Acessibilidade / Reportar erro

Pupal parasitoids of Antichloris eriphia (Fabr.) (Lepidoptera: Erebidae) in the Agreste region of the Alagoas state, northeastern Brazil

Brazil is the world's fourth largest producer of Musa spp. (Musaceae) with annual production of 6,953,747 tons (Pereira et al., 2022aPEREIRA, B.S., FREITAS, C., VIEIRA, R.M. and BRIENZO, M., 2022a. Brazilian banana, guava, and orange fruit and waste production as a potential biorefinery feedstock. Journal of Material Cycles and Waste Management, vol. 24, no. 6, pp. 2126-2140. http://dx.doi.org/10.1007/s10163-022-01495-6.
http://dx.doi.org/10.1007/s10163-022-014...
) in a planted area of ​​ 457.910 ha, the second among cultivated fruits (IBGE, 2022INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA - IBGE, 2022 [viewed 28 July 2023]. Produção de banana[online]. Available from: https://www.ibge.gov.br/explica/producao-agropecuaria/banana/br
https://www.ibge.gov.br/explica/producao...
). Insect defoliators, pseudostem and rhizome borers, and root, fruit and flower pests, and sucking insect vectors of diseases, damage banana plants, Musa spp. (Krishnan et al., 2020KRISHNAN, J.U., JAYAPRAKAS, C.A., HARISH, E.R. and RAJESWARI, L.S., 2020. Banana (Musa spp.)-an unseen umbrella crop? Insect diversity on Musa spp. in the Indo-Pacific region. Oriental Insects, vol. 54, no. 3, pp. 433-445. http://dx.doi.org/10.1080/00305316.2019.1667926.
http://dx.doi.org/10.1080/00305316.2019....
).

Antichloris eriphia Fabricius, 1777 (Lepidoptera: Erebidae) occurs in southeast Brazil, Colombia, Ecuador, Paraguay and Suriname damaging banana plants and has been reported in banana importing countries (Draudt, 1917DRAUDT, M., 1917. Family Syntomidae. In Seitz, A. Die Gross-Schmetterlinge des Amerikanischen Faunengebietes. 6. ed. Stuttgart: Alfred Kernen, 1452 p., Die amerikanischen Spinner und Schwärmer.; Schaus, 1938SCHAUS, W., 1938. New species of American Heterocera in the United States National Museum (Lepidoptera). Annals & Magazine of Natural History, vol. 11, no. 2, pp. 504-517. http://dx.doi.org/10.1080/00222933808526880.
http://dx.doi.org/10.1080/00222933808526...
; Field, 1975FIELD, W.D., 1975. Ctenuchid moths of Ceramidia Butler, Ceramidiodes Hampson, and the caca species group of Antichloris Hübner. Washington: Smithsonian Institution Press, 45 p., Smithsonian Contributions to Zoology, no. 198.; Chalumeau and Delplanque 1978CHALUMEAU, F. and DELPLANQUE, A., 1978. Catalogue commenté des Ctenuchidae (Lepidoptera) des Antilles Françaises. Bulletin Mensuel de la Societe Linneenne de Lyon, vol. 47, no. 4, pp. 176-187. http://dx.doi.org/10.3406/linly.1978.10304.
http://dx.doi.org/10.3406/linly.1978.103...
; Gernaat, 2016GERNAAT, H.B., 2016. Notes on the early stages of Antichloris eriphia (Erebidae: Arctiinae) in Suriname. The Journal of the Lepidopterists' Society, vol. 70, no. 4, pp. 311-314. https://doi.org/10.18473/lepi.70i4.a10.
https://doi.org/10.18473/lepi.70i4.a10...
).

Caterpillars of A. eriphia which perforate and destroy the leaf area of Musa spp. and use Heliconia latispatha Benth. (Heliconiaceae) in Brazil, as intermediate host (Watanabe, 2007WATANABE, M.A., 2007. Pragas da bananeira atacando Heliconia latispatha Benth. (Heliconiaceae). Neotropical Entomology, vol. 36, no. 2, pp. 312-313. http://dx.doi.org/10.1590/S1519-566X2007000200021. PMid:17607468.
http://dx.doi.org/10.1590/S1519-566X2007...
), is one of the main moth species defoliator of banana plants reducing its photosynthetic area and assimilated material translocated from the rhizome to the fruit (Ostmark, 1974OSTMARK, H.E., 1974. Economic insect pests of bananas. Annual Review of Entomology, vol. 19, no. 1, pp. 161-176. http://dx.doi.org/10.1146/annurev.en.19.010174.001113.
http://dx.doi.org/10.1146/annurev.en.19....
).

Biological control methods of A. eriphia are scarce and the egg parasitoid Trichogramma sp. (Hymenoptera: Trichogrammatidae) is the only natural enemy of this pest reported in Musa spp. plantations in Brazil (Souza et al., 2016SOUZA, A.R., GIUSTOLIN, T.A., QUERINO, R.B. and ALVARENGA, C.D., 2016. Natural parasitism of lepidopteran eggs by Trichogramma species (Hymenoptera: Trichogrammatidae) in agricultural crops in Minas Gerais, Brazil. The Florida Entomologist, vol. 99, no. 2, pp. 221-225. http://dx.doi.org/10.1653/024.099.0210.
http://dx.doi.org/10.1653/024.099.0210...
). Parasitoids of the Hymenoptera order are efficient and more specific and, therefore, a sustainable method of biological control in the management of arthropod pest populations (Pinheiro et al., 2022PINHEIRO, R.A., ZANUNCIO, J.C., TOMA, R., ISAAC, J.B., SOARES, M.A., SANTOS, C.A., SERRÃO, J.E., CABRAL, M.J.S. and TAVARES, M.T., 2022. Brachymeria koehleri (Hymenoptera: Chalcididae): first record as hyperparasitoid in Dione juno juno (Lepidoptera: Nymphalidae) pupae. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 82, no. 1, pp. e260645. http://dx.doi.org/10.1590/1519-6984.260645. PMid:36515296.
http://dx.doi.org/10.1590/1519-6984.2606...
).

The objective is to report, for the first time, the parasitism of A. eriphia by Tetrastichus howardi Olliff, 1893 and Trichospilus diatraeae Cherian & Margabandhu, 1942 (Hymenoptera: Eulophidae) pupae on Heliconia psittacorum L.F. and Heliconia stricta Huber (Heliconiaceae) plants in an urbanized area of the Agreste region of Alagoas state, Brazil.

Caterpillars and pupae of A. eriphia were collected on H. psittacorum and H. stricta plants in the garden of the Universidade Estadual do Alagoas (09°45'09''S; 36°39'40''W) Campus I, in the municipality of Arapiraca, Alagoas state, Brazil.

Twenty A. eriphia pupa were collected using a 50 ml falcon tube, placed in containers and taken to the laboratory where they were individualized in Petri plates (60 x 15 mm area). Three pupae of the 20 collected were parasitized and 225 similar parasitoids emerged from two of them, while a second type emerged from the third parasitized pupa. The parasitoid wasps, emerged from A. eriphia pupae, were identified by one of the authors (VAC) as Trichospilus diatraeae Cherian & Margabandhu, 1942 and T. howardi. The identification of T. diatraeae was performed according to Bouček (1976)BOUČEK, Z., 1976. The African and Asiatic species of Trichospilus and Cotterellia (Hymenoptera, Eulophidae). Bulletin of Entomological Research, vol. 65, no. 4, pp. 669-681. http://dx.doi.org/10.1017/S0007485300006362.
http://dx.doi.org/10.1017/S0007485300006...
and Narendran (2011)NARENDRAN, T.C., 2011. Fauna of India, Eulophinae (Hymenoptera: Eulophidae). Calcutta: Zoological Survey of India, 442 p. and T. howardi based on La Salle and Polaszek (2007)LA SALLE, J. and POLASZEK, A., 2007. Afrotropical species of the Tetrastichus howardi species group (Hymenoptera: Eulophidae). African Entomology, vol. 15, no. 1, pp. 45-56. http://dx.doi.org/10.4001/1021-3589-15.1.45.
http://dx.doi.org/10.4001/1021-3589-15.1...
.

Two hundred and twenty-five individuals of T. diatraeae emerged from three pupae of A. eriphia, and ten T. howardi from one pupa of this insect host (Figure 1 A & B), among the 20 collected on H. psittacorum and H. stricta plants in Arapiraca, Agreste region of the Alagoas state, Brazil. Voucher specimens of the parasitoid wasps were deposited in the “Oscar Monte” Entomophagous Insect Collection at the Instituto Biológico in Campinas, São Paulo state, Brazil, under reference number IB-CBE-S-852 (curator: Valmir A. Costa).

Figure 1
Females of Tetrastichus howardi (A) and Trichospilus diatraeae (B) (Hymenoptera: Eulophidae).

Parasitism of A. eriphia pupae by T. diatraeae and T. howardi increases the number of natural enemies of A. eriphia, after the report of Trichogramma spp. (Hymenoptera: Trichogrammatidae) parasitizing eggs of this pest in the semi-arid region of the Minas Gerais state, Brazil (Souza et al., 2016SOUZA, A.R., GIUSTOLIN, T.A., QUERINO, R.B. and ALVARENGA, C.D., 2016. Natural parasitism of lepidopteran eggs by Trichogramma species (Hymenoptera: Trichogrammatidae) in agricultural crops in Minas Gerais, Brazil. The Florida Entomologist, vol. 99, no. 2, pp. 221-225. http://dx.doi.org/10.1653/024.099.0210.
http://dx.doi.org/10.1653/024.099.0210...
). Trichospilus diatraeae was also reported from Helicoverpa armigera Hübner, 1805 (Lepidoptera: Noctuidae) and Thyrinteina arnobia Stoll & Cramer, 1782 (Lepidoptera: Geometridae) pupae (Pereira et al., 2008PEREIRA, F.F., ZANUNCIO, J.C., TAVARES, M.T., PASTORI, P.L., JACQUES, G.C. and VILELA, E.F., 2008. New record of Trichospilus diatraeae as a parasitoid of the eucalypt defoliator Thyrinteina arnobia in Brazil. Phytoparasitica, vol. 36, no. 1, pp. 304-306. http://dx.doi.org/10.1007/BF02980777.
http://dx.doi.org/10.1007/BF02980777...
; Oliveira et al., 2016OLIVEIRA, H.N., SIMONATO, J., GLAESER, D.F. and PEREIRA, F.F., 2016. Parasitism of Helicoverpa armigera pupae (Lepidoptera: Noctuidae) by Tetrastichus howardi and Trichospilus diatraeae (Hymenoptera: Eulophidae). Semina: Ciências Agrárias, vol. 37, no. 1, pp. 111-115. http://dx.doi.org/10.5433/1679-0359.2016v37n1p111.
http://dx.doi.org/10.5433/1679-0359.2016...
). Tetrastichus howardi parasitized pests in different crops, including the sugarcane stem borer Diatraea saccharalis Fabricius, 1794 (Lepidoptera: Crambidae), the crucifer moth Plutella xylostella Linnaeus, 1758 (Lepidoptera: Plutellidae) and the cassava moth Erinnyis ello Linnaeus, 1758 (Lepidoptera: Sphingidae) (Barbosa et al., 2015BARBOSA, R.H., KASSAB, S.O., PEREIRA, F.F., ROSSONI, C., COSTA, D.P. and BERNDT, M.A., 2015. Parasitism and biological aspects of Tetrastichus howardi (Hymenoptera: Eulophidae) on Erinnyis ello (Lepidoptera: Sphingidae) pupae. Ciência Rural, vol. 45, no. 2, pp. 185-188. http://dx.doi.org/10.1590/0103-8478cr20130896.
http://dx.doi.org/10.1590/0103-8478cr201...
; Favero et al., 2015FAVERO, K., PEREIRA, F.F., TORRES, J.B., OLIVEIRA, H.N., KASSAB, S.O. and ZANUNCIO, J.C., 2015. Reproduction of Tetrastichus howardi (Hymenoptera: Eulophidae) in Diatraea saccharalis (Lepidoptera: Crambidae) pupae at different temperatures. The Florida Entomologist, vol. 98, no. 3, pp. 865-869. http://dx.doi.org/10.1653/024.098.0308.
http://dx.doi.org/10.1653/024.098.0308...
; Pereira et al., 2022b PEREIRA, H.C., PEREIRA, F.F., FERNANDES, W.C., CARNEIRO, Z.F., LUCCHETTA, J.T., ANDRADE, G.S. and ZANUNCIO, J.C., 2022b. Parasitism rate of Plutella xylostella (Lepidoptera: Plutellidae) larvae in greenhouse by Tetrastichus howardi (Hymenoptera: Eulophidae) females at different densities. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 82, no. 1, pp. e263443. http://dx.doi.org/10.1590/1519-6984.263443. PMid:36228286.
http://dx.doi.org/10.1590/1519-6984.2634...
).

The record of T. diatraeae and T. howardi parasitizing A. eriphia pupae increases the number of natural enemies of this defoliating lepidopteran, being the first record of these parasitoids associated with A. eriphia in Brazil, as well as in the urbanized area of the Arapiraca municipality in the Agreste region of the Alagoas state, northeastern Brazil.

Acknowledgements

To the Brazilian institutions “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES- Finance Code 001)”, “Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)” and “Programa Cooperativo sobre Proteção Florestal (PROTEF)” do “Instituto de Pesquisas e Estudos Florestais (IPEF)”. IVAC thanks the INCT-Hympar (Instituto Nacional de Ciência e Tecnologia dos Hymenoptera Parasitoides, CNPq Process 465562/2014-0) for financial support.

References

  • BARBOSA, R.H., KASSAB, S.O., PEREIRA, F.F., ROSSONI, C., COSTA, D.P. and BERNDT, M.A., 2015. Parasitism and biological aspects of Tetrastichus howardi (Hymenoptera: Eulophidae) on Erinnyis ello (Lepidoptera: Sphingidae) pupae. Ciência Rural, vol. 45, no. 2, pp. 185-188. http://dx.doi.org/10.1590/0103-8478cr20130896
    » http://dx.doi.org/10.1590/0103-8478cr20130896
  • BOUČEK, Z., 1976. The African and Asiatic species of Trichospilus and Cotterellia (Hymenoptera, Eulophidae). Bulletin of Entomological Research, vol. 65, no. 4, pp. 669-681. http://dx.doi.org/10.1017/S0007485300006362
    » http://dx.doi.org/10.1017/S0007485300006362
  • CHALUMEAU, F. and DELPLANQUE, A., 1978. Catalogue commenté des Ctenuchidae (Lepidoptera) des Antilles Françaises. Bulletin Mensuel de la Societe Linneenne de Lyon, vol. 47, no. 4, pp. 176-187. http://dx.doi.org/10.3406/linly.1978.10304
    » http://dx.doi.org/10.3406/linly.1978.10304
  • DRAUDT, M., 1917. Family Syntomidae. In Seitz, A. Die Gross-Schmetterlinge des Amerikanischen Faunengebietes 6. ed. Stuttgart: Alfred Kernen, 1452 p., Die amerikanischen Spinner und Schwärmer.
  • FAVERO, K., PEREIRA, F.F., TORRES, J.B., OLIVEIRA, H.N., KASSAB, S.O. and ZANUNCIO, J.C., 2015. Reproduction of Tetrastichus howardi (Hymenoptera: Eulophidae) in Diatraea saccharalis (Lepidoptera: Crambidae) pupae at different temperatures. The Florida Entomologist, vol. 98, no. 3, pp. 865-869. http://dx.doi.org/10.1653/024.098.0308
    » http://dx.doi.org/10.1653/024.098.0308
  • FIELD, W.D., 1975. Ctenuchid moths of Ceramidia Butler, Ceramidiodes Hampson, and the caca species group of Antichloris Hübner Washington: Smithsonian Institution Press, 45 p., Smithsonian Contributions to Zoology, no. 198.
  • GERNAAT, H.B., 2016. Notes on the early stages of Antichloris eriphia (Erebidae: Arctiinae) in Suriname. The Journal of the Lepidopterists' Society, vol. 70, no. 4, pp. 311-314. https://doi.org/10.18473/lepi.70i4.a10
    » https://doi.org/10.18473/lepi.70i4.a10
  • INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA - IBGE, 2022 [viewed 28 July 2023]. Produção de banana[online]. Available from: https://www.ibge.gov.br/explica/producao-agropecuaria/banana/br
    » https://www.ibge.gov.br/explica/producao-agropecuaria/banana/br
  • KRISHNAN, J.U., JAYAPRAKAS, C.A., HARISH, E.R. and RAJESWARI, L.S., 2020. Banana (Musa spp.)-an unseen umbrella crop? Insect diversity on Musa spp. in the Indo-Pacific region. Oriental Insects, vol. 54, no. 3, pp. 433-445. http://dx.doi.org/10.1080/00305316.2019.1667926
    » http://dx.doi.org/10.1080/00305316.2019.1667926
  • LA SALLE, J. and POLASZEK, A., 2007. Afrotropical species of the Tetrastichus howardi species group (Hymenoptera: Eulophidae). African Entomology, vol. 15, no. 1, pp. 45-56. http://dx.doi.org/10.4001/1021-3589-15.1.45
    » http://dx.doi.org/10.4001/1021-3589-15.1.45
  • NARENDRAN, T.C., 2011. Fauna of India, Eulophinae (Hymenoptera: Eulophidae) Calcutta: Zoological Survey of India, 442 p.
  • OLIVEIRA, H.N., SIMONATO, J., GLAESER, D.F. and PEREIRA, F.F., 2016. Parasitism of Helicoverpa armigera pupae (Lepidoptera: Noctuidae) by Tetrastichus howardi and Trichospilus diatraeae (Hymenoptera: Eulophidae). Semina: Ciências Agrárias, vol. 37, no. 1, pp. 111-115. http://dx.doi.org/10.5433/1679-0359.2016v37n1p111
    » http://dx.doi.org/10.5433/1679-0359.2016v37n1p111
  • OSTMARK, H.E., 1974. Economic insect pests of bananas. Annual Review of Entomology, vol. 19, no. 1, pp. 161-176. http://dx.doi.org/10.1146/annurev.en.19.010174.001113
    » http://dx.doi.org/10.1146/annurev.en.19.010174.001113
  • PEREIRA, F.F., ZANUNCIO, J.C., TAVARES, M.T., PASTORI, P.L., JACQUES, G.C. and VILELA, E.F., 2008. New record of Trichospilus diatraeae as a parasitoid of the eucalypt defoliator Thyrinteina arnobia in Brazil. Phytoparasitica, vol. 36, no. 1, pp. 304-306. http://dx.doi.org/10.1007/BF02980777
    » http://dx.doi.org/10.1007/BF02980777
  • PEREIRA, B.S., FREITAS, C., VIEIRA, R.M. and BRIENZO, M., 2022a. Brazilian banana, guava, and orange fruit and waste production as a potential biorefinery feedstock. Journal of Material Cycles and Waste Management, vol. 24, no. 6, pp. 2126-2140. http://dx.doi.org/10.1007/s10163-022-01495-6
    » http://dx.doi.org/10.1007/s10163-022-01495-6
  • PEREIRA, H.C., PEREIRA, F.F., FERNANDES, W.C., CARNEIRO, Z.F., LUCCHETTA, J.T., ANDRADE, G.S. and ZANUNCIO, J.C., 2022b. Parasitism rate of Plutella xylostella (Lepidoptera: Plutellidae) larvae in greenhouse by Tetrastichus howardi (Hymenoptera: Eulophidae) females at different densities. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 82, no. 1, pp. e263443. http://dx.doi.org/10.1590/1519-6984.263443 PMid:36228286.
    » http://dx.doi.org/10.1590/1519-6984.263443
  • PINHEIRO, R.A., ZANUNCIO, J.C., TOMA, R., ISAAC, J.B., SOARES, M.A., SANTOS, C.A., SERRÃO, J.E., CABRAL, M.J.S. and TAVARES, M.T., 2022. Brachymeria koehleri (Hymenoptera: Chalcididae): first record as hyperparasitoid in Dione juno juno (Lepidoptera: Nymphalidae) pupae. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 82, no. 1, pp. e260645. http://dx.doi.org/10.1590/1519-6984.260645 PMid:36515296.
    » http://dx.doi.org/10.1590/1519-6984.260645
  • SCHAUS, W., 1938. New species of American Heterocera in the United States National Museum (Lepidoptera). Annals & Magazine of Natural History, vol. 11, no. 2, pp. 504-517. http://dx.doi.org/10.1080/00222933808526880
    » http://dx.doi.org/10.1080/00222933808526880
  • SOUZA, A.R., GIUSTOLIN, T.A., QUERINO, R.B. and ALVARENGA, C.D., 2016. Natural parasitism of lepidopteran eggs by Trichogramma species (Hymenoptera: Trichogrammatidae) in agricultural crops in Minas Gerais, Brazil. The Florida Entomologist, vol. 99, no. 2, pp. 221-225. http://dx.doi.org/10.1653/024.099.0210
    » http://dx.doi.org/10.1653/024.099.0210
  • WATANABE, M.A., 2007. Pragas da bananeira atacando Heliconia latispatha Benth. (Heliconiaceae). Neotropical Entomology, vol. 36, no. 2, pp. 312-313. http://dx.doi.org/10.1590/S1519-566X2007000200021 PMid:17607468.
    » http://dx.doi.org/10.1590/S1519-566X2007000200021

Publication Dates

  • Publication in this collection
    18 Mar 2024
  • Date of issue
    2024

History

  • Received
    28 July 2023
  • Accepted
    24 Jan 2024
Instituto Internacional de Ecologia R. Bento Carlos, 750, 13560-660 São Carlos SP - Brasil, Tel. e Fax: (55 16) 3362-5400 - São Carlos - SP - Brazil
E-mail: bjb@bjb.com.br