith in Africa: the status and prospects. Acad Agric J 3:551–568

    Google Scholar 

  • Khan MA, Ahmad W (2015) The management of Spodopteran pests using fungal pathogens. In: Sree KS, Varma A (eds) Biocontrol of lepidopteran pests, vol 43, Soil biology. Springer, Cham, pp 123–160

    Google Scholar 

  • Leyva-Hernandez HA, Garcia-Gutiérrez C, Ruiz-Vega J, Calderon-Vazquez CL, Luna-Gonzalez A, Garcia-Salas S (2018) Evaluation of the virulence of Steinernema riobrave and Rhabditis blumi against third instar larvae of Spodoptera frugiperda. Southwest Entomol 43:189–197

    Google Scholar 

  • Lezama-Gutiérrez R, Alatorre-Rosas R, Bojalil-Jaber LF, Molina-Ochoa J, Arenas-Vargas M, Gonzalez-Ramirez M, Rebolledo-Dominguez O (1996) Virulence of five entomopathogenic fungi (Hyphomycetes) against Spodoptera frugiperda (Lepidoptera: Noctuidae) eggs and neonate larvae. Vedalia Revista Internacional de Control Biologico (Mexico) 3:35–39

    Google Scholar 

  • Lezama-Gutiérrez R, Hamm JJ, Molina-Ochoa J, López-Edwards M, Pescador-Rubio A, Gonzalez-Ramirez M, Styer EL (2001) Occurrence of entomopathogens of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Mexican states of Michoacan, Colima, Jalisco and Tamaulipas. Fla Entomol 84:23–30

    Google Scholar 

  • Li GP, Ji TJ, Sun XX, Jiang YY, Wu KM, Feng HQ (2019) Susceptibility evaluation of invaded Spodoptera frugiperda population in Yunan province to five Bt proteins. Chin Plant Prot 45:15–20

    Google Scholar 

  • Liu HM, Hu X, Wang YL, Yang PY, Shu CL, Zhu XM, Zhang J, Sun GZ, Zhang XM, Li Q (2019) Screening for Bacillus thuringiensis strains with high toxicity against Spodoptera frugiperda. Chin J Biol Control 35:721–728

    Google Scholar 

  • Mallapur CP, Naik AK, Hagari S, Praveen T, Patil RK, Lingappa S (2018) Potentiality of Nomuraea rileyi (Farlow) Samson against the fall armyworm, Spodoptera frugiperda (J E Smith) infesting maize. J Entomol Zool Stud 6:1062–1067

    Google Scholar 

  • McKinnon AC, Saari S, Moran-Diez ME, Meyling NV, Raad M, Glare TR (2017) Beauveria bassiana as an endophyte: a critical review on associated methodology and biocontrol potential. BioControl 62(1):1–17

    CAS  Google Scholar 

  • Molina-Ochoa J, Lezama-Gutiérrez R, Gonzalez-Ramirez M, Lopez-Edwards M, Rodriguez-Vega MA, Arceopalacios F (2003) Pathogens and parasitic nematodes associated with populations of fall armyworm (Lepidoptera: Noctuidae) larvae in Mexico. Fla Entomol 86:244–253

    Google Scholar 

  • Monnerat R, Martins E, Queiroz P, Orduz S, Jaramillo G, Benintende GB, Cozzi JG, Real MD, Martinezramirez AC, Rausell C, Ceron J, Ibarra JE, Del Rinconcastro MC, Espinoza AM, Mezabasso L, Cabrera L, Sanchez J, Soberon M (2006) Genetic variability of Spodoptera frugiperda Smith (Lepidoptera: Noctuidae) populations from Latin America is associated with variations in susceptibility to Bacillus thuringiensis Cry toxins. Appl Environ Microb 72:7029–7035

    CAS  Google Scholar 

  • Negrisoli AS, Garcia MS, Negrisoli CRCB (2010a) Compatibility of entomopathogenic nematodes (Nematoda: Rhabditida) with registered insecticides for Spodoptera frugiperda (Smith, 1797) (Lepidoptera: Noctuidae) under laboratory conditions. Crop Prot 29:545–549

    Google Scholar 

  • Negrisoli AS, Garcia MS, Negrisoli CRCB, Bernardi D, da Silva A (2010b) Efficacy of entomopathogenic nematodes (Nematoda: Rhabditida) and insecticide mixtures to control Spodoptera frugiperda (Smith, 1797) (Lepidoptera: Noctuidae) in maize crops. Crop Prot 29:677–683

    Google Scholar 

  • Ordónez-García M, Rios-Velasco C, Berlanga-Reyes DI, Acosta-Muniz CH, Salas-Marina M, Cambero-Campos OJ (2015) Occurrence of natural enemies of Spodoptera frugiperda (Lepidoptera: Noctuidae) in chihuahua, Mexico. Fla Entomol 98:843–847

    Google Scholar 

  • Pavone D, Díaz M, Trujillo L, Dorta B (2009) A granular formulation of nomuraea rileyi farlow (samson) for the control of spodoptera frugiperda (Lepidoptera: Noctuidae). Interciencia 34:130–134

    Google Scholar 

  • Polanczyk RA, Alves SB (2005) Biological parameters of Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae) assayed with Bacillus thuringiensis berliner. Sci Agric 62:464–468

    Google Scholar 

  • Polanczyk RA, Pires da Silva RF, Fiuza LM (2000) Effectiveness of Bacillus thuringiensis strains against Spodoptera frugiperda (Lepidoptera: Noctuidae). Braz J Microbiol 31:165–167

    Google Scholar 

  • Pérez PBMJ (2016) Control efficacy of Spodoptera frugiperda using the entomopathogens Heterorhabditis bacteriophora and Metarhizium anisopliae with insecticide mixtures in corn. Guácimo, Limón

    Google Scholar 

  • Quintela ED, Mascarin GM, da Silva RA, Barrigossi JAF, da Silva Martins JF (2013) Enhanced susceptibility of Tibraca limbativentris (Heteroptera: Pentatomidae) to Metarhizium anisopliae with sublethal doses of chemical insecticides. Biol Control 66:56–64

    CAS  Google Scholar 

  • Ramirez-Rodriguez D, Sánchez-Peña SR (2016) Endophytic Beauveria bassiana in Zea mays: pathogenicity against larvae of fall armyworm, Spodoptera frugiperda. Southwest Entomol 41:875–879

    Google Scholar 

  • Raun ES, Sutter GR, Revelo MA (1966) Ecological factors affecting the pathogenicity of Bacillus thuringiensis var. thuringiensis to the European corn borer and fall armyworm. J Invertebr Pathol 8(3):365–375

    Google Scholar 

  • Richter AR, Fuxa JR (1990) Effect of Steinernema feltiae on Spodoptera frugiperda and Heliothis zea (Lepidoptera: Noctuidae) in corn. J Econ Entomol 83:1286–1291

    Google Scholar 

  • Richter AR, Fuxa JR, Abdel-Fattah M (1987) Effect of host plant on the susceptibility of Spodoptera frugiperda (Lepidoptera: Noctuidae) to a nuclear polyhedrosis viruses. Environ Entomol 16:1004–1006

    Google Scholar 

  • Ríos-Díez JD, Siegfried B, Saldamando-Benjumea CI (2012) Susceptibility of Spodoptera frugiperda (Lepidoptera: Noctuidae) strains from central Colombia to Cry1Ab and Cry1Ac entotoxins of Bacillus thuringiensis. Southwest Entomol 37:281–294

    Google Scholar 

  • Rios-Velasco C, Gallegos-Morales G, Cambero-Campos J, Cerna-Chávez E, Del Rincón-Castro MC, Valenzue-Lagarcia R (2011) Natural enemies of the fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) in Coahuila, México. Fla Entomol 94:723–726

    Google Scholar 

  • Rivero-Borja M, Guzmán-Franco A, Rodríguez-Leyva E, Santillán-Ortega C, Pérez-Panduro A (2018) Interaction of Beauveria bassiana and Metarhizium anisopliae with chlorpyrifos ethyl and spinosad in Spodoptera frugiperda larvae. Pest Manag Sci 74:2047–2052

    CAS  Google Scholar 

  • Romero-Arenas O, Rivera A, Aragon A, Parraguirre C, Cabrera E, Lopez F (2014) Mortality evaluation of armyworm (Spodoptera frugiperda JE Smith) by using Metarhizium anisopliae in vitro. J Pure Appl Algebr 8:59–67

    Google Scholar 

  • Rothman LD, Myers JH (1996) Debilitating effects of viral diseases on host Lepidoptera. J Invertebr Pathol 67:1–10

    Google Scholar 

  • Ruiz-Nájera RE, Ruiz-Estudillo RA, Sánchez-Yáñez JM, Molina-Ochoa J, Skoda SR, Coutinoruiz R, Pintoruiz R, Guevarahernandez F, Foster JE (2013) Occurrence of entomopathogenic fungi and parasitic nematodes on Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae collected in central Chiapas, México. Fla Entomol 96:498–503

    Google Scholar 

  • Rwomushana I, Bateman M, Beale T, Beseh PK, Cameron KH, Chiluba M, Clottey VA, Davis T, Day RK, Early R, Godwin J, Gonzalez-Moreno P, Kansiime MK, Kenis M, Makale F, Mugambi I, Murphy ST, Nunda W, Phiri N, Pratt C, Tambo JA (2018) Fall armyworm: impacts and implications for Africa. Evidence Note Update; CABI, Oxfordshire

  • Salazar-Gutiérrez JD, Castelblanco A, Rodríguez-Bocanegra MX, Teran W, Sáenz-Aponte A (2017) Photorhabdus luminescens subsp. akhurstii SL0708 pathogenicity in Spodoptera frugiperda (Lepidoptera: Noctuidae) and Galleria mellonella (Lepidoptera: Pyralidae). J Asia-Pac Entomol 20:1112–1121

    Google Scholar 

  • Sánchez-Peña SR, Casas-De-Hoyo E, Hernandez-Zul R, Wall KM (2007) A comparison of the activity of soil fungal isolates against three insect pests. J Agric Urban Entomol 24:43–48

    Google Scholar 

  • Santiago IF, Gonçalves VN, Gómez-Silva B, Galetovic A, Rosa LH (2018) Fungal diversity in the Atacama Desert. Antonie Van Leeuwenhoek 111(8):1345–1360

    PubMed  Google Scholar 

  • Sayed AM, Behle RW (2017) Evaluating a dual microbial agent biopesticide with Bacillus thuringiensis var. kurstaki and Beauveria bassiana blastospores. Biocontrol Sci Technol 27:461–474

    Google Scholar 

  • Shylesha AN, Jalali SK, Ankita G, Richa V, Venkatesan T, Ojha R, Ganiger PC, Navik O, Subaharan K, Bakthavatsalam N, Ballal CR (2018) Studies on new invasive pest Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae) and its natural enemies. J Biol Control 32(3):145–151

    Google Scholar 

  • Siebert MW, Tindall KV, Leonard BR, Van Duyn JW, Babcock JM (2008) Evaluation of corn hybrids expressing Cry1F (Herculex® I Insect Protection) against fall armyworm (Lepidoptera: Noctuidae) in the southern United States. J Entomol Sci 43:41–51

    Google Scholar 

  • Silva AB, Beserra EB, Dantas JP (2008) Utilização de Metarhizium anisopliae e extratos vegetais para o controle de Spodoptera frugiperda e Helicoverpa zea (Lepdoptera: Noctuidae) em milho. Eng Ambiental 5:77–85

    Google Scholar 

  • Simmons AM, Rogers CE (1994) Effect of an ectoparasitic nematode, Noctuidonema guyanense, on adult longevity and egg fertility in Spodoptera frugiperda (Lepidoptera: Noctuidae). Biol Control 4(3):285–289

    Google Scholar 

  • Souza ML, Sanchesa MM, de Souzaa DA, Fariaa M, Espinel-Correal C, Sihler W, Lopes RB (2019) Within-host interactions of Metarhizium rileyi strains and nucleopolyhedroviruses in Spodoptera frugiperda and Anticarsia gemmatalis (Lepidoptera: Noctuidae). J Invertebr Pathol 162:10–18

    PubMed  Google Scholar 

  • Storey GK, Gardner WA (1986) Sensitivity of the entomogenous fungus Beauveria bassiana to selected plant growth regulators and spray additives. Appl Environ Microb 52:1–3

    CAS  Google Scholar 

  • Tefera T, Pringle KL (2004) Evaluation of Beauveria bassiana and Metarhizium anisopliae for controlling Chilo partellus (Lepidoptera: Crambidae) in maize. Biocontrol Sci Technol 14:849–853

    Google Scholar 

  • Tefera T, Vidal S (2009) Effect of inoculation method and plant growth medium on endophytic colonization of sorghum by the entomopathogenic fungus Beauveria bassiana. BioControl 54:663–669

    Google Scholar 

  • Tambo JA, Day RK, Lamontagne-Godwin J, Silvestri S, Beseh PK, Oppong-Mensah B, Phir NA, Matimelo M (2019) Tackling fall armyworm (Spodoptera frugiperda) outbreak in Africa: an analysis of farmers’ control actions. Int J Pest Manag 65(4):1–14

    Google Scholar 

  • Tigano-Milani MS, de Faria MR, Lecuona RE, Sartori MR, Arima EY, Diaz BM (1995) Pathogenicity and germination of the fungus Nomuraea rileyi (Farlow) Samson isolated in Brazilian federal district. Anais da sociedade Entomol do Brasi 24:53–60

    Google Scholar 

  • Todd EL, Poole RW (1980) Keys and illustrations for the armyworm moths of the noctuid genus Spodoptera Guenée from the Western hemisphere. Ann Entomol Soc Am 73:722–738

    Google Scholar 

  • Valderrama JAG, Agudelo EJG, Cubillos GPB, Prado AMC, Rivero LFV (2010) Isolation, identification and characterization of native nucleopolyhedrovirus of Spodoptera frugiperda in Colombia. Rev Revista Facultad Nacional de Agronomía Medellín 63:5511–5520

    Google Scholar 

  • Valicente FH, Barreto MR (2003) Bacillus thuringiensis survey in Brazil: geographical distribution and insecticidal activity against Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae). Neotrop Entomol 32:639–644

    Google Scholar 

  • Valicente FH, Lana UGDP (2010) Molecular characterization of the Bacillus thuringiensis (Berliner) strains 344 and 1644, efficient against fall armyworm Spodoptera frugiperda (JE Smith). Rev Bras Milho e Sorgo 7:195–209

    Google Scholar 

  • Villamizar L, Arriero C, Cotes A (2004) Development of preformulated producís based on iiomuraea rileyi for control of Spodoptera frugiperda (Lepidoptera: Moctuidae). Rev Colomb Entomol 30:99–105

    Google Scholar 

  • Viteri DM, Linares AM, Flores L (2018) Use of the entomopathogenic nematode Steinernema carpocapsae in combination with low-toxicity insecticides to control fall armyworm (Lepidoptera: Noctuidae) larvae. Fla Entomol 101:327–330

    CAS  Google Scholar 

  • 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 103:186–199

    CAS  PubMed  Google Scholar 

  • Yang F, Kerns DL, Brown S, Kurtz R, Dennehy T, Braxton B, Head G, Huang FN (2016) Performance and cross-crop resistance of Cry1F-maize selected Spodoptera frugiperda on transgenic Bt cotton: implications for resistance management. Sci Rep 6:28059

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zamora R, Markelyn J (2019) Caracterización de aislados nativos de nematodos entomopatógenos y uso potencial contra Spodoptera frugiperda. Diss Universidad Nacional Agraria. https://repositorio.una.edu.ni/3830/

  • Zhang L, Jin MH, Zhang DD, Jiang YY, Liu J, Wu KM, Xiao YT (2019) Molecular identification of invasive fall armyworm Spodoptera frugiperda in Yunnan province. Chin Plant Prot 45:19–24

    Google Scholar 

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Acknowledgements

This research was supported by The Agricultural Science and Technology Innovation Program (CAAS-ZDRW202007) and China Agriculture Research System (CARS-02).

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Correspondence to Dirk Babendreier or Zhenying Wang.

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Guo, J., Wu, S., Zhang, F. et al. Prospects for microbial control of the fall armyworm Spodoptera frugiperda: a review. BioControl 65, 647–662 (2020). https://doi.org/10.1007/s10526-020-10031-0

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