670 Florida Entomologist 96(2) June 2013

PREDATION OF ZAPRINUS INDIANUS (DIPTERA: DROSOPHILIDAE) BY THE SOCIAL WASP SYNOECA CYANEA (HYMENOPTERA: VESPIDAE)

Fábio Prezoto* and Nayara Braga Depto. Zoologia, Programa de Pós-Graduação em Ciências Biológicas, Comportamento e Biologia Animal – ICB, Univ. Federal de Juiz de Fora, Campus Universitário-Martelos, 36.036-900, Juiz de Fora, Minas Gerais, Brazil

*Corresponding author; E-mail: [email protected]

Fruit fly species in several dipteran families social wasps on different groups of insect pests are mainly responsible for the damage dealt to in agroecosystems (Giannotti et al. 1995; Elisei fruit in Brazil by insects (Fernandes & Elton 2011; et al. 2010), and in urban gardens (Andrade & Zart et al. 2011). The females of such dipteran Prezoto 2001; Prezoto et al. 2005; Prezoto et al. families inflict direct damage to fruit by punctur- 2006). This study is the first record of predation ing it with their ovipositors, and the larvae, which of Z. indianus (Gupta) larvae by the social wasp develop within the fruit, render it largely unmar- Synoeca cyanea (F.), which suggests that natural ketable. Also these actions result in premature enemy is potentially useful as a biocontrol agent fruit drop, and facilitate the entry of bacteria or for practical use in fruit protection Brazil. fungi that cause rotting, which strongly devalues During the month of Apr 2012, we registered the fruit (Souza-Filho et al. 2003). the predatory behavior of the social wasp S. cyanea The control of these pests is difficult because on larvae of Z. indianus in fruits of Spanish prune of their prolific production of viable eggs, high (S. purpurea) in an agricultural property at Piraci- capacity of dispersion of the adults and coloniza- caba city (S 22° 43’ W 47° 38’), São Paulo State, tion in many different ecological conditions, and Brazil. During 3 consecutive days, we conducted very importantly, because the immature stages observations ad libitum (sensu Altmann, 1974) on develop within the fruits (Copeland et al. 2002; the behavior of wasps S. cyanea foraging on ripe Raga et al. 2005). fruits of Spanish prune from 8 AM to 6 PM. The best known species in the genus Zaprionus Synoeca cyanea initiated foraging behavior (Drosophilidae), is the fig fly,Zaprionus indianus by landing on the fruits of Spanish prune anten- (Gupta), a pest species, which is reported with nating them, i.e., continually touching different increasing frequency in the Brazilian territory. points on the fruit surface with the antennae, pos- The polyphagous Z. indianus species, which is be- sibly in search of chemical cues of prey (Fig. 1). lieved to have originated from Africa, was first re- We observed that S. cyanea workers always ex- ported in Brazil in 1999, near Valinhos, São Paulo hibited antennation of the fruit of Spanish prune, State, in a culture of figs. Subsequently, because and this behavior was more prolonged when the this species multiplied very rapidly (Vilela 1999; fruit being inspected had holes in its skin (exo- Raga et al. 2003), it is now one of the principal carp) created by other insects. economic pests in national fruit production. When the wasps detected the presence of Z. In Brazil, the flyZ. indianus has already been indianus larvae, they persistently malaxed the observed to inflict damage to the following fruits: site, sometimes shifting to a new site, but always acerola (Malpighia glabra L., Malpighiaceae), on the same fruit in their quest to capture the banana (Musa sp. Musaceae), cashew (Anacar- prey. Larvae of Z .indianus that were captured dium occidentale L., Anacardiaceae), carombola were 2-4 mm in length, and they were captured (Averrhoa carambola L., Oxilidaceae), citrus (Cit- individually. When the larva was removed from rus spp., Rutaceae), guava (Psidium guajava L., the fruit, the wasp was seen to be malaxing it, Myrtaceae), jaboticaba (Myrcia jaboticaba Baill., transforming it into the form of an acorn, which Myrtaceae), iamb (Syzygium jambos L. (Alston), the wasp transported to the colony. Myrtaceae), mango (Mangiferaindica L., Anacar- The capture of Z. indianus larvae occurred diaceae), strawberry (Fragaria sp., Rosaceae), throughout the day, being more intense in the hot- peach (Prunus persica (L.) Stokes, Rosaceae), test hours (1-3 PM), when we recorded 3 catches Spanish prune (Spondias purpurea L., Anacar- per hour. We did not register any other species of diaceae) and tomato (Lycopersicum esculentum wasp foraging in Spanish prune. L., Solanaceae) (Raga 2002). The wasps of the genus Synoeca have colonies Social wasps visit a wide variety of fruits to with hundreds of individuals and their nests can obtain nutrients such as carbohydrates and ani- stay active for many years (Castellón 1980). Of mal protein derived from the capture of adult the 4 species of this genus found in Brazil, S. cya- insects and/or immature insects that occur in nea is the most abundant, and easily located in fruits and that are used for feeding wasp larvae different kinds of phyto-physiognomy (Elisei et (Prezoto et al. 2008). In the Neotropics, several al. 2005; Henrique-Simões et al. 2011). In a study studies have described the predatory behavior of on the foraging activity of S. cyanea, Elisei et al. Scientific Notes 671

Fig. 1. A social wasp, Synoeca cyanea (F.), apparently hunting larvae of Zaprinus indianus (Gupta) in fruits of Spanish prune (Spondias purpurea, Anacadiaceae).

(2005) reported that this species presents intense Summary activity, with an average of 76 sorties and returns per h, and Elisei et al. (2010) verified that this This study is the first record of predation of wasp species is capable of carrying a load that Zaprinus indianus (Gupta) (Drosophilidae) fig fly corresponds to 10% of its body weight. larvae—which has recently become a major pest Sometimes the interactions between social in fruit production in Brazil—by the social wasp wasps and fruit are not harmonious. De Souza et Synoeca cyanea (F.) (Hymenoptera: Vespidae) in al. (2010) reported that S. cyanea is capable of fruits of Spanish prune (Spondias purpurea L. breaking the skin of jabuticaba fruits (Myrciaria Anacadiaceae) in an agricultural property, at Pi- sp.; Myrtales: Myrtaceae), which entails a loss, racicaba city, São Paulo State, Brazil. since the damaged fruit rots and loses its com- Key Words: fruit fly, natural enemy, biological mercial value. In another study, Brugger et al. control, exotic pest (2011) verified that the same wasp species also damages Psidium sp. fruits. In both cases, the Resumo authors believe that this action of wasps on fruits is the result of depletion of natural resources in Este estudo é o primeiro registro da pre- their environment, which forces individuals to dação de larvas da mosca do figo aprinusZ forage on alternative resources. indianus(Gupta) (Drosophilidae)—que tem se This intense foraging activity of S. cyanea as- tornado recentemente uma das principais pra- sociated with predation and its broad distribution gas da produção de frutas no Brasil- pela vespa throughout Brazil qualifies it as an interesting social Synoeca cyanea (F.) (Hymenoptera: Vespi- natural enemy of larvae of Z. indianus, and also dae) em frutos de seriguela (Spondias purpurea as a prospective candidate for use in integrated L. Anacadiaceae) em uma propriedade agrícola, pest management programs against dipteran na cidade de Piracicaba, estado de São Paulo, pests of fruit crops. Brasil. 672 Florida Entomologist 96(2) June 2013

Palavras Chave: mosca-das-frutas, inimigo na- Giannotti, E., Prezoto, F., and Machado, V. L. L. 1995. tural, controle biológico, praga exótica Foraging activity of Polistes lanio lanio (Fabr.) (Hy- menoptera, Vespidae). An. Soc. Entomol. Brasil 24: 455-463. References Cited Henrique-Simões, M., Cuozzo, M. D., and Frieiro-Costa, F. A. 2011. Social wasps of Unilavras/Boqueirão Bio- Altmann, J. 1974. Observational study of behavior: sam- logical Reserve, Ingaí, state of Minas Gerais, Brazil. pling methods. Behaviour 49(4): 227-267. Check List 7(5): 656-667. Andrade, F. R., and Prezoto, F. 2001. Horários de ativi- Prezoto, F., Cortes, S. A. O., and Melo, A. C. 2008. dade forrageadora e material coletado por Polistes Vespas: de vilãs a parceiras. Ciência Hoje 43(253): ferreri Saussure, 1853 (Hymenoptera, Vespidae), nas 70-72. diferentes fases de seu ciclo biológico. Rev. Brasileira Prezoto, F., Lima, M. A. P., and Machado, V. L. L. Zoociências 3: 117-128. 2005. Survey of preys captured and used by Polybia Brugger, B. P., Araújo, L. S., De Souza, A. R., and Prezo- platycephala(Richards) (Hymenoptera: Vespidae; to, F. 20101 Social wasps (Synoeca cyanea) damag- Epiponini). Neotrop. Entomol. 34(5): 849-851. ing Psidium sp. (Myrtaceae) fruits in Minas Gerais Prezoto, F., Santos-Prezoto, H. H., Machado, V. L. L., state, Brazil. Sociobiology 57: 533-535. and Zanuncio, J. C. 2006. Prey captured and used Castellón, E. G. 1980. Reprodução e dinâmica de popu- in Polistes versicolor (Olivier) (Hymenoptera: Vespi- lação em Synoeca surinama (Hymenoptera, Vespi- dae) nourishment. Neotrop. Entomol. 35(5): 707-709. dae). Acta Amazonica 10(3): 679-690. Raga, A. 2002 Mosca-do-figo, pp. 75-79In Anais do VII Copeland, R. S., Wharton, R. A., Luke, Q., and Meyer, Reunião Itinerante de Fitossanidade do Instituto Bi- M. 2002. Indigenous hosts of Ceratitis capitata (Dip- ológico Frutas. Indaiatuba. tera: Tephritidae) in Kenya. Ann. Entomol. Soc. Raga, A., and Souza-Filho, M. F. 2003. Captura de Za- America 95: 672-694. prionus indianus (Gupta) (Diptera: Drosophilidae) De Souza, A. R., Venancio, D. F. A., Zanuncio, J. C., and em frascos de plásticos com iscasalimentares na Prezoto, F. 2010. Sampling methods for assessing cultura do figo, Revista Agr. Piracicaba 78(3): 323- social wasps diversity in a eucalyptus plantation. J. 329. Econ. Entomol. 104: 1120-1123. Raga, A., Machado, R. A., Souza-Filho, M. F., Sato, M. Elisei, T., Junior, C. R., Guimarães, D. L., and Prezoto, E., and Siloto, R. C. 2005. Tephritoidea (Diptera) F. 2005. Foraging activity and nesting of swarm- species from Myrtaceae fruits in the state of São founding wasp Synoeca cyanea (Hymenoptera: Ves- Paulo, Brazil. Entomotropica 20: 11-14. pidae, Polistinae). Sociobiology 46(2): 317-327. Souza-Filho, M. F., Raga, A., and Zucchi, R. A. 2003. Elisei, T., Nunes, J. V., Ribeiro-Junior, C., Junior, A. J. Moscas-das-frutas no estado de São Paulo: ocorrên- F., and Prezoto, F. 2010. Uso da vespa social Polistes cia e danos. Laranja. Cordeirópolis 24(1): 45-69. versicolor no controle de desfolhadores de eucalipto. Vilela, C. R. 1999. Is Zaprionus indianus Gupta, 1970 Pesquisa Agropecuária Brasileira 45: 958-964. (Diptera, Drosophilidae) currently colonizing the Fernandes, D. R. R., and Araújo, E. L. 2011. Ocorrência Neotropical Region? Drosophila Inf. Serv. 82: 37-39. de Zaprionus indianus Gupta (Diptera: Drosophili- Zart, M., Botton, M., and Fernandes, A. O. 2011. In- dae) em frutos de juazeiro Ziziphus joazeiro mart. júrias causadas por mosca-das-frutas sul-americana (Rhamnaceae) no estado do Rio Grande do Norte. em cultivares de videira. Bragantia, Campinas Rev. Brasileira Fruticultura 33(4): 1356-1358. 70(1): 64-71.