Exploring entomopathogenic fungi from South Sumatra (Indonesia) soil and their pathogenicity against a new invasive maize pest, Spodoptera frugiperda
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Abstract. Herlinda S, Octariati N, Suwandi S, Hasbi. 2020. Exploring entomopathogenic fungi from South Sumatra (Indonesia) soil and their pathogenicity against a new invasive maize pest, Spodoptera frugiperda. Biodiversitas 21: 2955-2965. Fall armyworm (Spodoptera frugiperda) is a new invasive maize pest in Indonesia that can cause maize yield losses of 18 million tons/year. To overcome the pest, local-specific entomopathogenic fungi are needed. This study aimed to explore entomopathogenic fungi from soil in South Sumatra and to determine their pathogenicity against S. frugiperda larvae. The fungi exploration was carried out in the lowlands and highlands of South Sumatra and the pathogenicity of obtained isolates were tested against the third instar larvae. The entomopathogenic fungi found were Metarhizium spp. and were successfully isolated as many as 14 isolates. All of the isolates were pathogenic to S. frugiperda larvae (70.67?78.67% mortality), the most pathogenic caused 78.67% mortality and significantly suppressed the emergence of adults up to 81.2%. Unhealthy larvae had a dry, shrunken, shrinking, odorless body, and its integument was covered in mycelia and conidia like yellowish-white powdery mixed with dark green. The unhealthy pupae and adults were in the abnormal and malformation shape. The abnormal pupae were shorter in size, bent, the to-be wings got wrinkled, and darker color, while the unhealthy adults had folded wings and were unable to fly. The two most pathogenic isolates were found from the lowland (PirOI) and highland (CasPsPGA) soil of South Sumatra. In conclusion, both of these isolates had the potential to be developed into local-specific mycoinsecticides to control pest insects in the highlands and/or lowlands in Indonesia.
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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). Journal of Applied Entomology 143: 626–634. DOI:10.1111/jen.12634.
Altre JA, Vandenberg JD. 2001. Factors influencing the infectivity of isolates of Paecilomyces fumosoroseus against diamondback moth, Plutella xylostella. Journal of Invertebrate Pathology 78: 31–36. DOI:10.1006/jipa.2001.5043.
Anwar W, Khan SN, Aslam M, Haider MS, Shahid AA, Ali M. 2015. Exploring fungal flora associated with insects of cotton agroecological zones of Punjab, Pakistan. Pakistan Entomologist 37: 27–31.
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.
Chen WH, Han YF, Liang JD, Liang ZQ. 2019. Morphological and phylogenetic characterization of novel Metarhizium species in Guizhou, China. Phytotaxa 419: 189–196. DOI:10.11646/phytotaxa.419.2.5.
Chen Z, Xu L, Yang F, Ji G, Yang J, Wang J. 2014. Efficacy of Metarhizium anisopliae isolate MAX-2 from Shangri-la, China under desiccation stress. BMC Microbiology 14: 1–8. DOI: 1471-2180/14/4.
Early R, González-Moreno P, Murphy ST, Day R. 2018. Forecasting the global extent of invasion of the cereal pest Spodoptera frugiperda, the fall armyworm. NeoBiota 40: 25–50. DOI: 10871/34861.
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.
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: 10.1016/j.jip.2007.05.007
Ganiger PC, Yeshwanth HM, Muralimohan K, Vinay N, Kumar ARV, Chandrashekara K. 2018. Occurrence of the new invasive pest, fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), in the maize fields of Karnataka, India. Current Science 115: 621–623.
Goergen G, Kumar PL, Sankung SB, Togola A, Tam M. 2016. First report of outbreaks of the fall armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera , Noctuidae), a new alien invasive pest in West and Central Africa. Plos One 11: 1–9. DOI:10.1371/journal.pone.0165632
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. Agriculture, Ecosystems and Environment 292: 1–10. DOI:10.1016/j.agee.2019.106804.
Gustianingtyas M, Herlinda S, Hamidson H. 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-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. Southwestern Entomologist 44: 409–421. DOI: 10.3958/059.044.0206
Harrison RD, Thierfelder C, Baudron F, Chinwada P, Midega C, Scha U, Berg J Van Den. 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. DOI: 10.1016/j.jenvman.2019.05.011
Hernandez-Trejo A, Estrada-Drouaillet B, López-Santillán J, Rios-Velasco C, Varela-Fuentes S, Rodríguez-Herrera R, Osorio-Hernández E. 2019. In vitro evaluation of native entomopathogenic fungi and neem (Azadiractha indica) extracts on Spodoptera frugiperda. International Journal of Experimental Botany 4: 75–84. DOI: 1037//0033-2909.I26.1.78.
Humber RA. 2005. Entomopathogenic Fungal Identification. USDA-ARS Plant Protection Research Unit: Ithaca.
IPPC. 2019. The Occurence of Fall Armyworm (Spodoptera frugiperda) in Indonesia. IPPC (International Plant Protection Convention) Official Pest Report, No. IDN-04/1. Rome, Italy: FAO. https://www.ippc.int/
Kalvnadi E, Mirmoayedi A, Alizadeh M, Pourian HR. 2018. Sub-lethal concentrations of the entomopathogenic fungus, Beauveria bassiana increase fitness costs of Helicoverpa armigera (Lepidoptera: Noctuidae) offspring. Journal of Invertebrate Pathology 158: 32–42. DOI: 10.1016/j.jip.2018.08.012.
Karthikeyan A, Shanthi V, Nagasathya A. 2008. Effect of different media and pH on the growth of Beauveria bassiana and its parasitism on leaf eating caterpillars. Res J Agric Biol Sci 4: 117–119.
Kumela T, Simiyu J, Sisay B, Likhayo P, Gohole L, Tefera T. 2018. Farmers knowledge, perceptions, and management practices of the new invasive pest, fall armyworm (Spodoptera frugiperda) in Ethiopia and Kenya. International Journal of Pest Management 65: 1–9. DOI: 10.1080/09670874.2017.1423129
Lestari P, Budiarti A, Fitriana Y, Susilo FX, Swibawa IG. 2020. Identification and genetic diversity of Spodoptera frugiperda in Lampung Province, Indonesia. 21: 1670–1677. DOI: 10.13057/biodiv/d210448.
Lopes RB, Souza DA, Rocha LFN, Montalva C, Luz C, Humber RA, Faria M. 2018. Metarhizium alvesii sp. nov.: A new member of the Metarhizium anisopliae species complex. Journal of Invertebrate Pathology 151: 165–168. DOI: 10.1016/j.jip.2017.12.001.
Machado BB, Orue JPM, Arruda MS, Santos C V., Sarath DS, Goncalves WN, Silva GG, Pistori H, Roel AR, Rodrigues-Jr JF. 2016. BioLeaf: A professional mobile application to measure foliar damage caused by insect herbivory. Computers and Electronics in Agriculture 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. Southwestern Entomol 44: 125–137. DOI: 10.3958/059.044.0114.
Montezano DG, Specht A, Sosa-gómez DR, Brasília UD. 2018. Host plants of Spodoptera frugiperda (Lepidoptera?: Noctuidae) in the Americas. African Entomology 26: 286–300. DOI: 10.4001/003.026.0286
Nagoshi RN, Fleischer S, Meagher RL, Hay-roe M, Silvie P, Vergara C, Westbrook J, Khan A, Muru MG, Silvie P, Vergara C, Westbrook J. 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
Nboyine JA, Kusi F, Abudulai M, Badii BK, Zakaria M, Adu GB, Haruna A, Seidu A, Osei V, Alhassan S, Yahaya A. 2020. A new pest, Spodoptera frugiperda (J.E. Smith), in tropical Africa: Its seasonal dynamics and damage in maize fields in northern Ghana. Crop Protection 127: 1–7. DOI: 10.1016/j.cropro.2019.104960.
Ngangambe MH, Mwatawala MW. 2020. Effects of entomopathogenic fungi (EPFs) and cropping systems on parasitoids of fall armyworm (Spodoptera frugiperda) on maize in eastern central, Tanzania. Biocontrol Science and Technology 30: 1–13. DOI: 10.1080/09583157.2020.1726878.
Otim MH, Tay WT, Walsh TK, Kanyesigye D, Adumo S, Abongosi J, Ochen S, Sserumaga J, Alibu S, Abalo G, Asea G, Agona A. 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
Prabawati G, Herlinda S, Pujiastuti Y. 2019. The abundance of canopy arthropods in South Sumatra (Indonesia) freshwater swamp main and ratooned rice applied with bioinsecticides and synthetic insecticide. Biodiversitas 20: 2921–2930. DOI: 10.13057/biodiv/d201021.
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. Egyptian Journal of Biological Pest Control 30: 1–6. DOI: 10.1186/s41938-020-00223-2.
Rivero-Borja M, Guzmán-Franco AW, 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 Management Science 74: 2047–2052. DOI: 10.1002/ps.4884.
Safitri A, Herlinda S, Setiawan A. 2018. Entomopathogenic fungi of soils of freshwater swamps, tidal lowlands, peatlands, and highlands of South Sumatra, Indonesia. Biodiversitas 19: 2365–2373. DOI: 10.13057/biodiv/d190647
Sharma L, Oliveira I, Torres L, Marques G. 2018. Entomopathogenic fungi in Portuguese vineyards soils: suggesting a ‘Galleria-Tenebrio-bait method’ as bait-insects Galleria and Tenebrio significantly underestimate the respective recoveries of Metarhizium (robertsii) and Beauveria (bassiana). MycoKeys 23: 1–23. DOI: 10.3897/mycokeys.38.26970.
Shylesha AN, Jalali SK, Gupta A, Varshney R, Venkatesan T. 2018. Studies on new invasive pest Spodoptera frugiperda (J .E . Smith) (Lepidoptera: Noctuidae) and its natural enemies. Journal of Biological Control 32: 145–151. DOI: 10.18311/jbc/2018/21707
Souza ML, Sanches MM, Souza DA de, Faria 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). Journal of Invertebrate Pathology 162: 10–18. DOI: 10.1016/j.jip.2019.01.006.
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
Thaochan N, Sausa-Ard W. 2017. Occurrence and effectiveness of indigenous Metarhizium anisopliae against adults Zeugodacus cucurbitae (Coquillett) (Diptera: Tephritidae) in Southern Thailand. Songklanakarin Journal of Science and Technology 39: 325–334. DOI:10.14456/sjst-psu.2017.35.
Wilson WM, Ibarra JE, Oropeza A, Hernández MA, Toledo-Hernández RA, Toledo J. 2020. Infection of Anastrepha ludens (Diptera: Tephritidae) adults during emergence from soil treated with Beauveria bassiana under various texture, humidity, and temperature conditions. Florida Entomologist 100: 503–508. DOI: 10.1653/024.100.0302.
Wu X, Zhang L, Yang C, Zong M, Huang Q, Tao L. 2016. Detection on emamectin benzoate-induced apoptosis and DNA damage in Spodoptera frugiperda Sf-9 cell line. Pesticide Biochemistry and Physiology 126: 6–12. DOI: 10.1016/j.pestbp.2015.06.009
Yang M, Wang B, Gao J, Zhang Y, Xu W, Tao L. 2017. Chemosphere spinosad induces programmed cell death involves mitochondrial dysfunction and cytochrome C release in Spodoptera frugiperda Sf9 cells. Chemosphere 169: 155–161. DOI: 10.1016/j.chemosphere.2016.11.065
Altre JA, Vandenberg JD. 2001. Factors influencing the infectivity of isolates of Paecilomyces fumosoroseus against diamondback moth, Plutella xylostella. Journal of Invertebrate Pathology 78: 31–36. DOI:10.1006/jipa.2001.5043.
Anwar W, Khan SN, Aslam M, Haider MS, Shahid AA, Ali M. 2015. Exploring fungal flora associated with insects of cotton agroecological zones of Punjab, Pakistan. Pakistan Entomologist 37: 27–31.
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.
Chen WH, Han YF, Liang JD, Liang ZQ. 2019. Morphological and phylogenetic characterization of novel Metarhizium species in Guizhou, China. Phytotaxa 419: 189–196. DOI:10.11646/phytotaxa.419.2.5.
Chen Z, Xu L, Yang F, Ji G, Yang J, Wang J. 2014. Efficacy of Metarhizium anisopliae isolate MAX-2 from Shangri-la, China under desiccation stress. BMC Microbiology 14: 1–8. DOI: 1471-2180/14/4.
Early R, González-Moreno P, Murphy ST, Day R. 2018. Forecasting the global extent of invasion of the cereal pest Spodoptera frugiperda, the fall armyworm. NeoBiota 40: 25–50. DOI: 10871/34861.
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.
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: 10.1016/j.jip.2007.05.007
Ganiger PC, Yeshwanth HM, Muralimohan K, Vinay N, Kumar ARV, Chandrashekara K. 2018. Occurrence of the new invasive pest, fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), in the maize fields of Karnataka, India. Current Science 115: 621–623.
Goergen G, Kumar PL, Sankung SB, Togola A, Tam M. 2016. First report of outbreaks of the fall armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera , Noctuidae), a new alien invasive pest in West and Central Africa. Plos One 11: 1–9. DOI:10.1371/journal.pone.0165632
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. Agriculture, Ecosystems and Environment 292: 1–10. DOI:10.1016/j.agee.2019.106804.
Gustianingtyas M, Herlinda S, Hamidson H. 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-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. Southwestern Entomologist 44: 409–421. DOI: 10.3958/059.044.0206
Harrison RD, Thierfelder C, Baudron F, Chinwada P, Midega C, Scha U, Berg J Van Den. 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. DOI: 10.1016/j.jenvman.2019.05.011
Hernandez-Trejo A, Estrada-Drouaillet B, López-Santillán J, Rios-Velasco C, Varela-Fuentes S, Rodríguez-Herrera R, Osorio-Hernández E. 2019. In vitro evaluation of native entomopathogenic fungi and neem (Azadiractha indica) extracts on Spodoptera frugiperda. International Journal of Experimental Botany 4: 75–84. DOI: 1037//0033-2909.I26.1.78.
Humber RA. 2005. Entomopathogenic Fungal Identification. USDA-ARS Plant Protection Research Unit: Ithaca.
IPPC. 2019. The Occurence of Fall Armyworm (Spodoptera frugiperda) in Indonesia. IPPC (International Plant Protection Convention) Official Pest Report, No. IDN-04/1. Rome, Italy: FAO. https://www.ippc.int/
Kalvnadi E, Mirmoayedi A, Alizadeh M, Pourian HR. 2018. Sub-lethal concentrations of the entomopathogenic fungus, Beauveria bassiana increase fitness costs of Helicoverpa armigera (Lepidoptera: Noctuidae) offspring. Journal of Invertebrate Pathology 158: 32–42. DOI: 10.1016/j.jip.2018.08.012.
Karthikeyan A, Shanthi V, Nagasathya A. 2008. Effect of different media and pH on the growth of Beauveria bassiana and its parasitism on leaf eating caterpillars. Res J Agric Biol Sci 4: 117–119.
Kumela T, Simiyu J, Sisay B, Likhayo P, Gohole L, Tefera T. 2018. Farmers knowledge, perceptions, and management practices of the new invasive pest, fall armyworm (Spodoptera frugiperda) in Ethiopia and Kenya. International Journal of Pest Management 65: 1–9. DOI: 10.1080/09670874.2017.1423129
Lestari P, Budiarti A, Fitriana Y, Susilo FX, Swibawa IG. 2020. Identification and genetic diversity of Spodoptera frugiperda in Lampung Province, Indonesia. 21: 1670–1677. DOI: 10.13057/biodiv/d210448.
Lopes RB, Souza DA, Rocha LFN, Montalva C, Luz C, Humber RA, Faria M. 2018. Metarhizium alvesii sp. nov.: A new member of the Metarhizium anisopliae species complex. Journal of Invertebrate Pathology 151: 165–168. DOI: 10.1016/j.jip.2017.12.001.
Machado BB, Orue JPM, Arruda MS, Santos C V., Sarath DS, Goncalves WN, Silva GG, Pistori H, Roel AR, Rodrigues-Jr JF. 2016. BioLeaf: A professional mobile application to measure foliar damage caused by insect herbivory. Computers and Electronics in Agriculture 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. Southwestern Entomol 44: 125–137. DOI: 10.3958/059.044.0114.
Montezano DG, Specht A, Sosa-gómez DR, Brasília UD. 2018. Host plants of Spodoptera frugiperda (Lepidoptera?: Noctuidae) in the Americas. African Entomology 26: 286–300. DOI: 10.4001/003.026.0286
Nagoshi RN, Fleischer S, Meagher RL, Hay-roe M, Silvie P, Vergara C, Westbrook J, Khan A, Muru MG, Silvie P, Vergara C, Westbrook J. 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
Nboyine JA, Kusi F, Abudulai M, Badii BK, Zakaria M, Adu GB, Haruna A, Seidu A, Osei V, Alhassan S, Yahaya A. 2020. A new pest, Spodoptera frugiperda (J.E. Smith), in tropical Africa: Its seasonal dynamics and damage in maize fields in northern Ghana. Crop Protection 127: 1–7. DOI: 10.1016/j.cropro.2019.104960.
Ngangambe MH, Mwatawala MW. 2020. Effects of entomopathogenic fungi (EPFs) and cropping systems on parasitoids of fall armyworm (Spodoptera frugiperda) on maize in eastern central, Tanzania. Biocontrol Science and Technology 30: 1–13. DOI: 10.1080/09583157.2020.1726878.
Otim MH, Tay WT, Walsh TK, Kanyesigye D, Adumo S, Abongosi J, Ochen S, Sserumaga J, Alibu S, Abalo G, Asea G, Agona A. 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
Prabawati G, Herlinda S, Pujiastuti Y. 2019. The abundance of canopy arthropods in South Sumatra (Indonesia) freshwater swamp main and ratooned rice applied with bioinsecticides and synthetic insecticide. Biodiversitas 20: 2921–2930. DOI: 10.13057/biodiv/d201021.
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. Egyptian Journal of Biological Pest Control 30: 1–6. DOI: 10.1186/s41938-020-00223-2.
Rivero-Borja M, Guzmán-Franco AW, 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 Management Science 74: 2047–2052. DOI: 10.1002/ps.4884.
Safitri A, Herlinda S, Setiawan A. 2018. Entomopathogenic fungi of soils of freshwater swamps, tidal lowlands, peatlands, and highlands of South Sumatra, Indonesia. Biodiversitas 19: 2365–2373. DOI: 10.13057/biodiv/d190647
Sharma L, Oliveira I, Torres L, Marques G. 2018. Entomopathogenic fungi in Portuguese vineyards soils: suggesting a ‘Galleria-Tenebrio-bait method’ as bait-insects Galleria and Tenebrio significantly underestimate the respective recoveries of Metarhizium (robertsii) and Beauveria (bassiana). MycoKeys 23: 1–23. DOI: 10.3897/mycokeys.38.26970.
Shylesha AN, Jalali SK, Gupta A, Varshney R, Venkatesan T. 2018. Studies on new invasive pest Spodoptera frugiperda (J .E . Smith) (Lepidoptera: Noctuidae) and its natural enemies. Journal of Biological Control 32: 145–151. DOI: 10.18311/jbc/2018/21707
Souza ML, Sanches MM, Souza DA de, Faria 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). Journal of Invertebrate Pathology 162: 10–18. DOI: 10.1016/j.jip.2019.01.006.
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
Thaochan N, Sausa-Ard W. 2017. Occurrence and effectiveness of indigenous Metarhizium anisopliae against adults Zeugodacus cucurbitae (Coquillett) (Diptera: Tephritidae) in Southern Thailand. Songklanakarin Journal of Science and Technology 39: 325–334. DOI:10.14456/sjst-psu.2017.35.
Wilson WM, Ibarra JE, Oropeza A, Hernández MA, Toledo-Hernández RA, Toledo J. 2020. Infection of Anastrepha ludens (Diptera: Tephritidae) adults during emergence from soil treated with Beauveria bassiana under various texture, humidity, and temperature conditions. Florida Entomologist 100: 503–508. DOI: 10.1653/024.100.0302.
Wu X, Zhang L, Yang C, Zong M, Huang Q, Tao L. 2016. Detection on emamectin benzoate-induced apoptosis and DNA damage in Spodoptera frugiperda Sf-9 cell line. Pesticide Biochemistry and Physiology 126: 6–12. DOI: 10.1016/j.pestbp.2015.06.009
Yang M, Wang B, Gao J, Zhang Y, Xu W, Tao L. 2017. Chemosphere spinosad induces programmed cell death involves mitochondrial dysfunction and cytochrome C release in Spodoptera frugiperda Sf9 cells. Chemosphere 169: 155–161. DOI: 10.1016/j.chemosphere.2016.11.065
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