Passion fruits are nutritious for fresh and industrial consumption (Zhang et al., 2021ZHANG, X., WEI, X., ALI, M.M., RIZWAN, H.M., LI, B., LI, H., JIA, K., YANG, X., MA, S., LI, S. and CHEN, F., 2021. Changes in the content of organic acids and expression analysis of citric acid accumulation-related genes during fruit development of yellow (Passifora edulis f favicarpa) and Purple (Passifora edulis f edulis) Passion Fruits. International Journal of Molecular Sciences, vol. 22, no. 11, pp. 5765. http://dx.doi.org/10.3390/ijms22115765. PMid:34071242.
http://dx.doi.org/10.3390/ijms22115765...
). Insect pests, such as defoliating caterpillars, including Dione juno juno (Cramer, 1779) (Lepidoptera: Nymphalidae), defoliate completely Passiflora spp. plants (Passifloraceae) at high population densities (Boiça Júnior et al., 2008BOIÇA JÚNIOR, A.L., ANGELINI, M.R. and OLIVEIRA, J.C.D., 2008. Aspectos biológicos de Dione juno juno (Cramer) (Lepidoptera: Nymphalidae) em genótipos de maracujazeiro. Revista Brasileira de Fruticultura, vol. 30, no. 1, pp. 101-105. http://dx.doi.org/10.1590/S0100-29452008000100019.
http://dx.doi.org/10.1590/S0100-29452008...
).
Biological control is an environmentally safe method to manage harmful arthropods. Parasitoid insects are known for their effectiveness and specificity as biological control agents and they are mainly of the Diptera and Hymenoptera orders (Scaramozzino et al., 2020SCARAMOZZINO, P.L., DI GIOVANNI, F., LONI, A., GISONDI, S., LUCCHI, A. and CERRETTI, P., 2020. Tachinid (Diptera, Tachinidae) parasitoids of Lobesia botrana (Denis & Schiffermüller, 1775) (Lepidoptera, Tortricidae) and other moths. ZooKeys, vol. 934, pp. 111-140. http://dx.doi.org/10.3897/zookeys.934.50823. PMid:32508497.
http://dx.doi.org/10.3897/zookeys.934.50...
).
Seventy-three species have been described for the genus Chetogena (Rondani, 1856) (Diptera: Tachinidae) (O’Hara et al., 2019O’HARA, J.E., HENDERSON, S.J. and WOOD, D.M., 2019. Preliminary checklist of the Tachinidae of the world, NADS, 681 pp. [online]. Available from: http://www.nadsdiptera.org/Tach/WorldTachs/Checklist/Worldchecklist.html
http://www.nadsdiptera.org/Tach/WorldTac...
, 2021O’HARA, J.E., WOOD, D.M. and GONZALEZ, C.R., 2021. Annotated Catalogue of Tachinidae (Insecta, Diptera) of the Chile. Zookeys, vol. 1064, no. 1988, pp. 1-200. https://doi.org/10.3897/zookeys.1064.62972.
https://doi.org/10.3897/zookeys.1064.629...
), including Chetogena scutellaris (Wulp, 1890) (Diptera: Tachinidae) (O’Hara et al., 2019O’HARA, J.E., HENDERSON, S.J. and WOOD, D.M., 2019. Preliminary checklist of the Tachinidae of the world, NADS, 681 pp. [online]. Available from: http://www.nadsdiptera.org/Tach/WorldTachs/Checklist/Worldchecklist.html
http://www.nadsdiptera.org/Tach/WorldTac...
), an endoparasitoid of Arctiidae, Geometridae, Noctuidae, Pieridae, Saturniidae, Sphingidae and Zygaenidae (Lepidoptera) caterpillars (Arnaud, 1978ARNAUD, P.H., 1978. A host-parasite catalog of North American Tachinidae (Diptera). Department of Agriculture. Science and Education Administration, vol. 1, no. 1319, pp. 860.).
Chalcididae are usually primary and solitary endoparasitoids, but some of its species are gregarious parasitoids or hyperparasitoids of Coleoptera, Diptera, Hymenoptera and Lepidoptera (Narendran and Van Achterberg, 2016NARENDRAN, T.C. and VAN ACHTERBERG, C., 2016. Revision of the family Chalcididae (Hymenoptera, Chalcidoidea) from Vietnam, with the description of 13 new species. ZooKeys, vol. 576, pp. 1-202. PMid:27110185.).
This study reports the first record of Brachymeria koehleri (Blanchard, 1935) (Hymenoptera: Chalcididae) as a hyperparasitoid in D. juno juno pupae trough C. aff. scutellaris. It also registers, for the first time, the association of a Chetogena species with D. juno juno in South America.
Forty-one lepidopteran pupae were collected from Passiflora edulis (Passifloraceae) plants in the Horticulture sector (S 18º 12’12,276”, W 43º34’16.86; 1,387 m.a.s.l.) of the Universidade Federal dos Vales do Jequitinhonha e Mucuri (UFVJM) in Diamantina, State of Minas Gerais, Brazil.
Adults of Lepidoptera emerged in the laboratory were kept in a cage (33 × 33 × 33 cm), photographed, and sent to Dr. Olaf Hermann Hendrik Mielke (Universidade Federal do Paraná, Biological Sciences Sector, Department of Zoology, Curitiba, State of Paraná, Brazil), who identified the species as Dione juno juno (Lepidoptera: Nymphalidae).
Pupae of D. juno juno were dissected and the puparia of dipteran parasitoids found transferred to a 500 ml plastic pots until emergence of adult of dipteran parasitoid or hyperparasitoids.
Specimens of Tachinidae flies that emerged from D. juno juno pupae were fixed in 70% ethanol and sent to the taxonomist Dr. Ronaldo Toma (FIOCRUZ Mato Grosso do Sul, Campo Grande, State of Mato Grosso do Sul, Brazil). These specimens were identified based on Parchami-Araghi’s (2008)PARCHAMI-ARAGHI, M., 2008. Identity of the previously unrecognized Chetogena flaviceps and its synonymy with C. scutellaris (Diptera: tachinidae). Journal of Entomological Society of Iran, vol. 28, no. 1, pp. 61-66. and Thompson’s (1968)THOMPSON, W.R., 1968. The Tachinids of Trinidad. VIII. Phorocerines. Memoirs of the Entomological Society of Canada, vol. 100, no. suppl S56, pp. 5-207. http://dx.doi.org/10.4039/entm10056fv.
http://dx.doi.org/10.4039/entm10056fv...
redescriptions, and voucher specimens were deposited in the Zoological Reference Collection at the Universidade Federal do Mato Grosso do Sul, Brazil.
Specimens of Chalcididae that emerged from Tachinidae pupae were fixed in 70% ethanol and sent to the taxonomist Dr. Marcelo Teixeira Tavares (Universidade Federal do Espírito Santo, Department of Biological Sciences, in Vitória, State of Espírito Santo, Brazil). These specimens were identified based on the key of Andrade and Tavares (2009)ANDRADE, T.V. and TAVARES, M.T., 2009. Revisão de Ceyxia, stat. rev., (Hymenoptera, Chalcididae, Brachymeriini). Revista Brasileira de Entomologia, vol. 53, no. 4, pp. 511-548., the description of Blanchard (1935)BLANCHARD, E.E., 1935. Apuntes sobre calcididos argentinos (Hym. Chalc.). Revista de la Sociedad Entomológica Argentina, vol. 7, pp. 103-122., and compared with the holotype of B. koehleri deposited in the Collection of IMYZA (Instituto de Microbiología y Zoología Agrícola at Hurlingham, Buenos Aires, Argentina).
The flies, wasps and chrysalis were photographed using a Canon EOS Rebel T7I camera and Segurimax© LED lights.
Eight C. aff. scutellaris larvae emerged from D. juno juno pupae (Figure 1A, C). This is the first record of a species of Chetogena parasitizing pupae of D. juno juno in South America. Chetogena scutellaris has been reported in D. juno juno pupae in Costa Rica (Janzen and Hallwachs, 2009JANZEN, D.H. and HALLWACHS, W., 2009 [viewed 22 February 2022]. Dynamic database for an inventory of the macrocaterpillar fauna, and its food plants and parasitoids, of Area de Conservacion Guanacaste (ACG), northwestern Costa Rica (nn-SRNP-nnnnn voucher codes) [online]. Available from: http://janzen.sas.upenn.edu
http://janzen.sas.upenn.edu...
). This parasitoid has also been obtained from pupae of Anaea troglodyta (Fabricius, 1775), Brassolis sophorae (Linnaeus, 1758) and Opsiphanes invirae (Huebner, 1818) (Lepidoptera: Nymphalidae) in the State of Pará, Brazil, and in the state of Florida, United States (Tinôco et al., 2010TINÔCO, R.S., RIBEIRO, R.C., VILELA, E.F., LEMOS, W.D.P., ZANUNCIO, J.C. and NIHEI, S.S., 2010. Primeiro registro de Chetogena scutellaris Wulp (Diptera: Tachinidae) parasitando pupas de Opsiphanes invirae e Brassolis sophorae (Lepidoptera: Nymphalidae) no Pará, Brasil. In: EMBRAPA AMAZÔNIA ORIENTAL. Resumo do 23° Anais do Congresso (ALICE). Congresso Brasileiro de Entomologia, 2010, Natal. Natal: Sociedade Brasileira de Entomologia.; Salvato et al., 2009SALVATO, M.H., SALVATO, H.L. and HENNESSEY, M.K., 2009. Chetogena scutellaris (Diptera: Tachinidae) an endoparasite of larval Anaea troglodyta floridalis (Nymphalidae). Journal of the Lepidopterists Society, vol. 66, no. 2, pp. 113-114. http://dx.doi.org/10.18473/lepi.v66i2.a5.
http://dx.doi.org/10.18473/lepi.v66i2.a5...
). Furthermore, C. scutellaris has been recorded from pupae of Anticarsia gemmatalis (Hübner, 1818), Alabama claycea (Hübner, 1823), Chrysodeixis includens (Walker, 1857), Helicoverpa zea (Boddie, 1850), Pseudaletia unipuncta (Haworth, 1809), Spodoptera eridania (Stoll, 1781), Spodoptera frugiperda (J.E. Smith, 1797), Trichoplusia ni (Hübner, 1803), (Lepidoptera: Noctuidae), and Hypena scabra (Fabricius, 1798) (Lepidoptera: Erebidae) in Costa Rica and Peru, and Strymon acis (Drury, 1773) (Lepidoptera: Lycaenidae) in the state of Florida, EUA (Salvato et al., 2012SALVATO, M.H., SALVATO, H.L. and STIREMAN 3rd., J.O., 2012. Chetogena scutellaris (Diptera: Tachinidae), an endoparasite of larval Strymon acis bartrami (Lycaenidae). Journal of the Lepidopterists Society, vol. 66, no. 2, pp. 113-114. http://dx.doi.org/10.18473/lepi.v66i2.a5.
http://dx.doi.org/10.18473/lepi.v66i2.a5...
; Sourakov and Mitchell, 2002SOURAKOV, A. and MITCHELL, E.R., 2002. Laboratory biology of Chetogena scutellaris (Diptera: Tachinidae), a parasitoid of Noctuidae, reared on fall armyworm and cabbage looper. The Florida Entomologist, vol. 85, no. 2, pp. 341-343. http://dx.doi.org/10.1653/0015-4040(2002)085[0341:LBOCSD]2.0.CO;2.
http://dx.doi.org/10.1653/0015-4040(2002...
). Chetogena spp., parasitized C. includens (Lepidoptera: Noctuidae) in Mato Grosso, Brazil (Massarolli et al., 2018MASSAROLLI, A., HOFFMANN, A.L., FAVETTI, B.M. and BUTNARIU, A.R., 2018. Ichneumonids (Hymenoptera) and tachinid flies (Diptera) associated to lepidopterans in soybean crops. Journal of Agricultural Science, vol. 10, no. 7, pp. 167-173. http://dx.doi.org/10.5539/jas.v10n7p167.
http://dx.doi.org/10.5539/jas.v10n7p167...
).
Primary parasitoid Chetogena aff. scutellaris (Diptera: Tachinidae) (A) size: 1.0 cm; Hyperparasitoid Brachymeria koehleri (Hymenoptera: Chalcididae) (B) size: 0.6 mm; and parasitized pupa of Dione juno juno (Lepidoptera: Nymphalidae) (C) size: 2.7 cm.
Five Chalcididae wasps, emerged from pupae of the parasitoid C. aff. scutellaris, were identified as B. koehleri (Figure 1B). In Brazil, B. koehleri was reported as a hyperparasitoid of C. scutellaris through Opsiphanes invirae (Huebner, 1818) (Lepidoptera: Nymphalidae), in Pará (Tinôco et al., 2012TINÔCO, R.S., RIBEIRO, R.C., TAVARES, M.T., VILELA, E.F., LEMOS, W.D.P. and ZANUNCIO, J.C., 2012. Brachymeria spp. (Hymenoptera: Chalcididae) parasitizing pupae of Hersperidae and Nymphalidae (Lepidoptera) pests of oil palm in the Brazilian Amazonian region. Florida Entomologist, vol. 95, no. 3, pp 788-789. https://doi.org/10.1653/024.095.0335.
https://doi.org/10.1653/024.095.0335...
) and was also reported as a hyperparasitoid of Lespesia melloi (Gil-Santana, Nihei & Nunez, 2014) (Diptera: Tachinidae) through pupae of Thagona tibialis Walker, 1855 (Lepidoptera: Lymantriidae) (Tavares et al., 2013TAVARES, W.S., LEGASPI, J.C., TAVARES, M.T., NUNEZ, E., PINTO, R. and ZANUNCIO, J.C., 2013. Brachymeria koehleri (Hymenoptera: Chalcididae) as a hyperparasitoid of Lespesia melloi (Diptera: Tachinidae) pupae in Thagona tibialis (Lepidoptera: Lymantriidae) caterpillars in Brazil. The Florida Entomologist, vol. 96, no. 4, pp. 1635-1638. http://dx.doi.org/10.1653/024.096.0457.
http://dx.doi.org/10.1653/024.096.0457...
), in Lespesia sp. (Diptera: Tachinidae) through pupae of Parides ascanius (Cramer, 1775) (Lepidoptera: Papilionidae) in Rio de Janeiro, Brazil (Tavares et al., 2006TAVARES, M.T., NAVARRO-TAVARES, A.B. and ALMEIDA, G.D.S., 2006. The species of Chalcididae (Hymenoptera) parasitoids of Parides ascanius (Cramer), an endangered Papilionidae (Lepidoptera) from rest-ingas of southeastern Brazil. Zootaxa, vol. 1197, no. 1, pp. 55-63.).
This is the first record of B. koehleri as a hyperparasitoid in a Chetogena species in South America. It is also the first report of a Chetogena species parasitizing D. juno juno. Chetogena aff. scutellaris may have potential as a control agent of D. juno juno, but the hyperparasitism relationship with B. koehleri is potentially harmful to this natural enemy.
Acknowledgements
To Olaf Hermann Hendrik Mielke for identifying the lepidopteran reported in the study. To Jim O'Hara for clarifying doubts about the name Chetogena scutellaris. To the photographer Dayvson Ayala Costa for the photographs used in the manuscript. To the Brazilian institutions “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES- Finance Code 001)” and “Programa Cooperativo sobre Proteção Florestal (PROTEF) do Instituto de Pesquisas e Estudos Florestais (IPEF)” for financial support.
References
- ANDRADE, T.V. and TAVARES, M.T., 2009. Revisão de Ceyxia, stat. rev., (Hymenoptera, Chalcididae, Brachymeriini). Revista Brasileira de Entomologia, vol. 53, no. 4, pp. 511-548.
- ARNAUD, P.H., 1978. A host-parasite catalog of North American Tachinidae (Diptera). Department of Agriculture. Science and Education Administration, vol. 1, no. 1319, pp. 860.
- BLANCHARD, E.E., 1935. Apuntes sobre calcididos argentinos (Hym. Chalc.). Revista de la Sociedad Entomológica Argentina, vol. 7, pp. 103-122.
- BOIÇA JÚNIOR, A.L., ANGELINI, M.R. and OLIVEIRA, J.C.D., 2008. Aspectos biológicos de Dione juno juno (Cramer) (Lepidoptera: Nymphalidae) em genótipos de maracujazeiro. Revista Brasileira de Fruticultura, vol. 30, no. 1, pp. 101-105. http://dx.doi.org/10.1590/S0100-29452008000100019
» http://dx.doi.org/10.1590/S0100-29452008000100019 - JANZEN, D.H. and HALLWACHS, W., 2009 [viewed 22 February 2022]. Dynamic database for an inventory of the macrocaterpillar fauna, and its food plants and parasitoids, of Area de Conservacion Guanacaste (ACG), northwestern Costa Rica (nn-SRNP-nnnnn voucher codes) [online]. Available from: http://janzen.sas.upenn.edu
» http://janzen.sas.upenn.edu - MASSAROLLI, A., HOFFMANN, A.L., FAVETTI, B.M. and BUTNARIU, A.R., 2018. Ichneumonids (Hymenoptera) and tachinid flies (Diptera) associated to lepidopterans in soybean crops. Journal of Agricultural Science, vol. 10, no. 7, pp. 167-173. http://dx.doi.org/10.5539/jas.v10n7p167
» http://dx.doi.org/10.5539/jas.v10n7p167 - NARENDRAN, T.C. and VAN ACHTERBERG, C., 2016. Revision of the family Chalcididae (Hymenoptera, Chalcidoidea) from Vietnam, with the description of 13 new species. ZooKeys, vol. 576, pp. 1-202. PMid:27110185.
- O’HARA, J.E., HENDERSON, S.J. and WOOD, D.M., 2019. Preliminary checklist of the Tachinidae of the world, NADS, 681 pp. [online]. Available from: http://www.nadsdiptera.org/Tach/WorldTachs/Checklist/Worldchecklist.html
» http://www.nadsdiptera.org/Tach/WorldTachs/Checklist/Worldchecklist.html - O’HARA, J.E., WOOD, D.M. and GONZALEZ, C.R., 2021. Annotated Catalogue of Tachinidae (Insecta, Diptera) of the Chile. Zookeys, vol. 1064, no. 1988, pp. 1-200. https://doi.org/10.3897/zookeys.1064.62972
» https://doi.org/10.3897/zookeys.1064.62972 - PARCHAMI-ARAGHI, M., 2008. Identity of the previously unrecognized Chetogena flaviceps and its synonymy with C. scutellaris (Diptera: tachinidae). Journal of Entomological Society of Iran, vol. 28, no. 1, pp. 61-66.
- SALVATO, M.H., SALVATO, H.L. and HENNESSEY, M.K., 2009. Chetogena scutellaris (Diptera: Tachinidae) an endoparasite of larval Anaea troglodyta floridalis (Nymphalidae). Journal of the Lepidopterists Society, vol. 66, no. 2, pp. 113-114. http://dx.doi.org/10.18473/lepi.v66i2.a5
» http://dx.doi.org/10.18473/lepi.v66i2.a5 - SALVATO, M.H., SALVATO, H.L. and STIREMAN 3rd., J.O., 2012. Chetogena scutellaris (Diptera: Tachinidae), an endoparasite of larval Strymon acis bartrami (Lycaenidae). Journal of the Lepidopterists Society, vol. 66, no. 2, pp. 113-114. http://dx.doi.org/10.18473/lepi.v66i2.a5
» http://dx.doi.org/10.18473/lepi.v66i2.a5 - SCARAMOZZINO, P.L., DI GIOVANNI, F., LONI, A., GISONDI, S., LUCCHI, A. and CERRETTI, P., 2020. Tachinid (Diptera, Tachinidae) parasitoids of Lobesia botrana (Denis & Schiffermüller, 1775) (Lepidoptera, Tortricidae) and other moths. ZooKeys, vol. 934, pp. 111-140. http://dx.doi.org/10.3897/zookeys.934.50823 PMid:32508497.
» http://dx.doi.org/10.3897/zookeys.934.50823 - SOURAKOV, A. and MITCHELL, E.R., 2002. Laboratory biology of Chetogena scutellaris (Diptera: Tachinidae), a parasitoid of Noctuidae, reared on fall armyworm and cabbage looper. The Florida Entomologist, vol. 85, no. 2, pp. 341-343. http://dx.doi.org/10.1653/0015-4040(2002)085[0341:LBOCSD]2.0.CO;2
» http://dx.doi.org/10.1653/0015-4040(2002)085[0341:LBOCSD]2.0.CO;2 - THOMPSON, W.R., 1968. The Tachinids of Trinidad. VIII. Phorocerines. Memoirs of the Entomological Society of Canada, vol. 100, no. suppl S56, pp. 5-207. http://dx.doi.org/10.4039/entm10056fv
» http://dx.doi.org/10.4039/entm10056fv - TINÔCO, R.S., RIBEIRO, R.C., VILELA, E.F., LEMOS, W.D.P., ZANUNCIO, J.C. and NIHEI, S.S., 2010. Primeiro registro de Chetogena scutellaris Wulp (Diptera: Tachinidae) parasitando pupas de Opsiphanes invirae e Brassolis sophorae (Lepidoptera: Nymphalidae) no Pará, Brasil. In: EMBRAPA AMAZÔNIA ORIENTAL. Resumo do 23° Anais do Congresso (ALICE). Congresso Brasileiro de Entomologia, 2010, Natal. Natal: Sociedade Brasileira de Entomologia.
- ZHANG, X., WEI, X., ALI, M.M., RIZWAN, H.M., LI, B., LI, H., JIA, K., YANG, X., MA, S., LI, S. and CHEN, F., 2021. Changes in the content of organic acids and expression analysis of citric acid accumulation-related genes during fruit development of yellow (Passifora edulis f favicarpa) and Purple (Passifora edulis f edulis) Passion Fruits. International Journal of Molecular Sciences, vol. 22, no. 11, pp. 5765. http://dx.doi.org/10.3390/ijms22115765 PMid:34071242.
» http://dx.doi.org/10.3390/ijms22115765 - TAVARES, M.T., NAVARRO-TAVARES, A.B. and ALMEIDA, G.D.S., 2006. The species of Chalcididae (Hymenoptera) parasitoids of Parides ascanius (Cramer), an endangered Papilionidae (Lepidoptera) from rest-ingas of southeastern Brazil. Zootaxa, vol. 1197, no. 1, pp. 55-63.
- TAVARES, W.S., LEGASPI, J.C., TAVARES, M.T., NUNEZ, E., PINTO, R. and ZANUNCIO, J.C., 2013. Brachymeria koehleri (Hymenoptera: Chalcididae) as a hyperparasitoid of Lespesia melloi (Diptera: Tachinidae) pupae in Thagona tibialis (Lepidoptera: Lymantriidae) caterpillars in Brazil. The Florida Entomologist, vol. 96, no. 4, pp. 1635-1638. http://dx.doi.org/10.1653/024.096.0457
» http://dx.doi.org/10.1653/024.096.0457 - TINÔCO, R.S., RIBEIRO, R.C., TAVARES, M.T., VILELA, E.F., LEMOS, W.D.P. and ZANUNCIO, J.C., 2012. Brachymeria spp. (Hymenoptera: Chalcididae) parasitizing pupae of Hersperidae and Nymphalidae (Lepidoptera) pests of oil palm in the Brazilian Amazonian region. Florida Entomologist, vol. 95, no. 3, pp 788-789. https://doi.org/10.1653/024.095.0335
» https://doi.org/10.1653/024.095.0335
Publication Dates
-
Publication in this collection
12 Dec 2022 -
Date of issue
2022
History
-
Received
02 Feb 2022 -
Accepted
31 Oct 2022