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1 March 2014 Belvosia sp. (Diptera: Tachinidae) Parasitizing Halysidota sp. (Lepidoptera: Arctiidae) Caterpillars on Ficus benjamina (Moraceae) in Brazil
Wagner De Souza Tavares, Enio Nunez, José Eduardo Serrão, Marcus Alvarenga Soares, Carlos Frederico Wilcken, José Cola Zanuncio
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Ficus benjamina L. (Moraceae), an ornamental plant from south and southeast Asia and Australia and specifically Malaysia, was introduced in Brazil because of traits not observed in other species of this group, including branches almost at ground level and glossy oval leaves with the acuminate tips (Fang et al. 2007; Lazzarotto et al. 2011). This plant can exceed 20 m in height in tropical regions, and be imposing in urban sites, such as parks and gardens (Miao et al. 2011).

Halysidota Hübner (Lepidoptera: Arctiidae) species include caterpillars that defoliate Moraceae and Myrtaceae plants, e.g., Halysidota orientalis Rothschild, which defoliated Morus alba L. (Moraceae) in São Paulo (Sánchez-Soto et al. 2004). In addition H. pearsoni Watson defoliated Eucalyptus spp. (Myrtaceae) in Minas Gerais, Brazil and its pupae were parasitized by the gregarious generalist endoparasitoid, Palmistichus elaeisis Delvare & LaSalle (Hymenoptera: Eulophidae), in the laboratory (Pereira et al. 2008). This natural enemy is a promising biological control agent for defoliators in agroforestry systems (Tavares et al. 2011a, 2012a, 2013a, 2013b).

Belvosia Robineau-Desvoidy (Diptera: Tachinidae) species parasitize caterpillars and pupae of moths of the families Hesperiidae, Noctuidae, Saturniidae and Sphingidae (Arnaud 1978). Belvosia spp. (Diptera: Tachinidae) emerged from 70.7 to 96.2% of Hylesia metabus Cramer (Lepidoptera: Saturniidae) pupae during 6 generations in northeastern Venezuela (Hernandez et al. 2009). Belvosia bifasciata F. (Diptera: Tachinidae) emerged from 0.7% of Anisota senatoria J. E. Smith (Lepidoptera: Saturniidae) pupae in 2 generations in southeast Virginia, USA (Coffelt & Schultz 1993) and Belvosia bicincta Robineau-Desvoidy (Diptera: Tachinidae) emerged from 26% of the Hyles lineata F. (Lepidoptera: Saturniidae) pupae in eastern New Mexico, USA (Jorgensen 1988).

The aim of this study was to assess the emergence of Belvosia sp. from Halysidota sp. pupae obtained from caterpillars aggregated on F. benjamina trunk bases in Viçosa, Minas Gerais, Brazil.

Hundreds of Halysidota sp. caterpillars on F. benjamina were allowed to feed during the night on leaves of this plant until the last instar. Four separate groups of last-instar Halysidota sp. caterpillars (158, 144, 137 and 129 individuals) were collected daily over 4 days at 10:00 A.M. (Fig. 1). Caterpillars were collected from the base of 4 mature F. benjamina trees, which were 10 m tall and spaced 3 m apart in the “Recanto da Cigarra” locality (S 20° 45′ W 42° 51′, 651 m asl) on the campus of the Federal University of Viçosa (UFV) in Viçosa, Minas Gerais, Brazil. These groups were chosen because they were observed to be the most numerous during sampling.

Each group of Halysidota sp. caterpillars was placed in a 5 L-plastic container in the Laboratory of Biological Control of Insects (LCBI) of the UFV in a room at 25 ± 1 °C, 12:12 h L:D and 70 ± 10% R.H. Each group was separated in rearing cages (32 cm long × 30 cm wide × 30 cm high) with F. benjamina branches for ad libitum feeding and the branches were changed daily. Each cage had sterilized fine sand at the bottom with leaves and thin branches under the sand to favor cocoon formation and pupation. The bases of the branches were moistened with water in dental type anesthetic tubes to reduce leaf wilting. Each Halysidota sp. pupa was placed in a 50 mL-plastic cup sealed with polyvinyl chloride (PVC) film and held for lepidopteran or parasitoid emergence. The numbers of pupae formed from last-instar Halysidota sp. caterpillars collected on F. benjamina plants and the emergence of this lepidopteran and its dipteran parasitoid (Belvosia sp.) were carefully recorded.

Fig. 1.

Last-instar Halysidota sp. (Lepidoptera: Arctiidae) caterpillars on Ficus benjamina L. (Moraceae) trunk in Viçosa, Minas Gerais, Brazil.

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This is the first report of Halysidota sp. developing on F. benjamina as the host plant. Parasitoids were identified by E.N. as an undescribed species of Belvosia. The lepidopteran defoliator of F. benjamina was identified by Dr. Olaf Hermann Hendrik Mielke of the Department of Zoology of the Federal University of Paraná in Curitiba, Paraná, Brazil as an undescribed Halysidota species. Some of these individuals (flies and lepidopteran adults) were deposited at the Regional Museum of Entomology, Department of Entomology, UFV.

One species of Lepidoptera (Halysidota sp.) and one of Diptera (Belvosia sp.) were collected on plants of F. benjamina in this study. Groups of Halysidota sp. with an average of 142 caterpillars on F. benjamina trunks displayed a gregarious habit during the day. Each group of pupae had an average of 118 individuals (Table 1). Only one Halysidota sp. adult emerged in the laboratory from 472 pupae of this insect (Table 1). One Belvosia sp. parasitoid individual emerged per Halysidota sp. pupa, and the average emergence rate was 62.5 individuals per 118 Halysidota sp. pupae (Table 1).

This is the first report of Halysidota sp. defoliating F. benjamina in Brazil and the second record of a lepidopteran pest on this plant. Ammalo helops Cramer (Lepidoptera: Arctiidae) caterpillars were reported defoliating this plant in El Salvador (Horgan 2005). Natural enemies identified on this plant include the predator Montandoniola confusa Streito & Matocq (Hemiptera: Anthocoridae), which reduced the galls caused by Gynaikothrips uzeli Zimmerman (Thysanoptera: Phlaeothripidae) on F. benjamina plants by 95% (Arthurs et al. 2011). Defoliation of F. benjamina plants by Halysidota sp. can reduce its biomass (Tavares et al. 2012b).

The gregarious habit of Halysidota sp. caterpillars on F. benjamina trunks facilitates observation of their behavior during the day, but at night they disperse to feed on leaves of upper branches of this plant, as was found for A. helops (Horgan 2005). The early instars of the latter species may aggregate on F. benjamina stems plants in refuge areas not filled by older instars of the same species. Small groups of A. helops caterpillars were present in holes of rotting wood and among branches and aerial roots of F. benjamina. On the other hand, large groups of caterpillars aggregated mainly on trunks of this plant (Horgan 2005).

Table 1.

Number of caterpillars and percent pupation and mortality (%) of Halysidota sp. (Lepidoptera: Arctiidae), and the number of Belvosia sp. (Diptera: Tachinidae) individuals that emerged from Halysidota sp. pupae. the Halysidota sp. caterpillars were collected from Ficus benjamina (Moraceae) at Viçosa, Minas Gerais, Brazil.

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Although in this study more than 50% of Halysidota sp. pupae were parasitized by Halysidota sp., the emergence of only 1 Halysidota sp. adult from 472 pupae is consistent with the low emergence rate of H. orientalis. Caterpillars fed on host leaves in the laboratory, yielded only 1 female and 4 males from a large number of them collected in São Paulo, Brazil (Sánchez-Soto et al. 2004). However, an artificial diet for caterpillars and optimum temperature, photoperiod and R.H. conditions and protection from natural enemies might increase the emergence rate of Lepidoptera not adapted to the laboratory (Tavares et al. 2011b; Costa et al. 2012).

Identification of adults of the Halysidota genus is complex and based on wing color and morphology, especially the variations in the chromatic patterns of the forewings. Two H. orientalis males observed that had the reniform spot united with a medial band in the costal region and an incomplete postmedial band, while others had this reniform spot separated from the medial band and the post-medial band complete (Sánchez-Soto et al. 2004). The lengths of the labial palps can be used to differentiate Halysidota spp. pupae from those of other genera of Arctiidae (Mosher 1969). Halysidota species can be differentiated by the morphology of male genitalia, and in this way Halysidota interlineata Walker (Lepidoptera: Arctiidae) is distinguished from H. orientalis (Watson 1980). Ferguson & Opler (2006) asserted that 282 Arctiidae species from North America to northern Mexico were reported since the last revision of this group in 1983.

The emergence of Belvosia sp. from Halysidota sp. pupae suggests that has considerable potential as a biocontrol agent. Belvosia sp. parasitized 22% of A. helops caterpillars, but lower rates of larger and older groups in large refuge areas on F. benjamina trees. This shows that larger groups of caterpillars and gregariousness are defensive formations (Horgan 2005). Tachinidae were reported flying near F. benjamina trunks with infested with A. helops caterpillars during the day (Horgan 2005). This lepidopteran showed defensive behavior with sudden movements of the head, while those in plant refuges were not disturbed (Horgan 2005). The parasitism rate of 50% by Belvosia sp. suggests that the final instar caterpillars in small groups on open trunks of trees (not refugees) were more vulnerable to natural enemies than those in refugees and in large groups (Horgan 2005).

Halysidota sp. caterpillars were found feeding on F. benjamina plants in Viçosa, Minas Gerais, Brazil and they were heavily parasitized by Belvosia sp. This parasitoid can reduce Halysidota sp. populations, and thereby facilitate the propagation and use of F. benjamina as a popular ornamental.

We thank the Brazilian institutions: “Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)”, “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)” and “Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG)” for financial support.

Summary

Ficus benjamina L. (Moraceae) is an exotic ornamental plant in Brazil. The aim of this study was to identify a defoliator and its parasitoid on F. benjamina plants in Viçosa, Minas Gerais, Brazil and to determine the number of pupae and the emergence of lepidopteran and a dipteran. Four Halysidota sp. (Lepidoptera: Arctiidae) groups, with 158, 144, 137 and 129 last-instar caterpillars aggregated on the trunks of 4 F. benjamina trees. These caterpillars were collected, held in plastic containers with ficus leaves until development and emergence were completed. Adults of 1 undescribed lepidopteran species (Halysidota) and 1 dipteran species [Belvosia (Tachinidae)] emerged from the Halysidota pupae. An average of 118 viable Halysidota pupae per group were formed, and an average of 62.5 Belvosia individuals emerged from these host pupae per Halysidota group. From a grand total of 472 Halysidota pupae only one adult emerged. Halysidota sp. damaged F. benjamina plants in Viçosa, Minas Gerais, Brazil, but this defoliator was parasitized by Belvosia sp. The findings reported here indicate that Belvosia sp. appears to have the potential to reduce populations of Halysidota sp. and possibly protect F. benjamina in ornamental plantings.

Key Words: Arctiinae, Exoristinae, gregarism, parasitism, Rosales

Resumo

Ficus benjamina L. (Moraceae) é uma espécie ornamental exótica cultivada no Brasil. O objetivo foi identificar um desfolhador e seu parasitoide em plantas de F. benjamina em Viçosa, Minas Gerais, Brasil e determinar o número de pupas e a taxa de emergência dos Lepidoptera e dos Diptera. Quatro grupos de Halysidota sp. (Lepidoptera: Arctiidae), com 158, 144, 137 e 129 lagartas de últimos estádios agregadas sobre os troncos de 4 árvores de F. benjamina foram coletados. Uma espécie não-descrita de Lepidoptera (Halysidota) e outra de Diptera [Belvosia (Tachinidae)] foram obtidas. Os números de pupas foram, em média, de 118 por grupo. A taxa de emergência do Diptera foi de 62,5 indivíduos por grupo de lagartas. Halysidota sp. danificou plantas de F. benjamina em Viçosa, Minas Gerais, Brasil, mas foi parasitada por Belvosia sp. Isso mostra a importância desse Tachinidae para reduzir populações deste desfolhador de F. benjamina, a qual é cultivada como ornamental.

Palavras Chave: Arctiinae, Exoristinae, gregarismo, parasitismo, Rosales

References Cited

1.

P. H. Arnaud Jr 1978. A host-parasite catalog of North American Tachinidae (Diptera). Washington, D.C.: United States Department of Agriculture. Miscellaneous Publication 1319(1): 1–860. Google Scholar

2.

S. Arthurs , J. J. Chen , M. Dogramaci , A. D. Ali , and C. Mannion 2011. Evaluation of Montandoniola confusa Streito and Matocq sp. nov. and Orius insidiosus Say (Heteroptera: Anthocoridae), for control of Gynaikothrips uzeli Zimmerman (Thysanoptera: Phlaeothripidae) on Ficus benjamina. Biol. Control 57(3): 202–207. Google Scholar

3.

P. B. Avery , C. M. Mannion , C. A. Powel , C. L. McKenzie , and L. S. Osborne 2011. Natural enemies managing the invasion of the fig whitefly, Singhiella simplex (Hemiptera: Aleyrodidae), infesting a Ficus benjamina hedge. Florida Entomol. 94(3): 696–698. Google Scholar

4.

M. A. Coffelt , and P. B. Schultz 1993. Larval parasitism of orange striped oakworm (Lepidoptera, Saturniidae) in the urban shade tree environment. Biol. Control 3(2): 127–134. Google Scholar

5.

M. A. Costa , W. S. Tavares , A. I. A. Pereira , I. 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

6.

J. Fang , J. Chen , R. J. Henny , and C. C. T. Chao 2007. Genetic relatedness of ornamental Ficus species and cultivars analyzed by amplified fragment length polymorphism markers. J. American Soc. Hortic. Sci. 132(6): 807–815. Google Scholar

7.

D. C. Ferguson , and P. A. Opler 2006. Checklist of the Arctiidae (Lepidoptera: Insecta) of the continental United States and Canada. Zootaxa 1(1): 1–33. Google Scholar

8.

J. V. Hernandez , F. Osborn , B. Herrera , C. V. Liendo- Barandiaran , J. Perozo , and D. Velasquez 2009. Larvae-pupae parasitoids of Hylesia metabus Cramer (Lepidoptera: Saturniidae) in Northeastern Venezuela: a case of natural biological control. Neotrop. Entomol. 38(2): 243–250. Google Scholar

9.

F. G. Horgan 2005. Two types of refuge have opposite effects on the size of larval aggregations in a tropical defoliator. European J. Entomol. 102(2): 225–230. Google Scholar

10.

N. M. Jorgensen 1988. Belvosia bicincta (Diptera, Tachinidae) parasitizing larvae of the white lined sphinx moth in Eastern New Mexico. Entomol. News 99(2): 85–86. Google Scholar

11.

C. M. Lazzarotto , S. M. N. Lazzari , and S. R. C. Penteado 2011. Feeding behavior of two exotic aphid species on their original hosts in a new invaded area. Neotrop. Entomol. 40(3): 316–321. Google Scholar

12.

B. G. Miao , D. R. Yang , C. Liu , Y. Q. Peng , and S. G. Compton 2011. The impact of a gall midge on the reproductive success of Ficus benjamina, a potentially invasive fig tree. Biol. Control 59(2): 228–233. Google Scholar

13.

E. Mosher 1969. Lepidoptera pupae: Five collected works on the pupae of North American Lepidoptera. Michigan, ERS, 323p. Google Scholar

14.

F. F. Pereira , T. V. Zanuncio , J. C. Zanuncio , D. Pratissoli , and M. T. Tavares 2008. Species of Lepidoptera defoliators of Eucalyptus as new host for the parasitoid Palmistichus elaeisis (Hymenoptera: Eulophidae). Brazilian Arch. Biol. Technol. 51(2): 259–262. Google Scholar

15.

S. Sánchez-Soto , F. C. B. Roman , and O. Nakano 2004. Ocurrence of Halysidota orientalis Rothschild (Lepidoptera: Arctiidae) on mulberry (Morus alba L.) in São Paulo State, Brazil. Neotrop. Entomol. 33(4): 517–518. Google Scholar

16.

W. S. Tavares , C. Hanss on , 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. Lepidopt. 41(161): 43–48. Google Scholar

17.

W. D. Tavares , T. V. Zanuncio , C. Hansson , J. E. Serrão , and J. C. Zanuncio 2011a. 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

18.

W. D. Tavares , O. H. H. Mielke , C. F. Wilcken , L. Simon , J. E. Serrão , and J. C. Zanuncio 2012a. 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

19.

W. D. Tavares , G. Salgado-Neto , J. C. Legaspi , F. D. Ramalho , J. E. Serrão , and J. C. Zanuncio 2012b. Biological and ecological consequences of Diolcogaster sp. (Hymenoptera: Braconidae) parasitizing Agaraea minuta (Lepidoptera: Arctiidae) and the effects on two Costus (Costaceae) plant species in Brazil. Florida Entomol. 95(4): 966–970. Google Scholar

20.

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 Delvare & 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

21.

W. S. Tavares , I. Cruz , R. B. Silva , M. L. C. Figueiredo , F. S. Ramalho , J. E. Serrão , and J. C. Zanuncio 2011b. 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.

A. Watson 1980. A revision of the Halysidota tessellaris species-group (Halysidota sensu stricto) (Lepidoptera: Arctiidae). Bull. British Mus. Nat. Hist. (Entomol.) 40(1): 1–65.  Google Scholar
Wagner De Souza Tavares, Enio Nunez, José Eduardo Serrão, Marcus Alvarenga Soares, Carlos Frederico Wilcken, and José Cola Zanuncio "Belvosia sp. (Diptera: Tachinidae) Parasitizing Halysidota sp. (Lepidoptera: Arctiidae) Caterpillars on Ficus benjamina (Moraceae) in Brazil," Florida Entomologist 97(1), 272-276, (1 March 2014). https://doi.org/10.1653/024.097.0138
Published: 1 March 2014
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