The endophytic fungi from South Sumatra (Indonesia) and their pathogenecity against the new invasive fall armyworm, Spodoptera frugiperda
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Abstract. Gustianingtyas M, Herlinda S, Suwandi. 2021. The endophytic fungi from South Sumatra (Indonesia) and their pathogenicity against the new invasive fall armyworm, Spodoptera frugiperda. Biodiversitas 22: 1051-1062. Maize in Indonesia is currently experiencing attacks and outbreaks of the new invasive fall armyworm, Spodoptera frugiperda. The S. frugiperda larvae emerge from the leaf midrib when eating, after hiding in the maize stalk so that it is difficult to control by contact. This study aimed to find out the endophytic fungi from the roots of maize, banana and chili in South Sumatra and to determine their pathogenicity against S. frugiperda larvae. The endophytic fungi were isolated from the plant roots. Fungal isolates proven to be endophytic were dropped (1 × 106 conidia mL?1) on the second instar larvae. The result showed that the endophytic fungi found were 8 isolates consisting of the genus, Aspergillus sp., Beauveria sp., Chaetomium sp., and Curvularia sp. First report of Aspergillus sp., Chaetomium sp., and Curvularia sp. have insecticidal activity against S. frugiperda larvae. However, the two most pathogenic isolates were JgCrJr and JgSPK isolates of Beauveria sp. with larval mortality of 29.33% and 26.67%, respectively, and could reduce the emergence of S. frugiperda adults up to 44%. So, the two isolates of Beauveria sp. have a high potential to be developed to control S. frugiperda larvae in maize both in the lowlands and the highlands.
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References
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Ayudya DR, Herlinda S, Suwandi S. 2019. Insecticidal activity of culture filtrates from liquid medium of Beauveria bassiana isolates from South Sumatra (Indonesia) wetland soil against larvae of Spodoptera litura. Biodiversitas 20: 2101–2109. DOI: 10.13057/biodiv/d200802.
Bamisile BS, Akutse KS, Dash CK, Qasim M, Aguila LCR, Ashraf HJ, et al. 2020. Effects of seedling age on colonization patterns of citrus limon plants by endophytic Beauveria bassiana and Metarhizium anisopliae and their influence on seedlings growth. J Fungi 6: 1–15. DOI: 10.3390/jof6010029.
Bamisile BS, Dash CK, Akutse KS, Qasim M, Aguila LCR, Wang F, et al. 2019. Endophytic Beauveria bassiana in foliar-treated citrus limon plants acting as a growth suppressor to three successive generations of Diaphorina citri Kuwayama (Hemiptera: Liviidae). Insects 10: 1–15. DOI: 10.3390/insects10060176.
Barra-Bucarei L, González MG, Iglesias AF, Aguayo GS, Peñalosa MG, Vera PV. 2020. Beauveria bassiana multifunction as an endophyte: growth promotion and biologic control of Trialeurodes vaporariorum, (Westwood) (Hemiptera: Aleyrodidae) in tomato. Insects 11: 1–15. DOI: 10.3390/insects11090591
Bateman ML, Day RK, Luke B, Edgington S, Kuhlmann U, Cock MJW. 2018. Assessment of potential biopesticide options for managing fall armyworm (Spodoptera frugiperda) in Africa. J Appl Entomol 142: 805-819. DOI: 10.1111/jen.12565.
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De Groote H, Kimenju SC, Munyua B, Palmas S, Kassie M, Bruce A. 2020. Spread and impact of fall armyworm (Spodoptera frugiperda J.E. Smith) in maize production areas of Kenya. Agric Ecosyst Environ 292: 1–10. DOI: 10.1016/j.agee.2019.106804.
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Gutiérrez-moreno R, Mota-sanchez D, Blanco CA, Whalon ME, Terán-santofimio H, Rodriguez-maciel JC, et al. 2018. Field-evolved resistance of the fall armyworm (Lepidoptera: Noctuidae) to synthetic insecticides in Puerto Rico and Mexico. J Econ Entomol 20: 1–11. DOI: 10.1093/jee/toy372.
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Herlinda S, Octariati N, Suwandi S. 2020b. Exploring entomopathogenic fungi from South Sumatra (Indonesia) soil and their pathogenicity against a new invasive maize pest, Spodoptera frugiperda. Biodiversitas 21: 2955–2965. DOI: 10.13057/biodiv/d210711.
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Hutasoit RT, Kalqutny SH, Widiarta IN. 2020. Spatial distribution pattern, bionomic, and demographic parameters of a new invasive species of armyworm Spodoptera frugiperda (Lepidoptera?; Noctuidae) in maize of South Sumatra, Indonesia. Biodiversitas 21: 3576–3582. DOI: 10.13057/biodiv/d210821.
Jaber LR, Ownley BH. 2018. Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biol Control 116: 36–45. DOI: 10.1016/j.biocontrol.2017.01.018.
Jones S, Behie SW, Jones SJ, Bidochka MJ, Hyde K. 2018. Plant tissue localization of the endophytic insect pathogenic fungi ScienceDirect Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria. Fungal Ecol 13: 112–119. DOI: 10.1016/j.funeco.2014.08.001.
Kasambala T, Vega FE, Klingen I. 2018. Establishment of the fungal entomopathogen Beauveria bassiana as anendophyte in sugarcane, Saccharum officinarum. Fungal Ecol 35: 70–77. DOI: 10.1016/j.funeco.2018.06.008.
Lestari P, Budiarti A, Fitriana Y, Susilo FX, Swibawa IG. 2020. Identification and genetic diversity of Spodoptera frugiperda in Lampung Province , Indonesia. Biodiversitas 21: 1670–1677. DOI: 10.13057/biodiv/d210448.
Lira AC de, Mascarin GM, Júnior ID. 2020. Microsclerotia production of Metarhizium spp. for dual role as plant biostimulant and control of Spodoptera frugiperda through corn seed coating. Fungal Biol 124: 689–699. DOI: 10.1016/j.funbio.2020.03.011.
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Mancillas-Paredes J., Hernández-Sánchez H, Jaramillo-Flores ME, García-Gutiérrez C. 2019. Proteases and chitinases induced in Beauveria bassiana during infection by Zabrotes subfasciatus. Southwest Entomol 44: 125–137. DOI: 10.3958/059.044.0114.
Montezano DG, Specht A, Sosa-gómez DR, Brasília U De. 2018. Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. African Entomol 26: 286–300. DOI: 10.4001/003.026.0286.
Nagoshi RN, Fleischer S, Meagher RL, Hay-roe M, Silvie P, Vergara C, et al. 2017. Fall armyworm migration across the Lesser Antilles and the potential for genetic exchanges between North and South American populations. PLoS One 12: 1–18. DOI: 10.1371/journal. pone.0171743.
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Qi G, Lan N, Ma X, Yu Z, Zhao X. 2011. Controlling Myzus persicae with recombinant endophytic fungi Chaetomium globosum expressing Pinellia ternata agglutinin using recombinant endophytic fungi to control aphids. J Appl Microbiol 110: 1314–1322. DOI: 10.1111/j.1365-2672.2011.04985.x.
Ramanujam B, Poornesha B, Shylesha AN. 2020. Effect of entomopathogenic fungi against invasive pest Spodoptera frugiperda (J.E. Smith) (Lepidoptera?: Noctuidae) in maize. Egypt J Biol Pest Control 30: 1–5. DOI: 10.1186/s41938-020-00291-4.
Ramirez-Rodriguez D, Sánchez-Peña SR. 2016. Endophytic Beauveria bassiana in Zea mays: pathogenicity against larvae of fall armyworm, Spodoptera frugiperda. Southwest Entomol Sci Note 41: 875–878.
Ramos Y, Taibo AD, Jiménez JA, Portal O. 2020. Endophytic establishment of Beauveria bassiana and Metarhizium anisopliae in maize plants and its effect against Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) larvae. Egypt J Biol Pest Control 30: 1–6. DOI: 10.1186/s41938-020-00223-2.
Renuka S, Ramanujam B, Poornesha B. 2016. Endophytic ability of different isolates of entomopathogenic fungi Beauveria bassiana (Balsamo) Vuillemin in stem and leaf tissues of maize (Zea mays L.). Indian J Microbiol 56: 126–133. DOI: 10.1007/s12088-016-0574-8.
Resquín-Romero G, Garrido-Jurado I, Delso C, Ríos-Moreno A, Quesada-Moraga E. 2016. Transient endophytic colonizations of plants improve the outcome of foliar applications of mycoinsecticides against chewing insects. J Invertebr Pathol 136: 23–31. DOI: 10.1016/j.jip.2016.03.003.
Russo ML, Jaber LR, Scorsetti AC, Vianna F, Cabello MN, Pelizza SA. 2020. Effect of entomopathogenic fungi introduced as corn endophytes on the development , reproduction , and food preference of the invasive fall armyworm Spodoptera frugiperda. J Pest Sci 93: 1–12. DOI: 10.1007/s10340-020-01302-x.
Sartiami D, Dadang, Harahap I, Kusumah Y, Anwar R. 2020. First record of fall armyworm (Spodoptera frugiperda) in Indonesia and its occurence in three provinces. In: IOP Conf. Ser.: Earth Environ. Sci. 468 012021. pp 1–8. DOI: 10.1088/1755-1315/468/1/012021.
Shikano I. 2018. Evolutionary ecology of multitrophic interactions between plants, insect herbivores and entomopathogens. J Chem Ecol 43: 586–598. DOI: 10.1007/s10886-017-0850-z.
Silva LF, Freire KTLS, Araújo-Magalhães GR, Agamez-Montalvo GS, Sousa MA, Costa-Silva TA, et al. 2018. Penicillium and Talaromyces endophytes from Tillandsia catimbauensis, a bromeliad endemic in the Brazilian tropical dry forest, and their potential for l-asparaginase production. World J Microbiol Biotechnol 34: 1–12. DOI: /10.1007/s11274-018-2547-z,
Sumikarsih E, Herlinda S, Pujiastuti Y. 2019. Conidial density and viability of Beauveria bassiana isolates from Java and Sumatra and their virulence against Nilaparvata lugens at different temperatures. Agrivita 41: 335–349. DOI: 10.17503/agrivita.v41i2.2105.
Tambo JA, Day RK, Lamontagne-godwin J, Silvestri S, Beseh PK, Oppong-mensah B, et al. 2020. Tackling fall armyworm (Spodoptera frugiperda) outbreak in Africa: an analysis of farmers’ control actions. Int J Pest Manag 66: 298–310. DOI: /10.1080/09670874.2019.1646942.
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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: 626–634. DOI: 10.1111/jen.12634.
Assaf LH, Haleema RA, Abdullah SK. 2011. Association of entomopathogenic and other opportunistic fungi. Jordan J Biol Sci 4: 87–92.
Ayudya DR, Herlinda S, Suwandi S. 2019. Insecticidal activity of culture filtrates from liquid medium of Beauveria bassiana isolates from South Sumatra (Indonesia) wetland soil against larvae of Spodoptera litura. Biodiversitas 20: 2101–2109. DOI: 10.13057/biodiv/d200802.
Bamisile BS, Akutse KS, Dash CK, Qasim M, Aguila LCR, Ashraf HJ, et al. 2020. Effects of seedling age on colonization patterns of citrus limon plants by endophytic Beauveria bassiana and Metarhizium anisopliae and their influence on seedlings growth. J Fungi 6: 1–15. DOI: 10.3390/jof6010029.
Bamisile BS, Dash CK, Akutse KS, Qasim M, Aguila LCR, Wang F, et al. 2019. Endophytic Beauveria bassiana in foliar-treated citrus limon plants acting as a growth suppressor to three successive generations of Diaphorina citri Kuwayama (Hemiptera: Liviidae). Insects 10: 1–15. DOI: 10.3390/insects10060176.
Barra-Bucarei L, González MG, Iglesias AF, Aguayo GS, Peñalosa MG, Vera PV. 2020. Beauveria bassiana multifunction as an endophyte: growth promotion and biologic control of Trialeurodes vaporariorum, (Westwood) (Hemiptera: Aleyrodidae) in tomato. Insects 11: 1–15. DOI: 10.3390/insects11090591
Bateman ML, Day RK, Luke B, Edgington S, Kuhlmann U, Cock MJW. 2018. Assessment of potential biopesticide options for managing fall armyworm (Spodoptera frugiperda) in Africa. J Appl Entomol 142: 805-819. DOI: 10.1111/jen.12565.
Bentivenha JPF, Baldin ELL, Montezano DG, Hunt TE, Paula-Moraes S V. 2017. Attack and defense movements involved in the interaction of Spodoptera frugiperda and Helicoverpa zea (Lepidoptera: Noctuidae). J Pest Sci 90: 433–445. DOI: 10.1007/s10340-016-0802-3.
Boaventura D, Martin M, Pozzebon A, Mota-sanchez D, Nauen R. 2020. Monitoring of target-site mutations conferringinsecticide resistance in Spodoptera frugiperda. Insects 11: 1–11. DOI: 10.3390/insects11080545.
Carolina A, Silva L, Silva GA, Henrique P, Abib N, Carolino AT, et al. 2020. Endophytic colonization of tomato plants by the entomopathogenic fungus Beauveria bassiana for controlling the South American tomato pinworm, Tuta absoluta. CABI Agric Biosci 1: 1–9. DOI: 10.1186/s43170-020-00002-x.
El-Ghany TMA. 2015. Entomopathogenic Fungi and their Role in Biological Control. Biology Department Faculty of Science Jazan University KSA: Cairo. DOI: 10.4172/978-1-63278-065-2-66.
Elfita, Mardiyanto, Fitrya, Larasati JE, Julinar, Widjajanti H, et al. 2019. Antibacterial activity of Cordyline fruticosa leaf extracts and its endophytic fungi extracts. Biodiversitas 20: 3804–3812. DOI: 10.13057/biodiv/d201245
Fernandes EKK, Rangel DEN, Moraes AM., Bittencourt VREP, Roberts DW. 2007. Variability in tolerance to UV-B radiation among Beauveria spp. isolates. J Invertebr Pathol 96: 237?243. DOI: 0.1016/j.jip.2007.05.007.
Flagel L, Lee YW, Wanjugi H, Swarup S, Brown A, Kraft E, et al. 2018. Mutational disruption of the ABCC2 gene in fall armyworm, Spodoptera frugiperda, confers resistance to the Cry1Fa and Cry1A. Sci Rep 8: 1–11. DOI: 10.1038/s41598-018-25491-9.
Ginting S, Zarkani A, Wibowo RH, Sipriyadi. 2020. New invasive pest, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) attacking corn in Bengkulu, Indonesia. Serangga 25: 105–117.
De Groote H, Kimenju SC, Munyua B, Palmas S, Kassie M, Bruce A. 2020. Spread and impact of fall armyworm (Spodoptera frugiperda J.E. Smith) in maize production areas of Kenya. Agric Ecosyst Environ 292: 1–10. DOI: 10.1016/j.agee.2019.106804.
Gustianingtyas M, Herlinda S, Suwandi, Suparman, Hamidson H, Hasbi, et al. 2020. Toxicity of entomopathogenic fungal culture filtrate of lowland and highland soil of South Sumatra (Indonesia) against Spodoptera litura larvae. Biodiversitas 21: 1839–1849. DOI: 10.13057/biodiv/d210510.
Gutiérrez-moreno R, Mota-sanchez D, Blanco CA, Whalon ME, Terán-santofimio H, Rodriguez-maciel JC, et al. 2018. Field-evolved resistance of the fall armyworm (Lepidoptera: Noctuidae) to synthetic insecticides in Puerto Rico and Mexico. J Econ Entomol 20: 1–11. DOI: 10.1093/jee/toy372.
Herlinda S, Efendi RA, Suharjo R, Hasbi, Setiawan A, Elfita, et al. 2020a. New emerging entomopathogenic fungi isolated from soil in South Sumatra (Indonesia) and their filtrate and conidial insecticidal activity against Spodoptera litura. Biodiversitas 21: 5102–5113. DOI: 10.13057/biodiv/d211115.
Herlinda S, Octariati N, Suwandi S. 2020b. Exploring entomopathogenic fungi from South Sumatra (Indonesia) soil and their pathogenicity against a new invasive maize pest, Spodoptera frugiperda. Biodiversitas 21: 2955–2965. DOI: 10.13057/biodiv/d210711.
Humber RA. 2005. Entomopathogenic Fungal Identification. USDA-ARS Plant Protection Research Unit: Ithaca.
Hutasoit RT, Kalqutny SH, Widiarta IN. 2020. Spatial distribution pattern, bionomic, and demographic parameters of a new invasive species of armyworm Spodoptera frugiperda (Lepidoptera?; Noctuidae) in maize of South Sumatra, Indonesia. Biodiversitas 21: 3576–3582. DOI: 10.13057/biodiv/d210821.
Jaber LR, Ownley BH. 2018. Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biol Control 116: 36–45. DOI: 10.1016/j.biocontrol.2017.01.018.
Jones S, Behie SW, Jones SJ, Bidochka MJ, Hyde K. 2018. Plant tissue localization of the endophytic insect pathogenic fungi ScienceDirect Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria. Fungal Ecol 13: 112–119. DOI: 10.1016/j.funeco.2014.08.001.
Kasambala T, Vega FE, Klingen I. 2018. Establishment of the fungal entomopathogen Beauveria bassiana as anendophyte in sugarcane, Saccharum officinarum. Fungal Ecol 35: 70–77. DOI: 10.1016/j.funeco.2018.06.008.
Lestari P, Budiarti A, Fitriana Y, Susilo FX, Swibawa IG. 2020. Identification and genetic diversity of Spodoptera frugiperda in Lampung Province , Indonesia. Biodiversitas 21: 1670–1677. DOI: 10.13057/biodiv/d210448.
Lira AC de, Mascarin GM, Júnior ID. 2020. Microsclerotia production of Metarhizium spp. for dual role as plant biostimulant and control of Spodoptera frugiperda through corn seed coating. Fungal Biol 124: 689–699. DOI: 10.1016/j.funbio.2020.03.011.
Machado BB, Orue JPM, Arruda MS, Santos C V., Sarath DS, Goncalves WN, et al. 2016. BioLeaf: A professional mobile application to measure foliar damage caused by insect herbivory. Comput Electron Agric 129: 44–55. DOI: 10.1016/j.compag.2016.09.007.
Mancillas-Paredes J., Hernández-Sánchez H, Jaramillo-Flores ME, García-Gutiérrez C. 2019. Proteases and chitinases induced in Beauveria bassiana during infection by Zabrotes subfasciatus. Southwest Entomol 44: 125–137. DOI: 10.3958/059.044.0114.
Montezano DG, Specht A, Sosa-gómez DR, Brasília U De. 2018. Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. African Entomol 26: 286–300. DOI: 10.4001/003.026.0286.
Nagoshi RN, Fleischer S, Meagher RL, Hay-roe M, Silvie P, Vergara C, et al. 2017. Fall armyworm migration across the Lesser Antilles and the potential for genetic exchanges between North and South American populations. PLoS One 12: 1–18. DOI: 10.1371/journal. pone.0171743.
Otim MH, Tay WT, Walsh TK, Kanyesigye D, Adumo S, Abongosi J, et al. 2018. Detection of sister-species in invasive populations of the fall armyworm Spodoptera frugiperda (Lepidoptera?: Noctuidae) from Uganda. PLoS One 13: 1–18. DOI: 10.1371/journal.pone.0194571.
Qi G, Lan N, Ma X, Yu Z, Zhao X. 2011. Controlling Myzus persicae with recombinant endophytic fungi Chaetomium globosum expressing Pinellia ternata agglutinin using recombinant endophytic fungi to control aphids. J Appl Microbiol 110: 1314–1322. DOI: 10.1111/j.1365-2672.2011.04985.x.
Ramanujam B, Poornesha B, Shylesha AN. 2020. Effect of entomopathogenic fungi against invasive pest Spodoptera frugiperda (J.E. Smith) (Lepidoptera?: Noctuidae) in maize. Egypt J Biol Pest Control 30: 1–5. DOI: 10.1186/s41938-020-00291-4.
Ramirez-Rodriguez D, Sánchez-Peña SR. 2016. Endophytic Beauveria bassiana in Zea mays: pathogenicity against larvae of fall armyworm, Spodoptera frugiperda. Southwest Entomol Sci Note 41: 875–878.
Ramos Y, Taibo AD, Jiménez JA, Portal O. 2020. Endophytic establishment of Beauveria bassiana and Metarhizium anisopliae in maize plants and its effect against Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) larvae. Egypt J Biol Pest Control 30: 1–6. DOI: 10.1186/s41938-020-00223-2.
Renuka S, Ramanujam B, Poornesha B. 2016. Endophytic ability of different isolates of entomopathogenic fungi Beauveria bassiana (Balsamo) Vuillemin in stem and leaf tissues of maize (Zea mays L.). Indian J Microbiol 56: 126–133. DOI: 10.1007/s12088-016-0574-8.
Resquín-Romero G, Garrido-Jurado I, Delso C, Ríos-Moreno A, Quesada-Moraga E. 2016. Transient endophytic colonizations of plants improve the outcome of foliar applications of mycoinsecticides against chewing insects. J Invertebr Pathol 136: 23–31. DOI: 10.1016/j.jip.2016.03.003.
Russo ML, Jaber LR, Scorsetti AC, Vianna F, Cabello MN, Pelizza SA. 2020. Effect of entomopathogenic fungi introduced as corn endophytes on the development , reproduction , and food preference of the invasive fall armyworm Spodoptera frugiperda. J Pest Sci 93: 1–12. DOI: 10.1007/s10340-020-01302-x.
Sartiami D, Dadang, Harahap I, Kusumah Y, Anwar R. 2020. First record of fall armyworm (Spodoptera frugiperda) in Indonesia and its occurence in three provinces. In: IOP Conf. Ser.: Earth Environ. Sci. 468 012021. pp 1–8. DOI: 10.1088/1755-1315/468/1/012021.
Shikano I. 2018. Evolutionary ecology of multitrophic interactions between plants, insect herbivores and entomopathogens. J Chem Ecol 43: 586–598. DOI: 10.1007/s10886-017-0850-z.
Silva LF, Freire KTLS, Araújo-Magalhães GR, Agamez-Montalvo GS, Sousa MA, Costa-Silva TA, et al. 2018. Penicillium and Talaromyces endophytes from Tillandsia catimbauensis, a bromeliad endemic in the Brazilian tropical dry forest, and their potential for l-asparaginase production. World J Microbiol Biotechnol 34: 1–12. DOI: /10.1007/s11274-018-2547-z,
Sumikarsih E, Herlinda S, Pujiastuti Y. 2019. Conidial density and viability of Beauveria bassiana isolates from Java and Sumatra and their virulence against Nilaparvata lugens at different temperatures. Agrivita 41: 335–349. DOI: 10.17503/agrivita.v41i2.2105.
Tambo JA, Day RK, Lamontagne-godwin J, Silvestri S, Beseh PK, Oppong-mensah B, et al. 2020. Tackling fall armyworm (Spodoptera frugiperda) outbreak in Africa: an analysis of farmers’ control actions. Int J Pest Manag 66: 298–310. DOI: /10.1080/09670874.2019.1646942.
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