Brachymeria koehleri (Hymenoptera: Chalcididae): first record as hyperparasitoid in Dione juno juno (Lepidoptera: Nymphalidae) pupae

Passion fruits are nutritious for fresh and industrial consumption (Zhang et al., 2021). 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., 2008).

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., 2020).

Seventy-three species have been described for the genus Chetogena (Rondani, 1856) (Diptera: Tachinidae) (O’Hara et al., 2019, 2021), including Chetogena scutellaris (Wulp, 1890) (Diptera: Tachinidae) (O’Hara et al., 2019), an endoparasitoid of Arctiidae, Geometridae, Noctuidae, Pieridae, Saturniidae, Sphingidae and Zygaenidae (Lepidoptera) caterpillars (Arnaud, 1978).

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, 2016).

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) and Thompson’s (1968) 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), the description of Blanchard (1935), 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, 2009). 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., 2010; Salvato et al., 2009). 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., 2012; Sourakov and Mitchell, 2002). Chetogena spp., parasitized C. includens (Lepidoptera: Noctuidae) in Mato Grosso, Brazil (Massarolli et al., 2018).

Figure 1
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., 2012) 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., 2013), in Lespesia sp. (Diptera: Tachinidae) through pupae of Parides ascanius (Cramer, 1775) (Lepidoptera: Papilionidae) in Rio de Janeiro, Brazil (Tavares et al., 2006).

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.

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Publication Dates

• Publication in this collection
  12 Dec 2022
• Date of issue
  2022

History

• Received
  02 Feb 2022
• Accepted
  31 Oct 2022