BRACHYMERIA KOEHLERI (HYMENOPTERA: CHALCIDIDAE) AS A HYPERPARASITOID OF LESPESIA MELLOI (DIPTERA: TACHINIDAE) PUPAE IN THAGONA TIBIALIS (LEPIDOPTERA: LYMANTRIIDAE) CATERPILLARS IN BRAZIL

Headnote

Summary

Hyperparasitoids use the immature offspring of other parasitoids for their development, which may reduce the efficiency of biological control. The aim of this study was to evaluate the hyperparasitoidism by Brachymeria koehleri Blanchard ( Hymenoptera: Chalcididae) in Lespesia melloi Gil-Santana, Nunez & Nihei (Diptera: Tachinidae) pupae parasitizing Thagona tibialis Walker (Lepidoptera: Lymantriidae) caterpillars in Brazil. Fifty pupae of various ages of T. tibialis were collected after the caterpillars had defoliated a Terminada catappa L. (Combretaceae) plant on the campus of the Federal University of Viçosa (Viçosa, Minas Gerais, Brazil). Each pupae was held individually under controlled conditions until the emergence of either the lepidopteran or the parasitoid. Thirteen T. tibialis pupae yielded L. melloi puparia, which resulted in the emergence of 8 L. melloi individuals, 1 B. koehleri female, and 4 unviable pupae. This is the first report of hyperparasitism by B. koehleri of L. melloi pupae parasitizing T. tibialis caterpillars in Brazil.

Resumo

Hiperparasitóides usam a prole de outros parasitóides para seu desenvolvimento, o que pode reduzir a eficiencia do controle biológico. O objetivo deste estudo foi avahar o hiperparasitoidismo por Brachymeria koehleri Blanchard (Hymenoptera: Chalcididae) em pupas de Lespesia melloi Gil-Santana, Nunez & Nihei (Diptera: Tachinidae) parasitando lagartas de Thagona tibialis Walker (Lepidoptera: Lymantriidae) no Brasil. Cinqüenta pupas de várias idades de T. tibialis foram coletadas após suas lagartas terem desfolhado urna planta de Terminalia catappa L. (Combretaceae) no campus da Universidade Federal de Viçosa (Viçosa, Minas Gerais, Brasil). Estas pupas foram individualizadas e mantidas em condiçôes controladas até a emergencia de lepidópteros ou parasitoides. Treze pupas de T. tibialis apresentaram pupários, resultando na emergencia de oito individuos de L. melloi, uma fêmea de B. koehleri e quatro pupas foram inviáveis. Este é o primeiro relato de hiperparasitoidismo por B. koehleri em pupas de L. melloi parasitando lagartas de T. tibialis no Brasil.

Terminalia catappa L. (Myrtales: Combretaceae), a cosmopolitan ornamental and medicinal plant, probably originated from India or New Guinea, is cultivated for shading in anthropogenic areas (Hayward 1990; Santos & Teixeira 2010). Compounds from the leaves and fruits of this plant are used to treat diseases in humans and against fish parasites (Chansue 2007; Yang et al. 2010). Thagona tibialis Walker (Lepidoptera: Lymantriidae) caterpillars defoliate T. catappa plants in Brazil with population peaks after the rainy season (Diniz et al. 2001, 2011). Damage by this insect on T. catappa crown was reported on TV and in newspapers during an infestation in Belo Horizonte, Minas Gerais, Brazil in 2005. This defoliator is distributed in the Cerrado (Savannah-type) and Atlantic Rainforest biomes in Brazil. The females differ from males in the number of black spots on their hind-wing and their wing color, depending on their geographical region of occurrence (Tavares et al. 2012).

The association of parasitoids with T. tibialis suggests that T. catappa can be grown along field borders or interspersed with crops as a refuge for parasitoids (Tavares et al. 2011c; Costa et al. 2012). Thagona tibialis pupae of various ages were collected from T. catappa, and the parasitoids, Palmistichus elaeisis Delvare & LaSalle and Trichospilus pupivorus Ferrière (Hymenoptera: Eulophidae), emerged from the T. tibialis pupae (Tavares et al. 2011b, 2013a, 2013b). Trichospilus pupivorus was evaluated in the laboratory showing high parasitism rates on Anticarsia gemmatalis Hübner (Lepidoptera: Noctuidae) (Tavares et al. 2011a, 2013c). However, hyperparasitism may reduce the efficiency of such biological control agents.

Hyperparasitism is a rare event in nature, as evidenced by the low number of chalcidid hyperparasitoids of Licomadidae collected between 2004 and 2009 in North America (Gates et al. 2012). Unlike most parasitoids, hyperparasitoids do not make cocoons, but pupate within the already prepared cocoon of the host parasitoid (Harvey et al. 2006). Lespesia melloi Gil-Santana, Nunez & Nihei (Díptera: Tachinidae) is a parasitoid ofXanthopastis timáis Cramer (Lepidoptera: Noctuidae) in Brazil (Gil-Santana et al. 2013). The aim of this study was to evaluate the hyperparasitism by Brachymeria koehleri Blanchard (Hymenoptera: Chalcididae) on L. melloi pupae parasitizing T. tibialis caterpillars in Brazil.

Fifty pupae of various ages of T. tibialis were collected during 5 days ( 10 pupae/day, starting on May 4, 2011) from one T. catappa plant grown at the campus of the Federal University of Viçosa (UFV) in Viçosa, Minas Gerais, Brazil (S 20°45' W 42°51', 651 m) and placed in 500 mL plastic pots lined with cotton. This material was brought to the Laboratory of Biological Control of Insects (UFV), and each pupa was held individually in a test tube ( 12 cm H x 2 cm diam) capped with cotton and kept at 25 ± 1 °C, 70 ± 10% RH, and 12:12 h L:D until the emergence of either the lepidopteran or the parasitoid. The number and percentage of puparia, adult emergence and sex ratio of L. melloi, B. koehleri and T. tibialis, and the number of unviable T. tibialis pupae were recorded. The puparia of L. melloi were examined after dissecting the remains of the caterpillars with a scalpel.

Thagona tibialis females were identified by Dr. Vitor Osmar Becker and deposited at the Uiraçu Institute in Camacan, Bahia, Brazil. Lespesia melloi males were identified by the fourth author and deposited at the Regional Museum of Entomology of the UFV in Viçosa, Minas Gerais, Brazil. Brachymeria koehleri was identified by the third author and deposited in the Department of Biological Sciences of the Federal University of Espirito Santo in Vitoria, Espirito Santo, Brazil.

A total of 13 T. tibialis pupae yielded puparia of L. melloi', 8 resulted in the emergence of adults of this tachinid (sex ratio = 0.625); 1 B. koehleri female emerged from a single pupa, and 4 pupae were unviable. Lastly, 33 T. tibialis adults emerged from the pupae of this insect ( sex ratio = 0.758).

Hyperparasitism by B. koehleri has been reported in association with species of Sarcophagidae and Tachinidae parasitizing Geometridae, Hesperiidae, Nymphalidae, Noctuidae, and Papilionidae caterpillars (Thompson 1954; De Santis 1967, 1989; Herting 1976, 1978; Tavares et al. 2006; Salgado-Neto et al. 2010; Tinoco et al. 2012; Zaché et al. 2012). Brachymeria spp. can occur in various environments: as Brachymeria vesparum Boucek (Hymenoptera: Chalcididae) parasitizing Polistes lanío lanío F. (Hymenoptera: Vespidae) larvae in Rio de Janeiro, Brazil (Silva-Filho et al. 2007) and Brachymeria sp. parasitizing larvae of stored grain pests in Namibia (Stejskal et al. 2006).

In recent reports in Brazil, B. koehleri was recorded as a hyperparasitoid of Lespesia sp. pupae parasitizing Paridesa scanius Cramer (Lepidoptera: Papilionidae) caterpillars, a defoliator of Aristolochia trilobata L. (Aristolochiales: Aristolochiaceae) in the Rio de Janeiro, Brazil (Tavares et al. 2006), and also as a hyperparasitoid of Chetogena scutellaris Wulp (Diptera: Tachinidae) parasitizing Opsiphanes invirae Hübner (Lepidoptera: Nymphalidae) caterpillars, which defoliate Elaeis guineensis Jacq (Arecales: Arecaceae) in the Pará, Brazil (Tinoco et al. 2012). Other Brachymeria spp. that parasitize Lepidoptera in Brazil include Brachymeria mnestor Walker and Brachymeria nigritibialis Tavares & NavarroTavares (Hymenoptera: Chalcididae) hyperparasitizing Lespesia sp. pupae in Parides ascanius Cramer (Lepidoptera: Papilionidae) (Tavares et al. 2006);Brachymeria pandora Crawford (Hymenoptera: Chalcididae) parasitizing Historis odius F. (Lepidoptera: Nymphalidae) in Rio de Janeiro (Gil-Santana & Tavares 2005), Argon lota Hewitson (Lepidoptera: Hesperiidae) in Rio Grande do Sul (Salgado-Neto et al. 2010), Saliana sp. (Lepidoptera: Hesperidae) in Pará (Tinoco et al. 2012) and Thyrinteina leiicoceraea Rindge (Lepidoptera: Geometridae) in Minas Gerais (Zaché et al. 2012); and Brachymeria annulipes Costa Lima (Hymenoptera: Chalcididae) parasitizing Opsiphanes invirae Hübner (Lepidoptera: Nymphalidae) pupae (Tinoco et al. 2012).

This is the first report of hyperparasitism by B. koeheri of L. melloi pupae parasitizing T. tibialis caterpillars defoliating a T. ca tappa plant in Brazil.

Acknowledgments

To "Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)", "Coordenaçào de Aperfeiçoamento de Pessoal de Nivel Superior (CAPES)", "Fundaçào de Amparo á Pesquisa do Espirito Santo (FAPES)", and "Fundaçào de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG)" for financial support. Global Edico Services of India edited and rewrote this manuscript.

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