Fungi from the body surface of Spodoptera frugiperda (Lepidoptera: Noctuidae) and bioassay of insecticidal activity

Authors

  • Bruna Novais Silva
  • Thiago Fernandes Sousa
  • Mateus Marques Maciel
  • Maykon Jhuly Martins de Paiva
  • Gilvan Ferreira da Silva
  • Bruna Alexandrino
  • Taides Tavares dos Santos

DOI:

https://doi.org/10.55905/oelv21n9-170

Keywords:

bioinsecticide, corn, fungus-insect interaction, insect pest, yeast

Abstract

Spodoptera frugiperda (Lepidoptera: Noctuidae) is an important insect pest in Brazil and worldwide, and its control is based mainly on chemical methods that are harmful to the environment and human and animal health. We investigated the fungal community associated with the body surface of S. frugiperda and evaluated the potential of members of this fungal community to act as biocontrol agents. The caterpillars were collected in the field, reared in the laboratory on a natural diet, evaluated for association with fungi on their surface and the environment, and subjected to a bioassay for insecticidal activity. Our results suggest that fungi are often associated with the body of S. frugiperda, as it was possible to obtain these microorganisms from all insects sampled, with a higher frequency of filamentous fungi than yeast. Fusarium verticillioides was the most frequent filamentous fungus species (F3 = 42.1%), followed by Aspergillus aureolus (F2 = 36.8%). Candida pseudointermedia was the most frequent yeast species (L1 = 57.1%). Aspergillus aureolus F2 was the only strain that exhibited toxicity against S. frugiperda and can be considered a good candidate to be explored from the perspective of obtaining biotechnological products of interest for agriculture.

References

ABBAS, A.; ULLAH, F.; HAFEEZ, M.; HAN, X.; DARA, M.Z.N.; GUL, H.; ZHAO, CR. Biological Control of Fall Armyworm, Spodoptera frugiperda. Agronomy, [S.L.], v. 12, n. 11, p. 2704, 31 out. 2022. DOI: https://doi.org/10.3390/agronomy12112704.

BAI, M.; ZHENG, C.J.; NONG, X.H.; ZHOU, X.M.; LUO, Y.P.; CHEN, G.Y. Four new insecticidal xanthene derivatives from the mangrove-derived fungus Penicillium sp. JY246. Marine Drugs, v. 17, p. 649, 20 nov. 2019. DOI: https://doi.org/10.3390/md17120649.

BARRILLI, É.T; TADIOTO, V.; MILANI, L.M.; DEOTI, J.R.; FOGOLARI, O.; MÜLLER, C.; BARROS, K.O.; ROSA, C.A.; DOS SANTOS, A.A.; STAMBUK, B.U.; TREICHEL, H.; ALVES, S.L. Biochemical analysis of cellobiose catabolism in Candida pseudointermedia strains isolated from rotten wood. Archives of Microbiology, [S.L.], v. 202, n. 7, p. 1729-1739, 23 abr. 2020. DOI: https://doi.org/10.1007/s00203-020-01884-1.

BATEMAN, M.L.; DAY, R.K.; LUKE B.; EDGINGTON, S.; KUHLMANN, U.; COCK, M.J.W. Assessment of potential biopesticide options for managing fall armyworm (Spodoptera frugiperda) in Africa. Journal of Applied Entomology, [S.L.], v. 142, n. 9, p. 805-819, 21 out. 2018. DOI: https://doi.org/10.1111/jen.12565.

BATISTELLA, M.; GUIMARÃES, M.; MIRANDA, E.E.; VIEIRA, H.R.; VALLADARES, G.S.; MANGABEIRA, J.A.D.C; ASSIS, M.C. Monitoramento da expansão agropecuária na região oeste da Bahia. Campinas: Embrapa Monitoramento por Satélite, 2002, 39 p.

BEDOLLA-TORRES, M.H.; ESPINOSA, A.P.; PALACIOS, O.A.; CHOIX, F.J.; VALLE, F.J.A.; AGUILAR, D. R. L.; VILLAVICENCIO, J.L.E.; PEÑA, R.L.; TRUJILLO, A.G.; SERRANO, N.Y.A.; PÉREZ, R.O. La irrigación con levaduras incrementa el contenido nutricional del forraje verde hidropónico de maíz. Revista Argentina de Microbiología, [S.L.], v. 47, n. 3, p. 236-244, jul. 2015. DOI: https://doi.org/10.1016/j.ram.2015.04.002.

BERESTETSKIY, A.; HU, Q. The chemical ecology approach to reveal fungal metabolites for arthropod pest management. Microorganisms, [S.L.], v. 9, n. 7, p. 1379, 24 jun. 2021. DOI: https://doi.org/10.3390/microorganisms9071379.

BIEDERMANN, P.H.W.; VEGA, F.E. Ecology and Evolution of Insect-Fungus Mutualisms. Annual Review of Entomology, [S.L.], v. 65, n. 1, p. 431-455, 7 jan. 2020.DOI: https://doi.org/10.1146/annurev-ento-011019-024910.

BRODERS, K.D.; LIPPS, P.E.; PAUL, P.A.; DORRANCE, A.E. Evaluation of Fusarium graminearum associated with corn and soybean seed and seedling disease in Ohio. Plant Disease, [S.L.], v. 91, n. 9, p. 1155-1160, set. 2007. DOI: https://doi.org/10.1094/PDIS-91-9-1155.

CASTELLANI, A. Viability of some pathogenic fungi in distilled water. Journal of Tropical Medicine and Hygiene, v. 42, p. 225-226, 1939.

CRUZ, I.; GONÇALVES, E.P.; FIGUEIREDO, M.L.C. Effect of a nuclear polyhedrosis virus on Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae) larvae, its damage and yield of maize crop. Revista Brasileira de Milho e Sorgo, v. 1, p. 20-27, 2002.

DOS SANTOS, C.A.M.; DO NASCIMENTO, J.; GONÇALVES, K.C.; SMANIOTTO, G.; ZECHIN, L.F; FERREIRA, M.C.; POLANCZYK, R.A. Compatibility of Bt biopesticides and adjuvants for Spodoptera frugiperda control. Scientific Reports, [S.L.], v. 5, p. 5271, 2021. DOI: https://doi.org/10.1038/s41598-021-84871-w.

DOUGLAS, A.E. Multiorganismal insects: diversity and function of resident microorganisms. Annual Review of Entomology, [S.L.], v. 60, p. 17-34, 7 jan. 2015. DOI: https://doi.org/10.1146/annurev-ento-010814-020822.

DOYLE, J.J.; DOYLE, J.L. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical bulletin, v. 19, p. 11-15, 1987.

FIGUEIREDO, M.L.C.; CRUZ, I.; LUCIA, T.M.C.D. Controle integrado de Spodoptera frugiperda (Smith, Abbott) utilizando-se o parasitóide Telenomus remus Nixon. Pesquisa Agropecuária Brasileira, [S.L.], v. 34, p. 1975-1982, nov. 1999. DOI: https://doi.org/10.1590/S0100-204X1999001100001.

FIRAKE, D.M.; BEHERE, G.T. Natural mortality of invasive fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) in maize agroecosystems of northeast India. Biological Control, [S.L.], v. 148, p. 1-11, set. 2020. DOI: https://doi.org/10.1016/j.biocontrol.2020.104303.

HORIKOSHI, R.J.; DOURADO, P.M.; BERNARDI, O.; WILLSE, A.; GODOY, W.A.; OMOTO, C.; BUENO, A.F.; MARTINELLI, S.; BERGER, G.U.; HEAD, G.P.; CORRÊA, A.S. Regional pest suppression associated with adoption of Cry1Ac soybean benefits pest management in tropical agriculture. Pest Management Science, [S.L.], v. 78, p. 4166-4172, 30 jun. 2022. DOI: https://doi.org/10.1002/ps.7034.

IBRAHIM, M.; SIEBER, T.N.; SCHLEGEL, M. Communities of fungal endophytes in leaves of Fraxinus ornus are highly diverse. Fungal Ecology, [S.L.], v. 29, p. 10-19, out. 2017. DOI: https://doi.org/10.1016/j.funeco.2017.05.001.

JARALEÑO-TENIENTE, J.; LOMELI-FLORES, J.R.; RODRÍGUEZ-LEYVA, E.; BUJANOS-MUÑIZ, R.; RODRÍGUEZ-RODRÍGUEZ, S.E. Egg parasitoids survey of Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae) in maize and sorghum in Central Mexico. Insects, [S.L.], v. 11, p. 157, mar. 2020. DOI: https://doi.org/10.3390/insects11030157.

KHAN, S.; GUO, L.; MAIMAITI, Y.; MIJIT, M.; QIU, D. Entomopathogenic fungi as microbial biocontrol agent. Molecular Plant Breed, [S.L.], v. 3, p. 63-79, 2012. DOI: https://doi.org/10.5376/mpb.2012.03.0007.

KHUNNAMWONG, P.; JINDAMORAKOT, S.; LIMTONG, S. Endophytic yeast diversity in leaf tissue of rice, corn and sugarcane cultivated in Thailand assessed by a culture-dependent approach. Fungal Biology, [S.L.], v. 122, n. 8, p. 785-799, ago. 2018. DOI: https://doi.org/10.1016/j.funbio.2018.04.006.

KNIGHT, A.L.; WITZGALL, P. Combining mutualistic yeast and pathogenic virus - a novel method for codling moth control. Journal of Chemical Ecology, [S.L.], v. 39, n. 7, p. 1019-1026, jul. 2013. DOI: https://doi.org/10.1007/s10886-013-0322-z.

KREBS, C.J. Ecology: The experimental analysis of distribution and abundance, 2nd ed. Harper & Row, New York, 1978.

LACAP, D.C.; HYDE, K.D.; LIEW, E.C.Y. An evaluation of the fungal ‘morphotype’ concept based on ribosomal DNA sequences. Fungal Diversity, v. 12, p. 53-66, 2003.

LESLIE, J.F. Introductory biology of Fusarium moniliforme. In: Jackson, L.S.; Devries, J.W.; Bullerman, L.B. (Eds). Fumonisins in Food, New York: Plenum Press, 1996. p. 153–165.

LIMA, R.K.; CARDOSO, M.G.; MORAES, J.C.; MELO, B.A.; RODRIGUES, V.G.; GUIMARÃES, P.L. Atividade inseticida do óleo essencial de pimenta longa (Piper hispidinervum C. DC.) sobre lagarta-do-cartucho do milho Spodoptera frugiperda (JE Smith; 1797) (Lepidoptera: Noctuidae). Acta Amazonica, [S.L.], v. 39, n. 2, p. 377-382, 2009. DOI: https://doi.org/10.1590/S0044-59672009000200016.

LUBIS, W.H.; LISNAWITA; TOBING, M.C. Fungi diversity in the rhizosphere of corn and Spodoptera frugiperda larvae. IOP Conference Series: Earth and Environmental Science, v. 782, p. 1-19, 2021.

LUDWIG, J.A.; REYNOLDS, J.F. Statistical ecology: a primer on methods and computing. John Wiley, New York. 1988.

MARTINS, M.S.; OLIVEIRA, H.C. The effects of pesticides on humans and the environment. International Journal of Advanced Engineering Research and Science, [S.L.], v. 9, n. 6, p. 259-264, 2022.DOI: https://doi.org/10.22161/ijaers.96.26.

MASOUD, W.; CESAR, L.B.; JESPERSEN, L.; JAKOBSEN, M. Yeast involved in fermentation of Coffea arabica in East Africa determined by genotyping and by direct denaturating gradient gel electrophoresis. Yeast, [S.L.], v. 21, n. 7, p. 549-556, maio 2004. DOI: https://doi.org/10.1002/yea.1124.

MEENA, R.S.; KUMAR, S.; DATTA, R.; LAL, R.; VIJAYAKUMAR, V.; BRTNICKY, M.; SHARMA, M.P.; YADAV, G.S.; JHARIYA, M.K.; JANGIR, C.K.; PATHAN, S.I.; DOKULILOVA, T.; PECINA, V.; MARFO, T.D. Impact of agrochemicals on soil microbiota and management: a review. Land, [S.L.], v. 9, n. 2, p. 34, 23 jan. 2020. DOI: https://doi.org/10.3390/land9020034.

MURPHY, K.A.; TABULOC, C.A.; CERVANTES, K.R.; CHIU, J.C. Ingestion of genetically modified yeast symbiont reduces fitness of an insect pest via RNA interference. Scientific Reports, v. 2, p. 22587, 2016. DOI: https://doi.org/10.1038/srep22587.

NAKASE, T.; KOMAGATA, K.; FUKAZAWA, Y. Candida pseudointermedia sp. nov. isolated from “Kamaboko,” a traditional fish-paste product in Japan. The Journal of General and Applied Microbiology, v. 22, n. 4, p. 177–182, 1976. DOI: https://doi.org/10.2323/jgam.22.177.

NICULAU, E.S.; ALVES, P.B.; NOGUEIRA, P.C.L.; MORAES, V.R.S.; MATOS, A.P.; BERNARDO, A.R.; VOLANTE, A.C.; FERNANDES, J.B.; SILVA, M.F.G.F.; CORRÊA, A.G.; BLANK, A.F.; SILVA, A.C.; RIBEIRO, L.P. Atividade inseticida de óleos essenciais de Pelargonium graveolens l'Herit e Lippia alba (Mill) NE Brown sobre Spodoptera frugiperda (JE Smith). Química Nova, [S.L.], v. 36, n. 9, p. 1391-1394, 2013.DOI: https://doi.org/10.1590/S0100-40422013000900020

OLIVEIRA, H.F.; Nunes, J. Eficiência de inseticidas no controle de Spodoptera frugiperda na cultura da soja. Revista Cultivando o Saber, v. 10, p. 156-168, 2017.

PAMPHILE, J.A.; Azevedo, J.L. Molecular characterization of endophytic strains of Fusarium verticillioides (= Fusarium moniliforme) from maize (Zea mays. L). World Journal of Microbiology and Biotechnology, [S.L.], v. 18, p. 391–396, 2002. DOI: https://doi.org/10.1023/A:1015507008786

PANG, Z.; ZHAO, Y.; XU, P.; YU, D. Microbial diversity of upland rice roots and their influence on rice growth and drought tolerance. Microorganisms, [S.L.], v. 8, n. 9, p. 1329, 31 ago. 2020. DOI: https://doi.org/10.3390/microorganisms8091329

PEEL, M.C.; FINLAYSON, B.L.; MCMAHON, T.A. Updated world map of the Koppen-Geiger climate classification. Hydrology and Earth System Sciences, [S.L.], v. 11, n. 5, p. 1633-1644, 11 out. 2007.DOI: https://doi.org/10.5194/hess-11-1633-2007

PIETERSE, Z.; AVELING, T.A.S.; JACOBS, A.; COWAN, D.A. Seasonal variability in fungal endophytes from Aizoaceae plants in the Succulent Karoo biodiversity hotspot; South Africa. Journal of Arid Environments, [S.L.], v. 156, p. 19-26, set. 2018.DOI: https://doi.org/10.1016/j.jaridenv.2018.05.004

POTSHANGBAM, M.; DEVI, S.I.; SAHOO, D.; STROBEL, G.A. Functional characterization of endophytic fungal community associated with Oryza sativa L. and Zea mays L. Frontiers in Microbiology, [S.L.], v. 8, p. 1-15, 2017. DOI: https://doi.org/10.3389/fmicb.2017.00325

RABELO, S.F.; SILVA, C.H.F.; SANTANA, M.D.F.; SANTOS, T.T.; ATAYDE, H.M.A. Efficacy of surface microbial decontamination of beer cans and cytotoxic activity of fungal isolates. Scientia Amazonia, v. 10, p. 1-11, 2021.

RAMOS, D.L.; CUNHA, W.L.; EVANGELISTA, J.; LIRA, L.A.; ROCHA, M.V.C.; GOMES, P.A.; FRIZZAS, M,R.; TOGNI, P.H.B. Ecosystem services provided by insects in Brazil: What do we really know? Neotropical Entomology [S.L.], v. 49, n. 6, p. 783-794, 28 maio 2020. DOI: https://doi.org/10.1007/s13744-020-00781-y.

RAMOS, D.P.; BARBOSA, R.M.; VIEIRA, B.G.T.L.; PANIZZI, R.C.; VIEIRA, R.D. Infecção por Fusarium graminearum e Fusarium verticillioides em sementes de milho. Pesquisa Agropecuária Tropical, [S.L.], v. 44, n. 1, p. 24-31, mar. 2014. DOI: https://doi.org/10.1590/S1983-40632014000100011

RIDDELL, R.W. Permanent stained mycological preparation obtained by slide culture. Mycologia, v. 42, p. 265–270, 1950.

RUIZ-NAJERA, R.; RUIZ-ESTUDILLO, R.A.; SANCHEZ-YANEZ, J.M.; MOLINA-OCHOE, J.; SKODA, S.R.; COUTINO-RUIZ, R.; PINTO-RUIZ, R.; GUEVARA-HERNANDEZ, F.; FOSTER, J.E. Occurrence of entomopathogenic fungi and parasitic nematodes on Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae collected in Central Chiapas, México. Florida Entomologist , [S.L.], v. 96, n. 2, p. 498-503, jun. 2013. DOI: https://doi.org/10.1653/024.096.0215.

SANO, E.E.; ROSA, R.; BRITO, J.L.S.; FERREIRA, L.G. Land cover mapping of the tropical savanna region in Brazil. Environmental Monitoring and Assessment, [S.L.], v. 166, n. 1-4, p. 113-124, 6 jun. 2009. DOI: https://doi.org/10.1007/s10661-009-0988-4.

SANTOS, T.T.; OLIVEIRA, D.P.; CABETTE, H.S.R.; MORAIS, P.B. The digestive tract of Phylloicus (Trichoptera: Calamoceratidae) harbours different yeast taxa in Cerrado streams; Brazil. Symbiosis, [S.L.], v. 77, n. 2, p. 147-160, 25 out. 2018. DOI: https://doi.org/10.1007/s13199-018-0577-9.

SANTOS, T.T.; PES, A.M.O.; MORAIS, P.B. A diverse and partially cellulolytic fungal community contributes to the diet of three species of the aquatic insect Phylloicus (Trichoptera: Calamoceratidae) in Amazonian streams. Anais da Academia Brasileira de Ciências, [S.L.], v. 93, p. 1-21, 2021. DOI: https://doi.org/10.1590/0001-3765202120210598.

SARTORI, A.F.; REIS, E.M.; CASA, R.T. Quantificação da transmissão de Fusarium moniliforme de sementes para plântulas de milho. Fitopatologia Brasileira, [S.L.], v. 29, n. 4, p. 456-458, ago. 2004. DOI: https://doi.org/10.1590/S0100-41582004000400018.

SMITH, J.E.; ABBOT, J. 1797. The Natural History of the Rarer Lepidopterous Insects of Georgia, including their systematic characters, the particulars of their several metamorphoses, and the plants on which they feed, collected from the observations of Mr. John Abbot, many years resident in that country. 2 vols. J. Edwards, Cadell & Davies, and J. White, London. 214 pp., 104 pl.

SOUZA, A.Q.L.; SOUZA, A.D.L.; ASTOLFI FILHO, S.; PINHEIRO, M.L.B.; SARQUIS, M.I.M.; PEREIRA, J.O. Atividade antimicrobiana de fungos endofíticos isolados de plantas tóxicas da amazônia: Palicourea longiflora (aubl.) rich e Strychnos cogens bentham. Acta Amazonica, [S.L.], v. 34, n. 2, p. 185-195, 2004. DOI: https://doi.org/10.1590/S0044-59672004000200006.

SPENCER, J.F.; SPENCER, D.M. Maintenance and culture of yeasts. Methods in Molecular Biology, v. 53, p. 5-15, 1996.

TAGLIARI, M.S.; KNAAK, N.; FIUZA, L.M. Efeito de extratos de plantas na mortalidade de lagartas de Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae). Arquivos do Instituto Biológico, [S.L.], v. 77, n. 2, p. 259-264, jun. 2010. DOI: https://doi.org/10.1590/1808-1657v77p2592010.

YAMOAH, E.; JONES, E.E.; WELD, R.J.; SUCKLING, D.M.; WAIPARA, N.; BOURDÔT, G.W.; HEE, A.K.W.; STEWART, A. Microbial population and diversity on the exoskeletons of four insect species associated with gorse (Ulex europaeus L.). Australian Journal of Entomology, [S.L.], v. 47, n. 4, p. 370-379, 29 out. 2008. DOI: https://doi.org/10.1111/j.1440-6055.2008.00655.x.

YUAN, X.-L.; WANG, X.-F.; XU, K.; LI, W.; CHEN, D.; ZHANG, P. Characterization of a new insecticidal anthraquinone derivative from an endophyte of Acremonium vitellinum against Helicoverpa armigera. Journal of Agricultural and Food Chemistry, [S.L.], v. 68, p. 11480– 11487, 2020. DOI: https://doi.org/10.1021/acs.jafc.0c05680.

ZHANG, P.; YOU, Y.; SONG, Y.; WANG, Y.; ZHANG, L. First record of Aspergillus oryzae (Eurotiales: Trichocomaceae) as an entomopathogenic fungus of the locust; Locusta migratoria (Orthoptera: Acrididae). Biocontrol Science and Technology, [S.L.], v. 25, n. 11, p. 1285-1298, 24 jul. 2015. DOI: https://doi.org/10.1080/09583157.2015.1049977.

Downloads

Published

2023-09-28

How to Cite

Silva, B. N., Sousa, T. F., Maciel, M. M., de Paiva, M. J. M., da Silva, G. F., Alexandrino, B., & dos Santos, T. T. (2023). Fungi from the body surface of Spodoptera frugiperda (Lepidoptera: Noctuidae) and bioassay of insecticidal activity. OBSERVATÓRIO DE LA ECONOMÍA LATINOAMERICANA, 21(9), 13647–13671. https://doi.org/10.55905/oelv21n9-170

Issue

Section

Articles

Most read articles by the same author(s)