Entomopathogenic fungi in passion fruit pests: A review and preliminary report of Fusarium sp. on Agraulis vanillae
DOI:
https://doi.org/10.30681/rcaa.v23i1.13186Keywords:
Biocontrol, Fungi, Passion fruit Plague, Review.Abstract
Agraulis vanillae Linnaeus, 1758, and Dione juno Cramer, 1779 (Insecta: Lepidoptera: Nymphalidae) are recognized as significant pest insects in passion fruit (Passiflora edulis – Passifloraceae) cultivation, causing substantial economic losses to farmers. Despite their agricultural relevance, there is still a noticeable scarcity of scientific records documenting fungal diseases that could affect these species. This lack of information hinders the development of effective and sustainable pest control strategies, which are highly necessary for reducing pesticide dependency. To address this knowledge gap, a comprehensive literature review was conducted to identify evidence and descriptions of infections or mortality caused by fungal pathogens in A. vanillae and D. juno. As part of this research, larvae of A. vanillae infected with a fungal pathogen belonging to the genus Fusarium (Fungi: Hypocreales: Nectriaceae) were collected in Vera Cruz, Rio Grande do Sul, Brazil. The taxonomic characteristics and cultivation conditions of this fungal isolate are thoroughly detailed in this study. This discovery holds significant potential for agricultural applications, offering an alternative to chemical pesticides in the management of passion fruit pests. However, further experimental studies are essential to evaluate the biocontrol efficacy and practical applicability of Fusarium sp. under field conditions. This work expands knowledge on fungal pathogens of agricultural pests and emphasizes their role in integrated pest management systems.
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ALI, S.; ULLAH, M.I.; SAJJAD, A.; SHAKEEL, Q.; HUSSAIN, A. Environmental and health effects of pesticide residues. Sustainable Agriculture Reviews 48: Pesticide Occurrence, Analysis and Remediation, v.2 Analysis, p. 311-336, 2021.
ALMEIDA, I.S.A.; DADAZIO, T.S.; NOGUEIRA, P.E.; ANDRADE, S.C.R.B.; SUSSAI, J.F.; HAMAMURA, H.; DOMINGUES, R.N.; SCARAMUSSA, A.S. Monitoramento de doenças na cultura do maracujá (Passiflora spp.) em duas diferentes cultivares submetidas a adubações distintas. Brazilian Journal of Development, v. 7, n. 9, p. 91224-91233, 2021.
ANGELINI, M.R.; BOIÇA JÚNIOR, A.L. Preferência alimentar de Dione juno juno (CRAMER, 1779) (Lepidoptera: Nymphalidae) por genótipos de maracujazeiro. Revista Brasileira de Fruticultura, v. 29, p. 276-281, 2007.
BIANCHI, V.; MOREIRA, G.R.P. Preferência alimentar, efeito da planta hospedeira e da densidade larval na sobrevivência e desenvolvimento de Dione juno juno (Cramer) (Lepidoptera, Nymphalidae). Revista Brasileira de Zoologia, v. 22, p. 43-50, 2005.
BOIÇA JÚNIOR, A.L.; ANGELINI, M.R.; OLIVEIRA, J.C. Aspectos biológicos de Dione juno juno (Cramer) (Lepidoptera: Nymphalidae) em genótipos de maracujazeiro. Revista Brasileira de Fruticultura, v. 30, p. 101-105, 2008.
BOTELHO-JÚNIOR, S.; SIQUEIRA-JÚNIOR, C.L.; JARDIM, B.C.; MACHADO, O.L.T.; NEVES-FERREIRA, A.G.C.; PERALES, J.; JACINTO, T. Trypsin inhibitors in passion fruit (Passiflora f. edulis flavicarpa) leaves: accumulation in response to methyl jasmonate, mechanical wounding, and herbivory. Journal of Agricultural and Food Chemistry, v. 56, n. 20, p. 9404-9409, 2008.
CASTRILLO, L.A.; WHEELER, M.M. USDA-ARS Collection of Entomopathogenic Fungal Cultures (ARSEF): Isaria. Ithaca, NY: USDA-ARS Emerging Pests and Pathogens Research Unit, Robert W. Holley Center for Agriculture & Health, 2020. 44p.
COPP, N.H.; DAVENPORT, D. Agraulis and Passiflora I. Control of specificity. The Biological Bulletin, v. 155, n. 1, p. 98-112, 1978.
COPP, N.H.; DAVENPORT, D. Agraulis and Passiflora II. Behavior and sensory modalities. The Biological Bulletin, v. 155, n. 1, p. 113-124, 1978.
DREWNIAK, M.E.; BRISCOE, A.D.; COCUCCI, A.A.; BECCACECE, H.M.; ZAPATA, A.I.; MORÉ, M. From the butterfly’s point of view: learned colour association determines differential pollination of two co-occurring mock verbains by Agraulis vanillae (Nymphalidae). Biological Journal of the Linnean Society, v. 130, n. 4, p. 715-725, 2020.
ECHEVERRI, F.; CARDONA, G.; TORRES, F.; PELAEZ, C.; QUIÑONES, W.; RENTERIA, E. Ermanin: an insect deterrent flavonoid from Passiflora foetida resin. Phytochemistry, v. 30, n. 1, p. 153‑155, 1991.
ESCANDÓN-ARBOLAY, M.C.; DÍAZ-VIRULICHE, L.; CASTRO-LIZAZO, I. Lecanicillium lecanii (Zare y Gams) parasitando larvas de Agraulis vanillae insularis Maynard. Revista de Protección Vegetal, v. 28, n. 1, p. 78-78, 2013.
FALEIRO, F.G.; JUNQUEIRA, N.T.V.; JUNGHANS, T.G.; JESUS, O.N.; MIRANDA, D.; OTONI, W.C. Advances in passion fruit (Passiflora spp.) propagation. Revista Brasileira de Fruticultura, v. 41, p. e-155, 2019.
GENTRY, S.L.; LORCH, J.M.; LANKTON, J.S.; PRINGLE, A. Koch’s postulates: confirming Nannizziopsis guarroi as the cause of yellow fungal disease in Pogona vitticeps. Mycologia, v. 113, n. 6, p. 1253-1263, 2021.
HAJEK, A.E.; NELSON, P.E.; HUMBER, R.A.; PERRY, J.L. Two Fusarium species pathogenic to gypsy moth, Lymantria dispar. Mycologia, v. 85, n. 6, p. 937-940, 1993.
HERNIOU, E.A.; JEHLE, J.A. Baculovirus phylogeny and evolution. Current Drug Targets, v. 8, n. 10, p. 1043-1050, 2007.
JIANG, Y.; WANG, J. The registration situation and use of mycopesticides in the world. Journal of Fungi, v. 9, n. 9, p. 940, 2023.
KARTHI, S.; VASANTHA‑SRINIVASAN, P.; GANESAN, R.; RAMASAMY, V.; SENTHIL‑NATHAN, S.; KHATER, H.F.; RADHAKRISHNAN, N.; AMALA, K.; KIM, T.-J.; EL‑SHEIKH, M.A.; KRUTMUANG, P. Target activity of Isaria tenuipes (Hypocreales: Clavicipitaceae) fungal strains against dengue vector Aedes aegypti (Linn.) and its non‑target activity against aquatic predators. Journal of Fungi, v.6, n.4, p.196, 2020.
KOCH, R. Untersuchungen über die Aetiologie der Wundinfectionskrankheiten. FCW Vogel, 1878, 88 p.
KRISTENSEN, N.P.; SCOBLE, M.J.; KARSHOLT, O. Lepidoptera phylogeny and systematics: the state of inventorying moth and butterfly diversity. Zootaxa, v. 1668, n. 1, p. 699–747, 2007.
KUMAR, K.K.; SRIDHAR, J.; MURALI-BASKARAN, R.K.; SENTHIL-NATHAN, S.; KAUSHAL, P.; DARA, S.K.; ARTHURS, S. Microbial biopesticides for insect pest management in India: Current status and future prospects. Journal of Invertebrate Pathology, v. 165, p. 74-81, 2019.
LANDOLT, P. J.; LENCZEWSKI, B. Lack of evidence for the toxic nectar hypothesis: a plant alkaloid did not deter nectar feeding by Lepidoptera. Florida Entomologist, v. 76, n. 4, p. 556-566, 1993.
LIMA, M.F.C.; VEIGA, A.F.S.L. Ocorrência de inimigos naturais de Dione juno juno (CR.), Agraulis vanillae maculosa S. e Eueides isabella dianasa (Hüb.) (Lepidoptera: Nymphalidae) em Pernambuco. Anais da Sociedade Entomológica do Brasil, v. 24, n. 3, p. 631-634, 1995.
LIMA, A.A.; NORONHA, A.C.S.; BORGES, A.L.; CARDOSO, C.E.L.; RITZINGER, C.H.S.; BARBOSA, C.J.; COSTA, D.C.; SANTOS FILHO, H.P.; FANCELLI, M.; CUNHA, M.A.P.; SANCHES, N.F. A cultura do maracujá. Brasília, DF: Embrapa Informação Tecnológica; Cruz das Almas: Embrapa Mandioca e Fruticultura Tropical, 2006.
LORDELLO, L. G. E. Insetos que vivem sobre o maracujazeiro. III – Notas acerca de Dione juno (Cramer) (Lep. Nymphalidae) e relação de alguns outros insetos habitualmente coligidos de Passiflora spp., Brazilian Journal of Agriculture - Revista de Agricultura, v.29, n.1-2, p.23-29, 1954.
LUNZ, A. M., DE SOUZA, L. A., LEMOS, W. D. P. Reconhecimento dos principais insetos-praga do maracujazeiro. Embrapa Amazônia Oriental, 2006. 36 p. (Documentos, 245).
MACHADO, C.F.; FALEIRO, F.G.; SANTOS FILHO, H.P.; FANCELLI, M.; CARVALHO, R.S.; RITZINGER, C.H.S.P.; ARAUJO, F.P.; JUNQUEIRA, N.T.V.; JESUS, O.N.; NOVAES, Q.S. Guia de identificação e controle de pragas na cultura do maracujazeiro. Brasília: Embrapa, 2017, 94 p.
MALPARTIDA-ZEVALLOS, J.; NARREA-CANGO, M.; DALE-LARRABURRE, W. Patogenicidad de Beauveria bassiana (Bals.) Vuill., sobre el gusano defoliador del maracuyá Dione juno (Cramer) (Lepidoptera: Nymphalidae) en laboratorio. Ecología Aplicada, v. 12, n. 2, p. 75-81, 2013.
MANTZOUKAS, S.; KITSIOU, F.; NATSIOTOPOULOS, D.; ELIOPOULOS, P.A. Entomopathogenic fungi: interactions and applications. Encyclopedia, v. 2, n. 2, p. 646-656, 2022.
MANTZOUKAS, S.; KITSIOU, F.; LAGOGIANNIS, I.; ELIOPOULOS, P.A. Potential use of Fusarium isolates as biological control agents: Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) Case study. Applied Sciences, v. 12, n. 17, p. 8918, 2022.
MASSARDO, D.; RORATTO, P.A.; VARGAS, H.A.; KRONFORST, M.R.; MOREIRA, G.R.P. Development of a microsatellite library for the passion flower butterfly Dione moneta Hübner (Lepidoptera: Nymphalidae: Heliconiinae). Conservation Genetics Resources, v. 4, p. 719-724, 2012.
MASSARDO, D.; FORNEL, R.; KRONFORST, M.; GONÇALVES, G.L.; MOREIRA, G.R.P. Diversification of the silverspot butterflies (Nymphalidae) in the Neotropics inferred from multi-locus DNA sequences. Molecular Phylogenetics and Evolution, v. 82, p. 156-165, 2015.
MILLAN, C.; BORGES, S.S.; RODRIGUES, D.; MOREIRA, G.R.P.; FREITAS, A.V.L. Behavioral and life-history evidence for interspecific competition in the larvae of two heliconian butterflies. Naturwissenschaften, v. 100, p. 901–911, 2013.
NARANJO, S.E.; ELLSWORTH, P.C.; FRISVOLD, G.B. Economic value of biological control in integrated pest management of managed plant systems. Annual Review of Entomology, v. 60, n. 1, p. 621-645, 2015.
QUESADA-MORAGA, E.; GARRIDO-JURADO, I.; YOUSEF-YOUSEF, M.; GONZÁLEZ-MAS, N. Multitrophic interactions of entomopathogenic fungi in BioControl. BioControl, v. 67, n. 5, p. 457-472, 2022.
RAMAKUWELA, T.; HATTING, J.; BOCK, C.; VEGA, F.E.; WELLS, L.; MBATA, G.N.; SHAPIRO-ILAN, D. Establishment of Beauveria bassiana as a fungal endophyte in pecan (Carya illinoinensis) seedlings and its virulence against pecan insect pests. Biological Control, v. 140, p. 104102, 2020.
RODRÍGUEZ-DIMATÉ, F.A.; PODEROSO, J.C.M.; RIBEIRO, R.C.; BRÜGGER, B.P.; WILCKEN, C.F.; SERRÃO, J.E.; ZANUNCIO, J.C. Palmistichus elaeisis (Hymenoptera: Eulophidae) parasitizing pupae of the passion fruit pest Agraulis vanillae vanillae (Lepidoptera: Nymphalidae). Florida Entomologist, v. 99, n. 1, p. 130-132, 2016.
SANTOS, A.C.S.; DINIZ, A.G.; TIAGO, P.V.; OLIVEIRA, N.T. Entomopathogenic Fusarium species: a review of their potential for the biological control of insects, implications and prospects. Fungal Biology Reviews, v. 34, n. 1, p. 41-57, 2020.
SILVA, D.S.; DELL’ERBA, R.; KAMINSKI, L.A.; MOREIRA, G.R.P. Morfologia externa dos estágios imaturos de heliconíneos neotropicais: V. Agraulis vanillae maculosa (Lepidoptera, Nymphalidae, Heliconiinae). Iheringia. Série Zoologia, v. 96, p. 219-228, 2006.
SILVA, C.J.A.; MALTA, D.J.N. A importância dos fungos na biotecnologia. Caderno de Graduação-Ciências Biológicas e da Saúde-UNIT-PERNAMBUCO, v. 2, n. 3, p. 49-49, 2016.
TAVARES, M.; KAMINSKI, L.A.; MOREIRA, G.R.P. Morfologia externa dos estágios imaturos de heliconíneos neotropicais: II. Dione juno juno (Cramer) (Lepidoptera, Nymphalidae, Heliconiinae). Revista Brasileira de Zoologia, v. 19, p. 961-976, 2002.
TEETOR-BARSCH, G.H.; ROBERTS, D.W. Entomogenous Fusarium species. Mycopathologia, v. 84, n. 1, p. 3-16, 1983.
TEFERA, T.; PRINGLE, K.L. Food consumption by Chilo partellus (Lepidoptera: Pyralidae) larvae infected with Beauveria bassiana and Metarhizium anisopliae and effects of feeding natural versus artificial diets on mortality and mycosis. Journal of Invertebrate Pathology, v. 84, n. 3, p. 220-225, 2003.
THOKCHOM, R.; MANDAL, G. Production preference and importance of passion fruit (Passiflora edulis): A review. Journal of Agricultural Engineering and Food Technology, v. 4, n. 1, p. 27-30, 2017.
WALKER, T.J. Butterfly migrations in Florida: seasonal patterns and long-term changes. Environmental Entomology, v. 30, n. 6, p. 1052-1060, 2001.
WANG, H.; PENG, H.; LI, W.; CHENG, P.; GONG, M. The toxins of Beauveria bassiana and the strategies to improve their virulence to insects. Frontiers in Microbiology, v. 12, p. 705343, 2021.
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