Translator Disclaimer
1 December 2013 Brachymeria koehleri (Hymenoptera: Chalcididae) as a Hyperparasitoid of Lespesia melloi (Diptera: Tachinidae) Pupae in Thagona tibialis (Lepidoptera: Lymantriidae) Caterpillars in Brazil
Author Affiliations +

Terminalia catappa L. (Myrtales: Combreta-ceae), 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 gemma-talis 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 hy-perparasitoids of Licomadidae collected between 2004 and 2009 in North America (Gates et al. 2012). Unlike most parasitoids, hyperparasit-oids 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 (Diptera: Tachinidae) is a parasitoid of Xanthopastis timais 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 Espiríto Santo in Vitória, Espírito 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 Sarcophagi-dae and Tachinidae parasitizing Geometridae, Hesperiidae, Nymphalidae, Noctuidae, and Pa-pilionidae caterpillars (Thompson 1954; De San-tis 1967, 1989; Herting 1976, 1978; Tavares et al. 2006; Salgado-Neto et al. 2010; Tinôco et al. 2012; Zaché et al. 2012). Brachymeria spp. can occur in various environments: as Brachymeria vesparum Bouĉek (Hymenoptera: Chalcididae) parasitizing Polistes lanio lanio 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 (Lepidop-tera: Papilionidae) caterpillars, a defoliator of Aristolochia trilobata L. (Aristolochiales: Aris-tolochiaceae) 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 (Lepi-doptera: Nymphalidae) caterpillars, which defoliate Elaeis guineensis Jacq (Arecales: Arecaceae) in the Para, Brazil (Tinôco et al. 2012). Other Brachymeria spp. that parasitize Lepidoptera in Brazil include Brachymeria mnestor Walker and Brachymeria nigritibialis Tavares & Navarro-Tavares (Hymenoptera: Chalcididae) hyperpara-sitizing 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 Para (Tinôco et al. 2012) and Thyrinteina leucoceraea Rindge (Lepidoptera: Geometridae) in Minas Gerais (Zaché et al. 2012); and Brachymeria annulipes Costa Lima (Hymenoptera: Chalcididae) parasitizing Opsiphanes invirae Hübner (Lepidoptera: Nymphalidae) pupae (Tinôco et al. 2012).

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

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 Terminalia catappa L. (Combretaceae) plant on the campus of the Federal University of Viçosa (Viçosa, Minas Gérais, 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 para-sitóides para seu desenvolvimento, o que pode re-duzir a eficiência do controle biológico. O objetivo deste estudo foi avaliar 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. Cinqüen-ta pupas de várias idades de T. tibialis foram co-letadas após suas lagartas terem desfolhado uma planta de Terminalia catappa L. (Combretaceae) no campus da Universidade Federal de Viçosa (Viçosa, Minas Gerais, Brasil). Estas pupas foram individualizadas e mantidas em condiçães controladas até a emergência de lepidópteros ou parasitoides. Treze pupas de T. tibialis apresenta-ram pupários, resultando na emergência de oito indivíduos 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.

Acknowledgments

To “Conselho National de Desenvolvimento Cientí-fico e Tecnológico (CNPq)”, “Coordenação de Aperfeiçoa-mento de Pessoal de Nível Superior (CAPES)”, “Funda-çâo de Amparo a Pesquisa do Espirito Santo (FAPES)”, and “Fundaçâo de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG)” for financial support. Global Edico Services of India edited and rewrote this manuscript.

References Cited

1.

N. Chansue 2007. Effects of dried Indian almond leaf (Terminalia catappa L.) extract on monogenean parasites in goldfish (Carassius auratus). Wien Tierarz-tl. Monat 94(11/12): 269–273. Google Scholar

2.

M. A. Costa , W. S. Tavares , A. I. A. Pereira , L. Cruz, J. E. Serrão , and J. C. Zanuncio 2012. Chrysoperla externa (Neuroptera: Chrysopidae) and Utetheisa ornatrix (Lepidoptera: Arctiidae) on organically grown Crotalaria juncea (Fabaceae). Planta Daninha 30(3): 459–468. Google Scholar

3.

L. De Santis 1967. Catálogo de los himenópteros ar-gentinos de la serie parasítica, incluyendo Bethy-loidea. 337pp. La Plata: Provincia de Buenos Aires, Comisión de Investigation Científica. Google Scholar

4.

L. De Santis 1989. Catalogo de los Himenópteros Cal-cidoides (Hymenoptera) al sur de los Estados Uni-dos, Segundo Suplemento. Acta Entomol. Chilena 15(1): 1–12. Google Scholar

5.

I. R. Diniz , H. C. Morais , and A. J. A. Camargo 2001. Host plants of lepidopteran caterpillars in the cer-rado of the Distrito Federal, Brazil. Rev. Brasileira Entomol. 45(1): 107–122. Google Scholar

6.

I. R. Diniz , C. Lepesqueur , M. S. Milhomen , F. C. S. Ban-Deira , and H. C. Morais 2011. Eloria sub-apicalis (Lepidoptera: Noctuidae: Lymantriidae): rare and specialist species on Erythroxylum (Eryth-roxylaceae) in the cerrado. Zoologia 28(1): 58–62. Google Scholar

7.

M. W. Gates , J. T. Lill , R. R. Kula , J. E. O'hara , D. B. Wahl , D. R. Smith , J. B. Whitfield , S. M. Murphy , and T. M. Stoepler 2012. Review of parasitoid wasps and flies (Hymenoptera: Diptera) associated with Limacodidae (Lepidoptera) in North America, with a key to genera. Proc. Entomol. Soc. Washington 114(1): 24–110. Google Scholar

8.

H. R. Gil-Santana , and M. T. Tavares 2005. Brachy-meria pandora (Crawford) (Hymenoptera: Chalcidi-dae): a new parasitoid of Historisodius (Fabricius) (Lepidoptera: Nymphalidae). Rev. Brasileira Zool. 22(4): 1211–1212. Google Scholar

9.

H. R. Gil-Santana , E. Nunez , and S. S. Nihei 2013. Lespesia melloi sp. nov. (Diptera: Tachinidae) from Brazil, parasitoid of Xanthopastis timais (Lepidoptera: Noctuidae). J. Insect Sci. (in press) Google Scholar

10.

J. A. Harvey , L. E. M. Vet , L. M. A. Witjes , and T. M. Be-Zemer 2006. Remarkable similarity in body mass of a secondary hyperparasitoid Lysibia nana and its primary parasitoid host Cotesia glomerata emerging from cocoons of comparable size. Arch. Insect Biochem. Physiol. 61(3): 170–183. Google Scholar

11.

D. F. Hayward 1990. The phenology and economic potential of Terminalia catappa L in south central Ghana. Vegetation 90(2): 125–131. Google Scholar

12.

B. Herting 1976. Lepidoptera, Part 2 (Macrolepidop-tera). A catalogue of parasites and predators of terrestrial arthropods. Section A. Host or Prey/Enemy 7(1): 83–84. Commonwealth Agric. Bureaux, CIBC. Google Scholar

13.

B. Herting 1978. Neuroptera, Diptera, Siphonaptera. A catalogue of parasites and predators of terrestrial arthropods. Section A. Host or Prey/Enemy 5(1): 110–111. Commonwealth Agric. Bureaux, CIBC. Google Scholar

14.

G. Salgado-Neto , R. A. Di Mare , and M. Lopes-Da-Silva 2010. Parasitism of Argon lota Hewitson (Lepidoptera: Hesperiidae) by Brachymeria pandora (Crawford) (Hymenoptera: Chalcididae) in Rio Grande do Sul, Brazil. Neotropical Entomol. 39(2): 311–312. Google Scholar

15.

M. N Santos , and M. L.F. Teixeira . 2010. Tropical almond seeds (Terminalia catappa L.) (Combretaceae) as a substrate for epiphytic orchid cultivation. Acta Sci. Agron. 32(2): 339–343. Google Scholar

16.

R. Silva-Fllho , P. C. R. Cassino , O. M. Marques , A. M. Penteado-Dias , W. C. Rodrigues , and J. C. Zanuncio 2007. Parasitoids of Polistes lanio lanio (Hymenoptera: Vespidae) larvae in the municipality of Seropédica, Rio de Janeiro State, Brazil. Sociobiology 50(3): 1191–1198. Google Scholar

17.

V. Stejskal , P. Kosina , and L. Kanyomeda 2006. Arthropod pests and their natural enemies in stored crops in northern Namibia. J. Pest Sci. 79(1): 51–55. Google Scholar

18.

M. T. Tavares , A. B. Navarro-Tavares , and G. D. S. Almeida 2006. The species of Chalcididae (Hymenoptera) parasitoids of Parides ascanius (Cramer), an endangered Papilionidae (Lepidoptera) from rest-ingas of southeastern Brazil. Zootaxa 1197(1): 55–63. Google Scholar

19.

W. S. Tavares , C. Hansson , J. E. Serrão , and J. C. Zanuncio 2011a. First report of Trichospilus pupivorus (Hymenoptera: Eulophidae) parasitizing pupae of Anticarsia gemmatalis (Lepidoptera: Noctuidae). Entomol. Gen. 33(4): 281–282. Google Scholar

20.

W. S. Tavares , T. V. Zanuncio , C. Hansson , J. E. Serrão , and J. C. Zanuncio 2011b. Emergence of Palmistichus elaeisis (Hymenoptera: Eulophidae) from pupae of Thagona tibialis (Lepidoptera: Lymantriidae) collected in the medicinal plant Terminalia catappa (Combretaceae). Entomol. News 122(3): 250–256. Google Scholar

21.

W. S. Tavares , L. Cruz, R. B. Silva , M. L. C. Figueiredo , F. S. Ramalho , J. E. Serrão , and J. C. Zanuncio 2011c. Soil organisms associated to the weed suppressant Crotalaria juncea (Fabaceae) and its importance as a refuge for natural enemies. Planta Daninha 29(3): 473–479. Google Scholar

22.

W. S. Tavares , O. H. H. Mielke , C. F. Wilcken , L. Simon , J. E. Serrão , and J. C. Zanuncio 2012. Palmistichus elaeisis (Hymenoptera: Eulophidae) parasitizing pupae of Citioica anthonilis (Lepidoptera: Saturniidae) collected on Piptadenia gonoacantha (Fabaceae). J. Lepid. Soc. 66(4): 216–220. Google Scholar

23.

W. S. Tavares , C. Hansson , O. H. H. Mielke , J. E. Serrão , and J. C. Zanuncio 2013a. Parasitism of Palmistichus elaeisis Delvare & LaSalle, 1993 on pupae of Methona themisto (Hübner, [1818]) reared on two hosts (Lepidoptera: Nymphalidae; Hymenoptera: Eulophidae). SHILAP-Rev. Lepidopterol. 41(161): 43–48. Google Scholar

24.

W. S. Tavares , M. A. Soares , O. H. H. Mielke , J. C. M. Poderoso , J. E. Serrão , and J. C. Zanuncio 2013b. Emergence of Palmistichus elaeisis Del-vare & LaSalle, 1993 (Hymenoptera: Eulophidae) from pupae of Heraclides anchisiades capys (Hübner, [1809]) (Lepidoptera: Papilionidae) in the laboratory. Folia Biol. -Krakow 61(3/4): 233–237. Google Scholar

25.

W. S. Tavares , C. Hansson , J. E. Serrão , and J. C. Zanuncio 2013c. First report of Tfichospilus pupivorus (Hymenoptera: Eulophidae) to the American continent and its parasitism on Thagona tibialis (Lepidoptera: Lymantriidae). Stud. Neotropical Fauna E. 48(2): 1–2. Google Scholar

26.

W. R. Thompson 1954. A catalogue of the parasites and predators of insect pests - Section 2 - Host parasite catalogue, Part 3 - Hosts of the Hymenoptera (Cal-liceratid to Evaniid). 198 pp. Commonwealth Agric. Bureaux, CIBC. Google Scholar

27.

R. S. Tinôco , R. C. Ribeiro, M. T. Tavares , E. F. Vilela , W. P. Lemos , and J. C. Zanuncio 2012. Brachy-meria spp. (Hymenoptera: Chalcididae) parasitizing pupae of Hersperidae and Nymphalidae (Lepidoptera) pests of oil palm in the Brazilian Amazonian region. Florida Entomol. 95(3): 788–789. Google Scholar

28.

S. F. Yang , M. K. Chen , Y. S. Hsieh , J. S. Yang, A. I. Zavras , Y H. Hsieh , S. C. Su, T. Y. Kao , P. N. Chen , and S. C. Chu 2010. Antimetastatic effects of Terminalia catappa L. on oral cancer via a down-regulation of metastasis-associated proteases. Food Chem. Toxicology 48(4): 1052–1058. Google Scholar

29.

B. Zaché , R. R. C. Zaché , M. T. Tavares , and C. F. Wilcken 2012. Brachymeria pandora (Crawford) (Hymenoptera: Chalcididae) as a new parasitoid of Thyrinteina leucocerae (Rindge) (Lepidoptera: Geo-metridae) in Brazil. Neotrop. Entomol. 41(4): 343–344. Google Scholar
Wagner De Souza Tavares, Jesusa Crisostomo Legaspi, Marcelo Teixeira Tavares, Enio Nunez, Rosenilson Pinto, and José Cola Zanuncio "Brachymeria koehleri (Hymenoptera: Chalcididae) as a Hyperparasitoid of Lespesia melloi (Diptera: Tachinidae) Pupae in Thagona tibialis (Lepidoptera: Lymantriidae) Caterpillars in Brazil," Florida Entomologist 96(4), 1635-1638, (1 December 2013). https://doi.org/10.1653/024.096.0457
Published: 1 December 2013
JOURNAL ARTICLE
4 PAGES


SHARE
ARTICLE IMPACT
Back to Top