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First record of Isia alcumena, Spodoptera cosmioides and S. eridania (LEPIDOPTERA: NOCTUOIDEA) attacking Passion Fruit (Passiflora edulis Sims) in Brazil

Primeiro registro de Isia alcumena, Spodoptera cosmioides e Spodoptera eridania (LEPIDOPTERA: NOCTUOIDEA) em maracujazeiro (Passiflora edulis Sims) no Brasil

Abstract

Brazil is considered the center of origin and diversity of passifloras. These species have a great importance to in natura fruits consumption, industrialization, medicinal use and also as ornamental plants. The different Passiflora speciesare host of a great diversity of arthropods that can cause injuries, economic damages and, in some situations, the plant death. Among the arthropods, leafhopper caterpillars are considered frequent and severe pests in the main passion fruit producing regions. The present work is an occurrence report of Isia alcumena and Spodoptera cosmioides attacking passion fruit plants (Passiflora edulis Sims) in the Federal District, Brazil. The S. cosmioides and S. eridania caterpillars were collected while consuming leaves of Passiflora edulis intra-specific hybrid located in the Germplasm Active Bank ‘Flor da Paixão’ at Embrapa Cerrados. The caterpillars of I. alcumena were collected on leaves of the Passiflora edulis cv. BRS Rubi do Cerrado at the Agricultural Support Unit, Embrapa Cerrados. After collected, the caterpillars were individualized in a breeding system with leaves of the host plants. The development of the caterpillar was accompanied until the emergence of the adults, which were identified and fixed in entomological pins for permanent dry preservation.

Index terms
Insecta; polyphagous larvae; passion fruit; owlet moths; occasional pests

Resumo

O Brasil é considerado o centro de origem e de diversidade das passifloras, que apresentam importância, tanto para o consumo in natura, industrialização, uso medicinal e também como plantas ornamentais. As diferentes espécies de Passiflora hospedam uma grande diversidade de artrópodes que, ocasionando injúrias, podem causar danos econômicos e morte da planta. Dentre os artrópodes, as lagartas-desfolhadoras são consideradas as pragas mais frequentes e severas nas principais regiões produtoras de maracujá. Assim, o objetivo foi informar o primeiro registro da ocorrência das espécies Isia alcumena, Spodoptera cosmioides e S. eridania atacando maracujazeiros no Distrito Federal, Brasil. As lagartas de S. cosmioides e S. eridania foram coletadas enquanto consumiam folhas de híbridos intraespecíficos de Passiflora edulis cultivado no banco ativo de germoplasma “Flor da Paixão” da Embrapa Cerrados. Já as lagartas de I. alcumena foram coletadas em folhas da cultivar BRS Rubi do Cerrado, na Unidade de Apoio da Fruticultura da Embrapa Cerrados. Após a coleta, as lagartas foram individualizadas em sistema de criação com folhas das plantas hospedeiras. O desenvolvimento das lagartas foi acompanhado até à emergência dos adultos, que foram identificados e fixados em alfinetes entomológicos para preservação permanente, a seco.

Termos para indexação
Insecta; lagartas polífagas; maracujá; noctuoides; pragas ocasionais

Introduction

Passion fruit, widely distributed in the tropics and temperate regions, belong to the family Passifloraceae, which is composed of 24 subgenera and approximately 520 species. It is estimated that more than 150 of them are originated from Brazil and about 70 produce edible fruits (BERNACCI et al. 2013 BERNACCI, L. C.; CERVI, A. C.; MILWARD-DE-AZEVEDO, M. A.; NUNES, T. S., IMIG, D.C.; MEZZONATO, A.C. Passifloraceae. Lista de Espécies da Flora do Brasil. Rio de Janeiro: Jardim Botânico do Rio de Janeiro, 2013. Disponível em: http://floradobrasil.jbrj.gov.br/. ; VIEIRA e CARNEIRO, 2004 VIEIRA, M.L.C.; CARNEIRO, M.C. Passiflora spp. Passionfruit. In: LITZ, R. (ed.). Biotechnology of fruit and nut crops. Gainesville: University of Florida, 2004. p.436-453. ).

The species of the genus Passiflora are important since they are associated to the basic needs of the human being and can be used in food, medicine manufacturing and also as ornamental plants due to the beauty and diversity of their flowers and leaves (FALEIRO et al. 2012 FALEIRO, F.G.; JUNQUEIRA, N.T.V.; BRAGA, M.F.; COSTA, A.M. Conservação e caracterização de espécies silvestres de maracujazeiro (Passiflora spp.) e utilização potencial no melhoramento genético, como porta-enxertos, alimentos funcionais, plantas ornamentais e medicinais - resultados de pesquisa. Planaltina: Embrapa Cerrados, 2012. 34p. (Documentos, 312) ).

Although there are several different species of Passiflora, only some of them are considered economically important. According to Faleiro et al. (2008 FALEIRO, F.G.; JUNQUEIRA, N.T.V.; BRAGA, M.F.; PEIXOTO, J.R. Caracterização de germoplasma e melhoramento genético do maracujazeiro assistidos por marcadores moleculares: resultados de pesquisa 2005-2008. Planaltina: Embrapa Cerrados, 2008. 59 p. (Boletim de Pesquisa e Desenvolvimento, 207). ; 2017 FALEIRO, F.G.; JUNQUEIRA, N.T.V.; JESUS, O.N.; COSTA, A.M.; MACHADO, C.F.; JUNQUEIRA, K.P.; ARAÚJO, F.P.; JUNGHANS, T.G. Espécies de maracujazeiro no mercado internacional. In: JUNGHANS, T.G.; JESUS, O.N. (ed.). Maracujá: do cultivo à comercialização. Brasília, DF: Embrapa, 2017. p.15-37. ), P. edulis Sims (sour passion fruit) is the most cultivated species worldwide. In general, in the commercial crops of P. edulis, phytosanitary problems occur resulted from the expansion and continued use of the same planting areas. Other species such as P. ligularis, P. alata, P. setacea, P. cincinnata, P. tripartita, P. quadrangularis and P. maliformis are also commercially cultivated mainly in Brazil and Colombia (FALEIRO et al. 2008 FALEIRO, F.G.; JUNQUEIRA, N.T.V.; BRAGA, M.F.; PEIXOTO, J.R. Caracterização de germoplasma e melhoramento genético do maracujazeiro assistidos por marcadores moleculares: resultados de pesquisa 2005-2008. Planaltina: Embrapa Cerrados, 2008. 59 p. (Boletim de Pesquisa e Desenvolvimento, 207). ; 2017 FALEIRO, F.G.; JUNQUEIRA, N.T.V.; JESUS, O.N.; COSTA, A.M.; MACHADO, C.F.; JUNQUEIRA, K.P.; ARAÚJO, F.P.; JUNGHANS, T.G. Espécies de maracujazeiro no mercado internacional. In: JUNGHANS, T.G.; JESUS, O.N. (ed.). Maracujá: do cultivo à comercialização. Brasília, DF: Embrapa, 2017. p.15-37. ) Among the insects and pests that can damage the passion fruit tree, the Lepidoptera represented especially by the Nymphalidae and Notodontidae (subfamily Dioptinae), are the most common species that attack passion fruit, which evolution coincides with the Passifloraceae (MILLER, 2009 MILLER, J.S. Generic revision of the Dioptinae (Lepidoptera: Noctuoidea: Notodontidae). Part 2: Josiini. Bulletin of the American Museum of Natural History, New York, v.321, p.675–1022, 2009. ; MASSARDO et al. 2015 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, Orlando, v.82, p.156-165, 2015. ). However, there have been species of Lepidoptera of other families associated to the Passiflora including: Coleophoridae, Cossidae, Erebidae, Geometridae, Gracillariidae, Hepialidae, Noctuidae, Oecophoridae, Psychidae, Pyralidae, Saturniidae, Sphingidae and Tortricidae (SILVA et al. 1968 SILVA, A.G.D’A.; GONÇALVES, C.R.; GALVÃO, D.M.; GONÇALVES, A.J.L.; GOMES, J.; SILVA, N.M.; SIMONI, L. Quarto catálogo dos insetos que vivem nas plantas do Brasil, seus parasitos e predadores. Rio de Janeiro: Ministério da Agricultura, 1968. tomo 1, pt. 2, 622 p. ; CHACON e ROJAS 1984 CHACON, P.; ROJAS, M. Entomofauna asociada a Passiflora mollissima, P. edulis f. flavicarpa y P. quadrangularis en el Departamento del Valle del Cauca.Turrialba, Costa Rica, v.34, p.297-311, 1984. ; MESSENGER, 1997 MESSENGER, C. The Sphinx Moths (Lepidoptera: Sphingidae) of Nebraska. Transactions of the Nebraska Academy of Sciences, Lincoln, v.24, p.89-141, 1997. ; CAUSTON et al. 2000 CAUSTON, C.E.; MARKIN, G.P; AND FRIESEN, R. Exploratory survey in Venezuela for biological control agents of Passiflora mollissima in Hawaii. Biological Control, San Diego, v.18, p.110–119, 2000. ; PASTRANA, 2004 PASTRANA, J.A. Los lepidópteros argentinos: sus plantas hospedadoras y otros sustratos alimenticios. Buenos Aires: Sociedad Entomológica Argentina, 2004. p.350. ; BRITO et al. 2013 BRITO, R.; GONÇALVES, G.L.; VARGAS, H.A.; MOREIRA, G.R.P. A new Brazilian Passiflora leafminer: Spinivalva gaucha, gen.n., sp. n. (Lepidoptera, Gracillariidae, Gracillariinae), the first gracillariid without a sap-feeding instar. ZooKeys, Sofia, v.291, p.1–26, 2013. ).

The present work is the first occurrence report of Isia alcumena (Berg, 1882) (Erebidae: Arctiinae), Spodoptera cosmioides (Walker, 1858) and Spodoptera eridania (Stoll, 1782) (Noctuidae: Noctuini) caterpillars attacking sour passion fruit plants (Passiflora edulis Sims) in the Federal District, Brazil.

The caterpillars of I. alcumena (n = 43) were collected on leaves, flowers and fruits of the P. edulis cultivar BRS Rubi do Cerrado in a greenhouse at the Fruit Support Unit, at Embrapa Cerrados, in Planaltina, DF. The S. cosmioides (n = 27) and S. eridania (n = 117) caterpillars were collected while consuming leaves, flowers and fruits of Passiflora edulis intra-specific hybrids located in the Germplasm Active Bank ‘Flor da Paixão’ at Embrapa Cerrados in Planaltina, DF (15°35’30’’S; 47°42’00’’W).

The infestation caused by the larvae of I. Alcumena (December 2018), S. Cosmioides (September 2018) and S. Eridania (January 2019) was recorded (Figure 1).

Figure 1
Owlet moths associated to Passiflora edulis: Isia alcumena - a. caterpillar (35.2 mm long), b. male adult (32.7 mm of wingspan), c. female adult (40.6 mm of wingspan); Spodoptera cosmioides - d. caterpillar (47.8 mm long), e. male adult (37.3 mm of wingspan), f. female adult (42.8 mm of wingspan); Spodoptera eridania – g. caterpillar (36.8 mm long), h. male adult (30.8 mm of wingspan), i. female adult (30.0 mm of wingspan), j. I. alcumena caterpillar eating the leaf of P. edulis, k. S.cosmioides caterpillar eating the leaf of P.edulis, l. S. eridania caterpillar eating the fruit of P.edulis. Photos: Fabiano Bastos.

After collected, the caterpillars were individually placed in transparent plastic containers with lids (30 mL) and fed with leaves of the passion fruit plants where they were found. The development of the caterpillars was monitored until the pupa stage and the emergence of adults. The pupae were kept in moistened containers and with expanded vermiculite. After the emergence, the adults were killed and fixed in entomological pins for permanent dry preservation.

The identification of the emerged adults was performed using bibliographical sources such as from Travassos (1947) TRAVASSOS, L. Contribuição ao conhecimento dos “Arctiidae” XII. Gênero “Isia” Walker, 1856. Revista Brasileira de Biologia, São Carlos, v.7, n.2, p.181-194, 1947. for I. Alcumena, from the taxonomists and author José Augusto Teston and Pogue (2002) for S. Cosmioides and S. Eridania from the taxonomists and author Alexandre Specht. There are records of I. Alcumena caterpillars feeding on one type of arnica (“arnica do mato” - Chromolaena odorata L.) and mango (Mangifera indica L.), (GUAGLIUMI, 1966 GUAGLIUMI, P. Insetti e Arachidi dele piante comuni del Venezuela Segnelati nel período 1938-1963. Relazioni e monografie agrarie subtropicali e tropicali. Istituto Agronomico per l'Oltremare, Firenze, n.86, p.391, 1966. Nuova serie ). On the other side, S. cosmioides are polyphagous and eat leaves of 126 host plants belonging to 40 botanical families (SPECHT e ROQUE-SPECHT, 2016 SPECHT, A.; ROQUE-SPECHT, V.F. Immature stages of Spodoptera cosmioides (Lepidoptera: Noctuidae): developmental parameters and host plants. Zoologia, Curitiba, v.33, n.4, p.1-10, 2016. ). It is important to emphasize that S. eridania caterpillars were found eating P. edulis, in Puerto Rico, during an outbreak after the passage of hurricane Hugo in 1989 (TORRES 1992 TORRES, J.A. Lepidoptera outbreaks in response to successional changes after the passage of Hurricane Hugo in Puerto Rico. Journal Tropical Ecology, Cambridge, v.8, p.285–289, 1992. ). Other authors that mention the association between S. eridania and P. edulis (POGUE 2012 POGUE, G.M. World database Spodoptera (Lepidoptera: Noctuidae). 2012. Disponível em: http://www.sel.barc.usda.gov/lep/spodoptera/spodoptera.html . Acesso em: 10 fev.2019.
http://www.sel.barc.usda.gov/lep/spodopt...
, MONTEZANO et al. 2014 MONTEZANO, D.G.; SPECHT, A.; SOSA-GÓMEZ, D.R.; ROQUE-SPECHT, V.F.; BARROS, N.M. Immature stages of the armyworm, Spodoptera eridania: Developmental parameters and host plants. Journal of Insect Science, Tuckson, v.14, p.1-11, 2014. ) also observed this fact. Therefore, the occurrence of S. eridania causing damages in passion fruits in Brazil is considered as the first record.

Both species of caterpillar belong to the superfamily Noctuoidea, which is represented by different species with a high degree of polyphagia. As for I. alcumena, although the bibliographic record (GUAGLIUMI, 1966 GUAGLIUMI, P. Insetti e Arachidi dele piante comuni del Venezuela Segnelati nel período 1938-1963. Relazioni e monografie agrarie subtropicali e tropicali. Istituto Agronomico per l'Oltremare, Firenze, n.86, p.391, 1966. Nuova serie ) only refers to two host plants (“arnica-do-mato” and mango tree), the current report stating that the caterpillar of I. alcumena eat leaves of P. edulis cv. BRS Rubi do Cerrado represents the capacity of the caterpillars hosting plants of three different botanical families, which is in agreement with several studies that associate many species of the subfamily Arctiinae (Erebidae) with a high degree of polyphagia (ZENKER et al. 2016 ZENKER, M.M.; WAHLBERG, N.; BREHM, G.; TESTON, J.A.; PRZYBYLOWICZ, L.; PIE, M.R.; FREITAS, A.V.L. Systematics and origin of moths in the subfamily Arctiinae (Lepidoptera, Erebidae) in the Neotropical region. Zoologica Scripta, Stockholm, v.46, n.3, p.348–362, 2016. ). As for the polyphagia, several species of the genus Spodoptera are reported as Passifloraceae pests throughout the American continent: S. androgea (JANZEN e HALLWACHS, 2009 JANZEN, D.H.; HALLWACHS, W. Dynamic database for an inventory of the macrocaterpillar fauna, and its food plants and parasitoids, of Area de Conservacion Guanacaste (ACG), northwestern Costa Rica. 2009. (nn-SRNP-nnnnn voucher codes) Disponível em: http://janzen.sas.upenn.edu. ), S. exigua (CAUSTON et al. 2000 CAUSTON, C.E.; MARKIN, G.P; AND FRIESEN, R. Exploratory survey in Venezuela for biological control agents of Passiflora mollissima in Hawaii. Biological Control, San Diego, v.18, p.110–119, 2000. ), S. frugiperda (MONTEZANO et al. 2018 MONTEZANO, D.G.; SPECHT, A.; SOSA-GÓMEZ, D.R.; ROQUE-SPECHT, V.F.; SOUSA-SILVA, J.C.; PAULA-MORAES, S.V. Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. African Entomology, Hatfield, v.26, n.2, p.286-300, 2018. ) and S. ornithogalli (CHACON e ROJAS, 1984 CHACON, P.; ROJAS, M. Entomofauna asociada a Passiflora mollissima, P. edulis f. flavicarpa y P. quadrangularis en el Departamento del Valle del Cauca.Turrialba, Costa Rica, v.34, p.297-311, 1984. ).

The first occurrence record of these caterpillars attacking passion fruits is an alert to make individuals aware that studies on bioecology and behavior are necessary. In the future, these studies will provide information so that if these species become pests, they will be managed more efficiently.

Acknowledgments

The authors would like to thank Willian Rogers Ferreira de Camargo for helping them to collect, grow and preserve the samples and also Fabiano Marques Dourado Bastos for the photos of immature and adult samples.

  • BERNACCI, L. C.; CERVI, A. C.; MILWARD-DE-AZEVEDO, M. A.; NUNES, T. S., IMIG, D.C.; MEZZONATO, A.C. Passifloraceae. Lista de Espécies da Flora do Brasil. Rio de Janeiro: Jardim Botânico do Rio de Janeiro, 2013. Disponível em: http://floradobrasil.jbrj.gov.br/.
  • BRITO, R.; GONÇALVES, G.L.; VARGAS, H.A.; MOREIRA, G.R.P. A new Brazilian Passiflora leafminer: Spinivalva gaucha, gen.n., sp. n. (Lepidoptera, Gracillariidae, Gracillariinae), the first gracillariid without a sap-feeding instar. ZooKeys, Sofia, v.291, p.1–26, 2013.
  • CAUSTON, C.E.; MARKIN, G.P; AND FRIESEN, R. Exploratory survey in Venezuela for biological control agents of Passiflora mollissima in Hawaii. Biological Control, San Diego, v.18, p.110–119, 2000.
  • CHACON, P.; ROJAS, M. Entomofauna asociada a Passiflora mollissima, P. edulis f. flavicarpa y P. quadrangularis en el Departamento del Valle del Cauca.Turrialba, Costa Rica, v.34, p.297-311, 1984.
  • FALEIRO, F.G.; JUNQUEIRA, N.T.V.; BRAGA, M.F.; COSTA, A.M. Conservação e caracterização de espécies silvestres de maracujazeiro (Passiflora spp.) e utilização potencial no melhoramento genético, como porta-enxertos, alimentos funcionais, plantas ornamentais e medicinais - resultados de pesquisa. Planaltina: Embrapa Cerrados, 2012. 34p. (Documentos, 312)
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  • GUAGLIUMI, P. Insetti e Arachidi dele piante comuni del Venezuela Segnelati nel período 1938-1963. Relazioni e monografie agrarie subtropicali e tropicali. Istituto Agronomico per l'Oltremare, Firenze, n.86, p.391, 1966. Nuova serie
  • JANZEN, D.H.; HALLWACHS, W. Dynamic database for an inventory of the macrocaterpillar fauna, and its food plants and parasitoids, of Area de Conservacion Guanacaste (ACG), northwestern Costa Rica. 2009. (nn-SRNP-nnnnn voucher codes) Disponível em: http://janzen.sas.upenn.edu.
  • 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, Orlando, v.82, p.156-165, 2015.
  • MESSENGER, C. The Sphinx Moths (Lepidoptera: Sphingidae) of Nebraska. Transactions of the Nebraska Academy of Sciences, Lincoln, v.24, p.89-141, 1997.
  • MILLER, J.S. Generic revision of the Dioptinae (Lepidoptera: Noctuoidea: Notodontidae). Part 2: Josiini. Bulletin of the American Museum of Natural History, New York, v.321, p.675–1022, 2009.
  • MONTEZANO, D.G.; SPECHT, A.; SOSA-GÓMEZ, D.R.; ROQUE-SPECHT, V.F.; BARROS, N.M. Immature stages of the armyworm, Spodoptera eridania: Developmental parameters and host plants. Journal of Insect Science, Tuckson, v.14, p.1-11, 2014.
  • MONTEZANO, D.G.; SPECHT, A.; SOSA-GÓMEZ, D.R.; ROQUE-SPECHT, V.F.; SOUSA-SILVA, J.C.; PAULA-MORAES, S.V. Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. African Entomology, Hatfield, v.26, n.2, p.286-300, 2018.
  • PASTRANA, J.A. Los lepidópteros argentinos: sus plantas hospedadoras y otros sustratos alimenticios. Buenos Aires: Sociedad Entomológica Argentina, 2004. p.350.
  • POGUE, G.M. World database Spodoptera (Lepidoptera: Noctuidae). 2012. Disponível em: http://www.sel.barc.usda.gov/lep/spodoptera/spodoptera.html . Acesso em: 10 fev.2019.
    » http://www.sel.barc.usda.gov/lep/spodoptera/spodoptera.html
  • POGUE, M.G. A world revision of the genus Spodoptera Guenée (Lepidoptera: Noctuidae). Memoirs of the American Entomological Society, Philadelphia, v.43, p.1–202, 2002.
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  • SPECHT, A.; ROQUE-SPECHT, V.F. Immature stages of Spodoptera cosmioides (Lepidoptera: Noctuidae): developmental parameters and host plants. Zoologia, Curitiba, v.33, n.4, p.1-10, 2016.
  • TORRES, J.A. Lepidoptera outbreaks in response to successional changes after the passage of Hurricane Hugo in Puerto Rico. Journal Tropical Ecology, Cambridge, v.8, p.285–289, 1992.
  • TRAVASSOS, L. Contribuição ao conhecimento dos “Arctiidae” XII. Gênero “Isia” Walker, 1856. Revista Brasileira de Biologia, São Carlos, v.7, n.2, p.181-194, 1947.
  • VIEIRA, M.L.C.; CARNEIRO, M.C. Passiflora spp. Passionfruit. In: LITZ, R. (ed.). Biotechnology of fruit and nut crops. Gainesville: University of Florida, 2004. p.436-453.
  • ZENKER, M.M.; WAHLBERG, N.; BREHM, G.; TESTON, J.A.; PRZYBYLOWICZ, L.; PIE, M.R.; FREITAS, A.V.L. Systematics and origin of moths in the subfamily Arctiinae (Lepidoptera, Erebidae) in the Neotropical region. Zoologica Scripta, Stockholm, v.46, n.3, p.348–362, 2016.

Publication Dates

  • Publication in this collection
    14 Nov 2019
  • Date of issue
    2019

History

  • Received
    13 Mar 2019
  • Accepted
    11 July 2019
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