SHILAP Revista de Lepidopterología ISSN: 0300-5267 [email protected] Sociedad Hispano-Luso-Americana de Lepidopterología España

Tavares, W. S.; Hansson, C.; Mielke, O. H. H.; Serrão, J. E.; Zanuncio, J. C. Parasitism of Palmistichus elaeisis Delvare & LaSalle, 1993 on pupae of themisto (Hübner, [1818]) reared on two hosts (: ; : ) SHILAP Revista de Lepidopterología, vol. 41, núm. 161, marzo, 2013, pp. 43-48 Sociedad Hispano-Luso-Americana de Lepidopterología Madrid, España

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How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative 43-48 Parasitism of Palmistichu 10/3/13 18:39 Página 43

SHILAP Revta. lepid., 41 (161), marzo 2013: 43-48 CODEN: SRLPEF ISSN: 0300-5267

Parasitism of Palmistichus elaeisis Delvare & LaSalle, 1993 on pupae of (Hübner, [1818]) reared on two hosts (Lepidoptera: Nymphalidae; Hymenoptera: Eulophidae)

W. S. Tavares, C. Hansson, O. H. H. Mielke, J. E. Serrão & J. C. Zanuncio

Abstract

Previous studies showed that larvae of Methona themisto (Hübner, [1818]) (Lepidoptera: Nymphalidae) display a showy yellow color to avoid predation. In addition, these larvae absorb secondary compounds when feeding on Brunfelsia uniflora (Pohl) D. Don () plants, although this does not prevent pupal parasitism by Palmistichus elaeisis Delvare & LaSalle, 1993 (Hymenoptera: Eulophidae). The aim of this study was to assess in the laboratory parasitism by P. elaeisis on pupae of M. themisto after their larvae fed on a new host plant, Inga edulis Martius (Fabaceae) (T1) cultivated in the herbarium of the Federal University of Viçosa (UFV) in Viçosa, Minas Gerais State, Brazil or on plants of B. uniflora (T2) cultivated in the campus of the UFV. The percentage of emergence, developmental time, number of individuals emerged and sex ratio of adults of P. elaeisis and the length and width of the pupae of M. themisto were similar between treatments (P > 0.05). Palmistichus elaeisis showed good reproductive performance when reared on pupae of the host M. themisto independently of larval food. KEY WORDS: Lepidoptera, Nymphalidae, Hymenoptera, Eulophidae, Biological control, Brunfelsia uniflora, defoliation, emergency, Fabaceae, Inga edulis, natural enemies, parasitism, pupal parasitoid, Solanaceae.

Parasitismo de Palmistichus elaeisis Delvare & LaSalle, 1993 sobre pupas de Methona themisto (Hübner, [1818]) observados sobre dos anfitriones (Lepidoptera: Nymphalidae; Hymenoptera: Eulophidae)

Resumen

Estudios anteriores indicaron que las larvas de Methona themisto (Hübner, [1818]) (Lepidoptera: Nymphalidae) muestran un marcado color amarillo para evitar ser víctimas de predadores. Por añadidura estas larvas absorben compuestos secundarios al alimentarse de plantas de Brunfelsia uniflora (Pohl) D. Don (Solanaceae), aunque esto no evita que las pupas sean parasitadas por Palmistichus elaeisis Delvare & LaSalle, 1993 (Hymenoptera: Eulophidae). El objeto de este estudio era valorar en el laboratorio el parasitismo de P. elaeisis sobre las pupas de M. themisto después de que sus larvas se alimentaran de una nueva planta huesped, Inga edulis Martius (Fabaceae) (T1), cultivada en el herbolario de la Universidad Federal de Vicosa (UFV), en Vicosa, Estado Minas Gerais, Brasil, o, alternativamente, de plantas de B. uniflora (T2) cultivadas en el campus de la UFV. El porcentaje de emergencia, tiempo de desarrollo, número de individuos emergidos, ratio de sexos de adultos de P. elaeisis y ancho y largo de pupas de M. themisto fueron similares durante los tratamientos (P >

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W. S. TAVARES, C. HANSSON, O. H. H. MIELKE, J. E. SERRÃO & J. C. ZANUNCIO

0.05). Palmistichus elaeisis muestra buen comportamiento reproductor cuando se cría sobre pupas de M. themisto, independientemente del alimento larvario. PALABRAS CLAVE: Lepidoptera, Nymphalidae, Hymenoptera, Eulophidae, control biológico, Brunfelsia uniflora, defoliación, emergencia, Fabaceae, Inga edulis, enemigos naturales, parasitismo, parasitoide pupal, Solanaceae.

Introduction

Inga edulis Martius (Fabaceae) is an Amazonian plant. Its trees reach 15 m high (DAWSON et al., 2008). This that achieves rapid growth, with open canopy, branches and leaves with leaflets attached to a rust-coloured hair shaft of rust-colored. Abundant white and green scented flowers throughout the year (HOLL et al., 2011; IGLESIAS et al., 2011). Green-colored 0.8 and 1.0 m fruit in pods, and seeds surrounded by an aerated and sweet aril (ALEXANDER & USMA, 1994; SOMARRIBA & BEER, 2011). Inga edulis is common at edges of rivers and lakes and has a scent attractive to wildlife and humans, as well as to bees (LARBI et al., 2000). Brunfelsia uniflora (Pohl) D. Don is a tree of the Solanaceae family originating in the Atlantic Rainforest in Brazil (MARTINS et al., 2009). Its leaves are small and permanent, with an average rate of growth and it can reach about 3 m height, with a 2 m diameter rounded crown (DUARTE & WOLF, 2010). Flowering occurs from September to March and produces white and lilac flowers. The fruit is of capsule type. This species is widely used as an ornament for its beauty and fragrance (MORAES et al., 2009). Methona themisto (Hübner, [1818]) (Lepidoptera: Nymphalidae) fly around moist and shaded places of the Brazilian Atlantic Rainforest. This play dead to stay alive when they are caught, displaying a warning coloration and remaining static for a few minutes, to avoid predators (MASSUDA & TRIGO, 2009). Females of M. themisto lay white colored eggs on the abaxial face of the leaves. Black caterpillars with yellow rings, larval and adult period of 30 days. Wings of adults with yellow, black and white dots and translucent regions (CORSATO-ALVARENGA et al., 1987; MASSUDA & TRIGO, 2009). Methona themisto adapts to urban environments on ornamental plants grown in parks and gardens, such as Araucaria araucana (Molina) K. Knoch, 1873 (Araucariaceae), B. uniflora and Brunfelsia pilosa Plowman (Solanaceae), Cordyline terminalis (L.) Kunth (Liliaceae), Dypsis lutescens (H. Wendl.) Beentje & J. Dransf. (Arecaceae), Hibiscus rosa-sinensis L. (Malvaceae), Philodendron hastatum K. Knoch & Sello (Araceae), Pilea cardieri Gagnep. & Guillamin (Urticaceae), Rhododendron simsii Planch. (Ericaceae), Spiraea spp. and Tectona grandis L. f. (Verbenaceae) (CORSATO-ALVARENGA et al., 1987; RUSZCZYK & NASCIMENTO, 1999). These plants may be larval hosts and/or source of nectar for adults of this species. A new genus of , including a new species named Palmistichus elaeisis Delvare & LaSalle, 1993 (Hymenoptera: Eulophidae) was described in the Neotropical region (DELVARE & LASALLE, 1993). The first report of parasitism of this Eulophidae was on pupae of Hispoleptis subfasciata Pic., 1938 (Coleoptera: Chrysomelidae), defoliating pest of oil palm Elaeis guineensis Jacq. (Arecaceae) (LE VERDIER & GENTY, 1988). This gregarious pupal endoparasitoid of Lepidoptera and Coleoptera is reared on alternative hosts and is used in the biological control of pests in various agricultural and forest crops (ANDRADE et al., 2010; PEREIRA et al., 2008, 2010, 2011). The hypothesis is that the biological parameters of P. elaeisis are different with M. themisto reared on I. edulis or B. uniflora. The objectives of this paper were: First, to assess the parasitism by P. elaeisis on M. themisto reared on Fabaceae or Solanaceae plants in the laboratory. Second, to report I. edulis as a new host for this Lepidoptera defoliator.

Material and methods

Fifty first instar larvae of M. themisto were collected on the adaxial face of leaves on an adult plant fruited of I. edulis in the herbarium of the Federal University of Viçosa (UFV) in Viçosa, Minas Gerais

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PARASITISM OF PALMISTICHUS ELAEISIS DELVARE & LASALLE, 1993 ON PUPAE OF METHONA THEMISTO (HÜBNER, [1818])

State, Brazil and hung on branches on an adult flowered plant of B. uniflora in the campus of the UFV (20º 45’ S, 42º 51’ W, 651 m - above sea level). These hosts were chosen because they are common in the region. This area has little sharp relief, fragments of secondary forest and diversified fauna (TAVARES et al., 2011a, 2012, 2013). These were brought to the Laboratory of Biological Control of Insects (LCBI) of UFV (25 ± 1 ºC temperature, 12 hours photoperiod and 70 ± 10% relative humidity of air) and placed in plastic cups with branches of I. edulis or B. uniflora until pupation. Forty newly formed pupae of this insect (20 - I. edulis and 20 - B. uniflora) were exposed for two days to parasitism by 10 mated females of P. elaeisis according to the methodology proposed for Tenebrio molitor L., 1758 (Coleoptera: Tenebrionidae) (ZANUNCIO et al., 2008). Each pupa was placed in a test tube. These tubes were closed with cotton swab and a drop of honey was placed per recipient as food for the parasitoids. Ten pupae of M. themisto were left in plastic cups until adulthood for species identification. Palmistichus elaeisis adults were obtained from a first generation emerged from pupae of Thagona tibialis Walker, 1855 (Lepidoptera: Lymantriidae) collected from an adult tree of Terminalia catappa L. (Combretaceae) on the campus of UFV (TAVARES et al., 2011b, 2012, 2013). The percentage of emergence, developmental time, number of emerged individuals and the sex ratio (number of females/number of males + number of females) of adults of P. elaeisis were evaluated. In addition, the length and width of the pupae of M. themisto to assess if size of pupae affects numbers of individual parasitoids that emerged, was also observed. The sex of P. elaeisis adults was determined based on morphological characteristics of their antenna and abdomen (DELVARE & LASALLE, 1993). Size measurements were obtained with a micrometric ocular coupled to a stereomicroscope. Some characteristics of the defoliation of M. themisto larvae on the plant of I. edulis were described. Palmistichus elaeisis was identified in the Department of Biology of Lund University in Sölvegatan, Lund, Sweden and M. themisto in the Department of Zoology of Federal University of Paraná (UFPR) in Curitiba, Paraná State, Brazil. The study had two treatments: pupae of M. themisto reared on I. edulis (T1) or B. uniflora (T2). These treatments were arranged in completely randomized design. Each treatment had 20 replications. Each replication was one by a pupa of M. themisto and 10 females of P. elaeisis per by test tube. Data were obtained from the mean ± standard error of mean. These means were submitted to variance analysis and were compared with the F test by means of GENES software (CRUZ, 2006).

Results

The percentage of emergence of P. elaeisis adults on M. themisto pupae was similar between treatments (P > 0.05), 92.84 and 100.00% reared on I. edulis and B. uniflora, respectively. The developmental time (parasitism-emergence) of P. elaeisis adults on M. themisto pupae was similar between treatments (P > 0.05), 22.31 ± 0.17 and 20.42 ± 0.15 days reared on I. edulis and B. uniflora, respectively. The number of individuals of P. elaeisis produced per pupa of M. themisto was similar between treatments (P > 0.05), 130 ± 8 and 138 ± 9 reared on I. edulis and B. uniflora, respectively. The sex ratio of P. elaeisis adults on M. themisto pupae was similar between treatments (P > 0.05), 0.91 ± 0.01 and 0.95 ± 0.02 reared on I. edulis and B. uniflora, respectively. The length and width (cm) of pupae of M. themisto were 2.7 ± 0.08 x 0.4 ± 0.05 cm and 2.9 ± 0.09 x 0.6 ± 0.07 cm reared on I. edulis and B. uniflora (P > 0.05), respectively. Methona themisto defoliated a tree of I. edulis in Viçosa, Minas Gerais State, Brazil and P. elaeisis parasitized pupae of this host reared on I. edulis. Larvae of this defoliator preferred younger leaves and they left the leaf ribs intact.

Discussion

This paper records the occurrence of I. edulis as a new host for M. themisto and the parasitism

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W. S. TAVARES, C. HANSSON, O. H. H. MIELKE, J. E. SERRÃO & J. C. ZANUNCIO

of adults of P. elaeisis on pupae of this defoliator reared on this plant or B. uniflora in Viçosa, Minas Gerais State, Brazil. Palmistichus elaeisis parasitized pupae of M. themisto after their larvae defoliated plants of the ornamental tree B. uniflora in Florianópolis, Santa Catarina State, Brazil (NARDI et al., 2006). This shows that this natural enemy parasitizes pupae of this Lepidoptera regardless of their host plant and place of occurrence. Caterpillars and pupae of M. themisto are yellowish and toxic to natural enemies. Feeding on B. uniflora, a plant rich in secondary compounds, did not prevent the parasitism of their pupae, and their larvae were preyed on by spiders and ants (MASSUDA & TRIGO, 2009; OPTIZ & MÜLLER, 2009). Predators that locate their prey by the color of the body, such as birds, avoided older caterpillars of this prey by being colorful and because the toxic activity of the dichloromethane extract from larvae by fifth instar of M. themisto (MASSUDA & TRIGO, 2009). Other natural enemies, such as Brachymeria annulata F., 1793 and Brachymeria mnestor Walker, 1841 (Hymenoptera: Chalcididae); Neotheronia sp. (Hymenoptera: Ichneumonidae) and Tetrastichus sp. (Hymenoptera: Eulophidae) parasitized pupae of M. themisto after this species fed on B. uniflora (NARDI et al., 2006). The parasitism of P. elaeisis on pupae of Cotesia sp. (Hymenoptera: Braconidae), H. subfasciata, Eupseudosoma involuta (Sepp, [1849]), (Lepidoptera: Arctiidae) and Euselasia eucerus (Hewitson, [1872]) (Lepidoptera: Riodinidae) (DELVARE & LASALLE, 1993) and other species of Lepidoptera of the Crambidae, Geometridae and Noctuidae families (BITTENCOURT & BERTI FILHO, 2004), shows the general character of this natural enemy.

Conclusion

Pupae of M. themisto, of larvae that fed on I. edulis or B. uniflora, were parasitized by the natural enemy P. elaeisis. This may create opportunities to use this parasitoid, regardless of the host plant and place of occurrence, in the biological control of this defoliator. In addition, finding out the secondary compounds and how the compounds affect parasitism of M. themisto by P. elaeisis needs to be conducted.

Acknowledgements

The authors thank Dr. Vitor Osmar Becker of the Institute Uiraçu in Camacan, Bahia State, Brazil by identifying Thagona tibialis Walker, 1855 (Lepidoptera: Lymantriidae). To Dr. Antônio Lélis Pinheiro of the Forestry Department of Federal University of Viçosa (UFV) in Viçosa, Minas Gerais State, Brazil by identifying Inga edulis Martíus (Fabaceae) and Brunfelsia uniflora (Pohl) D. Don (Solanaceae). To Dra. Mônica Ruediger de Britto Velho for English corrections and editing this manuscript. To “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq), “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior” (CAPES) and “Fundação de Amparo a Pesquisa do Estado de Minas Gerais” (FAPEMIG) for supporting this research.

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*W. S. T. C. H. Departamento de Fitotecnia Department of Biology Universidade Federal de Viçosa Lund University 36570-000 Sölvegatan 35 Viçosa, Minas Gerais State SE-22362 Lund BRASIL / BRAZIL SUECIA / SWEDEN E-mail: [email protected] E-mail: [email protected]

O. H. H. M. J. E. S. Departamento de Zoologia Departamento de Biologia Geral Universidade Federal do Paraná Universidade Federal de Viçosa Caixa Postal 19020 36570-000 Viçosa, Minas Gerais State 81531-980 Curitiba, Paraná State BRASIL / BRAZIL BRASIL / BRAZIL E-mail: [email protected] E-mail: [email protected]

J. C. Z. Departamento de Biologia Universidade Federal de Viçosa 36571-000 Viçosa, Minas Gerais State BRASIL / BRAZIL E-mail: [email protected]

*Autor para la correspondencia / Corresponding author

(Recibido para publicación / Received for publication 17-I-2012) (Revisado y aceptado / Revised and accepted 11-VI-2012) (Publicado / Published 30-III-2013)

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