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Brachymeria minuta (Hymenoptera: Chalcididae): parasitism on pupa of the eucalypt defoliator Thyrinteina arnobia (Lepidoptera: Geometridae) and its first record in the Americas

Thyrinteina arnobia Stoll, 1782 (Lepidoptera: Geometridae) is found in Central, North, and South America (Pohl et al., 2016POHL, G.R., PATTERSON, B. and PELHAM, J.P., 2016 [viewed 9 April 2022]. Annotated taxonomic checklist of the Lepidoptera of North America, North of Mexico [online]. Available from: https://www.researchgate.net/profile/Greg-Pohl-2/publication/302570819_Annotated_taxonomic_checklist_of_the_Lepidoptera_of_North_America_North_of_Mexico/links/5731597b08ae100ae557533a/Annotated-taxonomic-checklist-of-the-Lepidoptera-of-North-America-North-of-Mexico.pdf
https://www.researchgate.net/profile/Gre...
) and it is the main defoliator in Eucalyptus spp. (Myrtaceae) plantations in all regions of Brazil (Zanuncio et al., 2021ZANUNCIO, J.C., PLATA-RUEDA, A., LEMES, P.G. and BRÜGGER, B.P. 2021. Thyrinteina arnobia. In: P.G. LEMES and J.C. ZANUNCIO, eds. Novo manual de pragas florestais brasileiras. Montes Claros: Instituto de Ciências Agrárias da Universidade Federal de Minas Gerais, pp. 487-499.). Identifying new natural enemies is important because predatory stink bugs (Hemiptera: Pentatomidae) and the parasitoid wasps Palmistichus elaeisis Delvare & LaSalle, 1993 and Trichospilus diatraeae Cherian & Margabandhu, 1942 (Hymenoptera: Eulophidae) are used in the management of T. arnobia in Brazil (Pastori et al., 2012PASTORI, P.L., FAGUNDES-PEREIRA, F., SANTOS-ANDRADE, G., OLIVEIRA-SILVA, R., COLA-ZANUNCIO, J. and AZEVEDO-PEREIRA, A.I., 2012. Reproduction of Trichospilus diatraeae (Hymenoptera: Eulophidae) in pupae of two lepidopterans defoliators of eucalypt. Revista Colombiana de Entomologia, vol. 38, no. 1, pp. 91-93. http://dx.doi.org/10.25100/socolen.v38i1.8927.
http://dx.doi.org/10.25100/socolen.v38i1...
; Silva et al., 2012SILVA, R.B., CORRÊA, A.S., DELLA LUCIA, T.M.C., PEREIRA, A.I.A., CRUZ, I. and ZANUNCIO, J.C., 2012. Does the aggressiveness of the prey modify the attack behavior of the predator Supputius cincticeps (Stål) (Hemiptera, Pentatomidae). Revista Brasileira de Entomologia, vol. 56, no. 2, pp. 244-248. http://dx.doi.org/10.1590/S0085-56262012005000031.
http://dx.doi.org/10.1590/S0085-56262012...
; Barbosa et al., 2016BARBOSA, R.H., ZANUNCIO, J.C., PEREIRA, F.F., KASSAB, S.O. and ROSSONI, C., 2016. Foraging activity of Palmistichus elaeisis (Hymenoptera: Eulophidae) at various densities on pupae of the eucalyptus defoliator Thyrinteina arnobia (Lepidoptera: Geometridae). The Florida Entomologist, vol. 99, no. 4, pp. 686-690. http://dx.doi.org/10.1653/024.099.0417.
http://dx.doi.org/10.1653/024.099.0417...
).

Species of Chalcididae wasps are cosmopolitan with the majority reported from tropical regions (Hasanshahi et al., 2013HASANSHAHI, G., ABBASIPOUR, H., JAHAN, F. and ASKEW, R., 2013. New record of Brachymeria albicrus (Klug) (Hymenoptera: Chalcididae), a pupal parasitoid of the cabbage white butterfly, Pieris rapae (Linnaeus) from Iran. Journal of Biological Control, vol. 27, no. 2, pp. 124-125. http://dx.doi.org/10.18311/jbc/2013/3415.
http://dx.doi.org/10.18311/jbc/2013/3415...
) and Brachymeria Westwood, 1829 is one of the most widespread and common genera of this family. Species of this genus parasitize pupae of Coleoptera, Diptera, Hymenoptera and Lepidoptera pests (Zache et al., 2012ZACHE, B., ZACHÉ, R.R.C., TAVARES, M.T. and WILCKEN, C.F., 2012. Brachymeria pandora (Crawford) (Hymenoptera: Chalcididae) as a new parasitoid of Thyrinteina leucocerae (Rindge) (Lepidoptera: Geometridae) in Brazil. Neotropical Entomology, vol. 41, no. 4, pp. 343-344. http://dx.doi.org/10.1007/s13744-012-0049-5. PMid:23950072.
http://dx.doi.org/10.1007/s13744-012-004...
; Aquino et al., 2015AQUINO, D.A., TAVARES, M.T., BALDUCCI, E., BACA, V. and QUINTEROS, S.Q., 2015. The microlepidopterous natural enemy Brachymeria subrugosa Blanchard, 1942 (Hymenoptera, Chalcididae): identity, hosts and geographic distribution. Zootaxa, vol. 4013, no. 2, pp. 293-300. http://dx.doi.org/10.11646/zootaxa.4013.2.10. PMid:26623900.
http://dx.doi.org/10.11646/zootaxa.4013....
) or are pupal hyperparasitoids (Pinheiro et al., 2022PINHEIRO, R.A., ZANUNCIO, J.C., TOMA, R., ISAAC JUNIOR, 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, pp. e260645. http://dx.doi.org/10.1590/1519-6984.260645. PMid:36515296.
http://dx.doi.org/10.1590/1519-6984.2606...
). Brachymeria parasitized Thyrinteina sp. and Brachymeria pandora (Crawford) parasitized Thyrinteina leucocerae Rindge (Lepidoptera: Geometridae) pupae in the municipality of Sete Lagoas, Minas Gerais state, Brazil (Zache et al., 2012ZACHE, B., ZACHÉ, R.R.C., TAVARES, M.T. and WILCKEN, C.F., 2012. Brachymeria pandora (Crawford) (Hymenoptera: Chalcididae) as a new parasitoid of Thyrinteina leucocerae (Rindge) (Lepidoptera: Geometridae) in Brazil. Neotropical Entomology, vol. 41, no. 4, pp. 343-344. http://dx.doi.org/10.1007/s13744-012-0049-5. PMid:23950072.
http://dx.doi.org/10.1007/s13744-012-004...
).

The objective of this paper is to report, for the first time, Brachymeria minuta Linnaeus, 1767 (Hymenoptera: Chalcididae) parasitizing T. arnobia pupae and its first occurrence in the Americas.

Pupae of T. arnobia were collected from a eucalyptus plant near a native forest in Viçosa, Minas Gerais state, Brazil (20º45'14” S, 42º52'53 W, 648.74 m) and they were kept under laboratory conditions. A chalcidid pupal parasitoid emerged from one of them and it was preserved in a glass vial containing 70% alcohol and its dorsal and lateral photographs sent to Dr. Sagadai Manickavasagam (Faculty of Agriculture - Annamalai University, India, Chidambaram, India), who identified it as Brachymeria minuta.

This is the first report of an association between B. minuta and T. arnobia (Figure 1) in the world. Brachymeria minuta is, usually, a gregarious parasitoid in Lepidoptera, and solitary in Diptera, due to the host size and weight. This natural enemy parasitized pupa of important insect pests such as Apomyelois ceratoniae Zeller, 1839 (Lepidoptera: Pyralidae), Aproaerema modicella Deventer, 1904 (Lepidoptera: Gelechiidae), and Lymantria dispar Linnaeus, 1758 (Lepidoptera: Lymantriidae) (Kenis and Cugala, 2006KENIS, M. and CUGALA, D., 2006. Prospects for the biological control of the groundnut leaf miner, Aproaerema modicella, in Africa. Biocontrol News and Information, vol. 27, no. 031, pp. 1-9.; Lotfalizadeh et al., 2012LOTFALIZADEH, H, EBRAHIMI E. and DELVARE, G., 2012. A contribution to the knowledge of family Chalcididae (Hymenoptera: Chalcidoidea) in Iran. Journal of Entomological Society of Iran, vol. 31, no. 2, pp. 67-100.; Nobakht et al., 2015NOBAKHT, Z., KARIMZADEH, J., SHAKARAM, J. and JAFARI, S., 2015. Identification of parasitoids of Apomyelois ceratoniae (Zeller) (Lepidoptera, Pyralidae) on pomegranate in Isfahan province. Journal of Entomology and Zoology Studies, vol. 3, no. 1, pp. 287-289.). Brachymeria minuta also parasitizes synantropic dipterans, such as Musca domestica Linnaeus, 1758 (Diptera: Muscidae) (Chakraborty et al., 2015CHAKRABORTY, A., BANERJEE, D., GHOSH, S. and ANSAR, W., 2015. Thermophilic pupal endoparasitoids: Brachymeria minuta (Hymenoptera: Chalicididae) on forensic indicator Sarcophaga (Parasarcophaga) albiceps. Prommalia, vol. 3, pp. 85-94.).

Figure 1
Lateral (A) and dorsal (B) view of the parasitoid Brachymeria minuta (Hymenoptera: Chalcididae) emerged from Thyrinteina arnobia (Lepidoptera: Geometridae) pupa.

The record of B. minuta in the Americas expands the geographic range of this parasitoid widely distributed in Europe, with reports in Malta (Southern Europe), Portugal and Spain (Southwest Europe), Italy (Central-Southern Europe), Austria (Central Europe), Belgium, France, Germany, Netherlands and the United Kingdom (Western Europe), Turkey (Southeast Europe), Belarus, Hungary and Ukraine (Eastern Europe) and Denmark, Estonia, Lithuania, and Sweden (Northern Europe). This parasitoid has also been reported in India (South Asia), Japan (East Asia), Korea (Northeast Asia), Thailand and Vietnam (Southeast Asia), Russian Federation (Eurasia) and Saudi Arabia (Middle East), Morocco (Northwest Africa), Iran (Palearctic Region), and Australasia (Oceania) (Kenis and Cugala, 2006KENIS, M. and CUGALA, D., 2006. Prospects for the biological control of the groundnut leaf miner, Aproaerema modicella, in Africa. Biocontrol News and Information, vol. 27, no. 031, pp. 1-9.; Lotfalizadeh et al., 2012LOTFALIZADEH, H, EBRAHIMI E. and DELVARE, G., 2012. A contribution to the knowledge of family Chalcididae (Hymenoptera: Chalcidoidea) in Iran. Journal of Entomological Society of Iran, vol. 31, no. 2, pp. 67-100.; Nobakht et al., 2015NOBAKHT, Z., KARIMZADEH, J., SHAKARAM, J. and JAFARI, S., 2015. Identification of parasitoids of Apomyelois ceratoniae (Zeller) (Lepidoptera, Pyralidae) on pomegranate in Isfahan province. Journal of Entomology and Zoology Studies, vol. 3, no. 1, pp. 287-289.; 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. 1, no. 576, pp. 1-202. http://dx.doi.org/10.3897/zookeys.576.8177. PMid:27110185.
http://dx.doi.org/10.3897/zookeys.576.81...
; Falahatpisheh et al., 2018FALAHATPISHEH, A., FALLAHZADEH, M., DOUSTI, A.F. and DELVARE, G., 2018. Review of Iranian Chalcididae (Hymenoptera, Chalcidoidea) with nomenclatural notes. Zootaxa, vol. 4394, no. 2, pp. 251-269. http://dx.doi.org/10.11646/zootaxa.4394.2.8. PMid:29690375.
http://dx.doi.org/10.11646/zootaxa.4394....
; GBIF, 2022GLOBAL BIODIVERSITY INFORMATION FACILITY - GBIF, 2022 [viewed 9 April 2022]. Brachymeria minuta (Linnaeus, 1767) [online]. Available from: https://doi.org/10.15468/39omei.
https://doi.org/10.15468/39omei...
) (Figure 2).

Figure 2
First record of Brachymeria minuta (Hymenoptera: Chalcididae) in the Americas and its distribution in the world. Source: Kenis and Cugala (2006)KENIS, M. and CUGALA, D., 2006. Prospects for the biological control of the groundnut leaf miner, Aproaerema modicella, in Africa. Biocontrol News and Information, vol. 27, no. 031, pp. 1-9.; Lotfalizadeh et al. (2012)LOTFALIZADEH, H, EBRAHIMI E. and DELVARE, G., 2012. A contribution to the knowledge of family Chalcididae (Hymenoptera: Chalcidoidea) in Iran. Journal of Entomological Society of Iran, vol. 31, no. 2, pp. 67-100.; Nobakht et al. (2015)NOBAKHT, Z., KARIMZADEH, J., SHAKARAM, J. and JAFARI, S., 2015. Identification of parasitoids of Apomyelois ceratoniae (Zeller) (Lepidoptera, Pyralidae) on pomegranate in Isfahan province. Journal of Entomology and Zoology Studies, vol. 3, no. 1, pp. 287-289.; Narendran and van Achterberg (2016)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. 1, no. 576, pp. 1-202. http://dx.doi.org/10.3897/zookeys.576.8177. PMid:27110185.
http://dx.doi.org/10.3897/zookeys.576.81...
; Falahatpisheh et al. (2018)FALAHATPISHEH, A., FALLAHZADEH, M., DOUSTI, A.F. and DELVARE, G., 2018. Review of Iranian Chalcididae (Hymenoptera, Chalcidoidea) with nomenclatural notes. Zootaxa, vol. 4394, no. 2, pp. 251-269. http://dx.doi.org/10.11646/zootaxa.4394.2.8. PMid:29690375.
http://dx.doi.org/10.11646/zootaxa.4394....
; GBIF (2022)GLOBAL BIODIVERSITY INFORMATION FACILITY - GBIF, 2022 [viewed 9 April 2022]. Brachymeria minuta (Linnaeus, 1767) [online]. Available from: https://doi.org/10.15468/39omei.
https://doi.org/10.15468/39omei...
.

The association of B. minuta as an endoparasitoid of T. arnobia pupae increases the number of natural enemies of this important eucalyptus defoliator. This is the first record of B. minuta in the Americas, specifically in South America and Brazil.

Acknowledgements

To Philipe Guilherme Corcino Souza, from the Postgraduate Program in Plant Production at UFVJM, for drawing up the map. To “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES- Finance Code 001), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and “Programa Cooperativo sobre Proteção Florestal (PROTEF) do Instituto de Pesquisas e Estudos Florestais (IPEF)”.

References

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    » http://dx.doi.org/10.11646/zootaxa.4013.2.10
  • BARBOSA, R.H., ZANUNCIO, J.C., PEREIRA, F.F., KASSAB, S.O. and ROSSONI, C., 2016. Foraging activity of Palmistichus elaeisis (Hymenoptera: Eulophidae) at various densities on pupae of the eucalyptus defoliator Thyrinteina arnobia (Lepidoptera: Geometridae). The Florida Entomologist, vol. 99, no. 4, pp. 686-690. http://dx.doi.org/10.1653/024.099.0417
    » http://dx.doi.org/10.1653/024.099.0417
  • CHAKRABORTY, A., BANERJEE, D., GHOSH, S. and ANSAR, W., 2015. Thermophilic pupal endoparasitoids: Brachymeria minuta (Hymenoptera: Chalicididae) on forensic indicator Sarcophaga (Parasarcophaga) albiceps. Prommalia, vol. 3, pp. 85-94.
  • FALAHATPISHEH, A., FALLAHZADEH, M., DOUSTI, A.F. and DELVARE, G., 2018. Review of Iranian Chalcididae (Hymenoptera, Chalcidoidea) with nomenclatural notes. Zootaxa, vol. 4394, no. 2, pp. 251-269. http://dx.doi.org/10.11646/zootaxa.4394.2.8 PMid:29690375.
    » http://dx.doi.org/10.11646/zootaxa.4394.2.8
  • GLOBAL BIODIVERSITY INFORMATION FACILITY - GBIF, 2022 [viewed 9 April 2022]. Brachymeria minuta (Linnaeus, 1767) [online]. Available from: https://doi.org/10.15468/39omei
    » https://doi.org/10.15468/39omei
  • HASANSHAHI, G., ABBASIPOUR, H., JAHAN, F. and ASKEW, R., 2013. New record of Brachymeria albicrus (Klug) (Hymenoptera: Chalcididae), a pupal parasitoid of the cabbage white butterfly, Pieris rapae (Linnaeus) from Iran. Journal of Biological Control, vol. 27, no. 2, pp. 124-125. http://dx.doi.org/10.18311/jbc/2013/3415
    » http://dx.doi.org/10.18311/jbc/2013/3415
  • KENIS, M. and CUGALA, D., 2006. Prospects for the biological control of the groundnut leaf miner, Aproaerema modicella, in Africa. Biocontrol News and Information, vol. 27, no. 031, pp. 1-9.
  • LOTFALIZADEH, H, EBRAHIMI E. and DELVARE, G., 2012. A contribution to the knowledge of family Chalcididae (Hymenoptera: Chalcidoidea) in Iran. Journal of Entomological Society of Iran, vol. 31, no. 2, pp. 67-100.
  • 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. 1, no. 576, pp. 1-202. http://dx.doi.org/10.3897/zookeys.576.8177 PMid:27110185.
    » http://dx.doi.org/10.3897/zookeys.576.8177
  • NOBAKHT, Z., KARIMZADEH, J., SHAKARAM, J. and JAFARI, S., 2015. Identification of parasitoids of Apomyelois ceratoniae (Zeller) (Lepidoptera, Pyralidae) on pomegranate in Isfahan province. Journal of Entomology and Zoology Studies, vol. 3, no. 1, pp. 287-289.
  • PASTORI, P.L., FAGUNDES-PEREIRA, F., SANTOS-ANDRADE, G., OLIVEIRA-SILVA, R., COLA-ZANUNCIO, J. and AZEVEDO-PEREIRA, A.I., 2012. Reproduction of Trichospilus diatraeae (Hymenoptera: Eulophidae) in pupae of two lepidopterans defoliators of eucalypt. Revista Colombiana de Entomologia, vol. 38, no. 1, pp. 91-93. http://dx.doi.org/10.25100/socolen.v38i1.8927
    » http://dx.doi.org/10.25100/socolen.v38i1.8927
  • PINHEIRO, R.A., ZANUNCIO, J.C., TOMA, R., ISAAC JUNIOR, 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, pp. e260645. http://dx.doi.org/10.1590/1519-6984.260645 PMid:36515296.
    » http://dx.doi.org/10.1590/1519-6984.260645
  • POHL, G.R., PATTERSON, B. and PELHAM, J.P., 2016 [viewed 9 April 2022]. Annotated taxonomic checklist of the Lepidoptera of North America, North of Mexico [online]. Available from: https://www.researchgate.net/profile/Greg-Pohl-2/publication/302570819_Annotated_taxonomic_checklist_of_the_Lepidoptera_of_North_America_North_of_Mexico/links/5731597b08ae100ae557533a/Annotated-taxonomic-checklist-of-the-Lepidoptera-of-North-America-North-of-Mexico.pdf
    » https://www.researchgate.net/profile/Greg-Pohl-2/publication/302570819_Annotated_taxonomic_checklist_of_the_Lepidoptera_of_North_America_North_of_Mexico/links/5731597b08ae100ae557533a/Annotated-taxonomic-checklist-of-the-Lepidoptera-of-North-America-North-of-Mexico.pdf
  • SILVA, R.B., CORRÊA, A.S., DELLA LUCIA, T.M.C., PEREIRA, A.I.A., CRUZ, I. and ZANUNCIO, J.C., 2012. Does the aggressiveness of the prey modify the attack behavior of the predator Supputius cincticeps (Stål) (Hemiptera, Pentatomidae). Revista Brasileira de Entomologia, vol. 56, no. 2, pp. 244-248. http://dx.doi.org/10.1590/S0085-56262012005000031
    » http://dx.doi.org/10.1590/S0085-56262012005000031
  • ZACHE, B., ZACHÉ, R.R.C., TAVARES, M.T. and WILCKEN, C.F., 2012. Brachymeria pandora (Crawford) (Hymenoptera: Chalcididae) as a new parasitoid of Thyrinteina leucocerae (Rindge) (Lepidoptera: Geometridae) in Brazil. Neotropical Entomology, vol. 41, no. 4, pp. 343-344. http://dx.doi.org/10.1007/s13744-012-0049-5 PMid:23950072.
    » http://dx.doi.org/10.1007/s13744-012-0049-5
  • ZANUNCIO, J.C., PLATA-RUEDA, A., LEMES, P.G. and BRÜGGER, B.P. 2021. Thyrinteina arnobia In: P.G. LEMES and J.C. ZANUNCIO, eds. Novo manual de pragas florestais brasileiras Montes Claros: Instituto de Ciências Agrárias da Universidade Federal de Minas Gerais, pp. 487-499.

Publication Dates

  • Publication in this collection
    15 May 2023
  • Date of issue
    2023

History

  • Received
    09 Apr 2022
  • Accepted
    01 Mar 2023
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