Insect pests, including Dione juno juno Cramer, 1779 (Lepidoptera: Nymphalidae), feed on leaves and branches, reducing the production of the yellow passion fruit Passiflora edulis Sims (Boiça Júnior et al., 2008BOIÇA JÚNIOR, A.L., ANGELINI, M.R. and OLIVEIRA, J.C., 2008. Aspectos biológicos de Dione juno juno (Cramer) (Lepidoptera: Nymphalidae) em genótipos de maracujazeiro. Revista Brasileira de Fruticultura, vol. 30, no. 1, pp. 101-105. http://dx.doi.org/10.1590/S0100-29452008000100019.
http://dx.doi.org/10.1590/S0100-29452008... ). This pest is mainly controlled with chemical insecticides that can contaminate food, water, and soil, besides reducing populations of natural enemies and facilitating the emergence of resistant insects (Amatuzzi et al., 2018AMATUZZI, R.F., CARDOSO, N., POLTRONIERI, A.S., POITEVIN, C.G., DALZOTO, P., ZAWADENEAK, M.A. and PIMENTEL, I.C., 2018. Potential of endophytic fungi as biocontrol agents of Duponchelia fovealis (Zeller) (Lepidoptera: crambidae). Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 78, no. 3, pp. 429-435. http://dx.doi.org/10.1590/1519-6984.166681. PMid:29160362.
http://dx.doi.org/10.1590/1519-6984.1666... ; Costa et al., 2020COSTA, E.S.P., SOARES, M.A., CALDEIRA, Z.V., VELOSO, R.V.S., SILVA, L.A., SILVA, D.J.H., SANTOS, I.C.L., CASTRO, B.M.C., ZANUNCIO, J.C. and LEGASPI, J.C., 2020. Selectivity of deltamethrin doses on Palmistichus elaeisis (Hymenoptera: Eulophidae) parasitizing Tenebrio molitor (Coleoptera: Tenebrionidae). Scientific Reports, vol. 10, no. 1, pp. 12395. http://dx.doi.org/10.1038/s41598-020-69200-x. PMid:32709920.
http://dx.doi.org/10.1038/s41598-020-692... ). Biological control agents of D. juno juno (e.g., Eulophidae, Formicidae, Pentatomidae, Tachinidae and Vespidae) naturally regulate populations of this defoliating lepidopteran in P. edulis crops (Moreira et al., 1998MOREIRA, L.A., ZANUNCIO, J.C. and MOLINA-RUGAMA, A.J., 1998. Dados biológicos de Podisus nigrispinus (Dallas) alimentado com a lagarta do maracujazeiro Dione juno juno (Cramer). Anais da Sociedade Entomológica do Brasil, vol. 27, no., 4, pp. 645-647. http://dx.doi.org/10.1590/S0301-80591998000400018.
http://dx.doi.org/10.1590/S0301-80591998... ; Gil-Santana and Tavares, 2006GIL-SANTANA, H.R. and TAVARES, M.T., 2006. Palmistichus elaeisis Delvare & LaSalle (Hymenoptera, Eulophidae): a new parasitoid of Dione juno juno (Cramer) (Lepidoptera, Nymphalidae). Revista Brasileira de Zoologia, vol. 23, no. 3, pp. 891-892. http://dx.doi.org/10.1590/S0101-81752006000300040.
http://dx.doi.org/10.1590/S0101-81752006... ; Murgas et al., 2020MURGAS, A.S., MARTÍNEZ, A. and RODRÍGUEZ, L.M., 2020. Enemigos naturales de Dione juno (Cramer, 1779) (Lepidoptera: Nymphalidae) en cultivo de Passiflora edulis Sims, J. (1818). Centro Regional Universitario de Cocle, Universidad de Panamá. Tecnociencia, vol. 22, no. 1, pp. 97-108. http://dx.doi.org/10.48204/j.tecno.v22n1a7.
http://dx.doi.org/10.48204/j.tecno.v22n1... ). Social wasps forage water, plant fibbers, and protein. These insects approach, touch with the antennae, capture, kill and cut their prey into pieces, consuming or transporting them to their colonies (Silva-Filho et al., 2020SILVA-FILHO, R., BRÜGGER, B.P., CORRÊA, C.A., SOUZA, L.S.A., CASSINO, P.C.R., ZANUNCIO, J.C., SILVA, P.R R., SOARES, M.A. and ZANUNCIO, A.J.V., 2020. Flight distance and return capacity of Polistes lanio lanio (Hymenoptera: Vespidae) workers. The Florida Entomologist, vol. 103, no. 1, pp. 38-40. https://doi.org/10.1653/024.103.0406.
https://doi.org/10.1653/024.103.0406... ).

Predatory social wasps feed preferentially on immature Lepidoptera and generally return to continue searching for resources in successful locations, reducing populations of lepidopteran pests (Southon et al., 2019SOUTHON, R.J., FERNANDES, O.A., NASCIMENTO, F.S. and SUMNER, S., 2019. Social wasps are effective biocontrol agents of key lepidopteran crop pests. Proceedings of the Royal Society B: Biological Sciences, vol. 286, no. 1914, pp. 20191676. http://dx.doi.org/10.1098/rspb.2019.1676.
http://dx.doi.org/10.1098/rspb.2019.1676... ; Murgas et al., 2020MURGAS, A.S., MARTÍNEZ, A. and RODRÍGUEZ, L.M., 2020. Enemigos naturales de Dione juno (Cramer, 1779) (Lepidoptera: Nymphalidae) en cultivo de Passiflora edulis Sims, J. (1818). Centro Regional Universitario de Cocle, Universidad de Panamá. Tecnociencia, vol. 22, no. 1, pp. 97-108. http://dx.doi.org/10.48204/j.tecno.v22n1a7.
http://dx.doi.org/10.48204/j.tecno.v22n1... ). Polistes is one of the most efficient wasp genera controlling agricultural pests (Prezoto and Gobbi, 2005PREZOTO, F. and GOBBI, N., 2005. Flight range extension in Polistes simillimus Zikán, 1951 (Hymenoptera, Vespidae). Brazilian Archives of Biology and Technology, vol. 48, no. 6, pp. 947-950. http://dx.doi.org/10.1590/S1516-89132005000800011.
http://dx.doi.org/10.1590/S1516-89132005... ).

Polistes satan Bequaert, 1940 (Hymenoptera: Vespidae) occurs in the Neotropical region and has been reported in the states of Goiás, Minas Gerais, and São Paulo, Brazil, in the Atlantic Forest and Cerrado biomes (Souza et al., 2020aSOUZA, M.M., TEÓFILO-GUEDES, G.S., BUENO, E.T., MILANI, L.R. and SOUZA, A.S.B., 2020a. Social wasps (Hymenoptera, Polistinae) from the Brazilian savanna. Sociobiology, vol. 67, no. 2, pp. 129-138. http://dx.doi.org/10.13102/sociobiology.v67i2.4958. , bSOUZA, M.M., TEOFILO-GUEDES, G.S., MILANI, L.R., SOUZA, A.S.B. and GOMES, P.P., 2020b. Social wasps (Vespidae: Polistinae) from the Brazilian Atlantic Forest. Sociobiology, vol. 67, no. 1, pp. 1-12. http://dx.doi.org/10.13102/sociobiology.v67i1.4597.
http://dx.doi.org/10.13102/sociobiology.... ). This eusocial insect lives in large satellite-type colonies, attacking a wide variety of prey that makes up its diet, such as insects of the orders Coleoptera, Diptera, Hymenoptera and Lepidoptera (Southon et al., 2019SOUTHON, R.J., FERNANDES, O.A., NASCIMENTO, F.S. and SUMNER, S., 2019. Social wasps are effective biocontrol agents of key lepidopteran crop pests. Proceedings of the Royal Society B: Biological Sciences, vol. 286, no. 1914, pp. 20191676. http://dx.doi.org/10.1098/rspb.2019.1676.
http://dx.doi.org/10.1098/rspb.2019.1676... ).

The objective was to report P. satan preying on D. juno juno pupae in a P. edulis plantation.

Daily monitoring, during a period of 20 days, of P. edulis plants in the horticultural sector of the “Federal University of the Jequitinhonha and Mucuri Valleys (UFVJM)”, Campus JK in Diamantina, Minas Gerais state, Brazil (18º 12' S, W 43º34' W; 1,387 m a.s.l.) from September to October 2020 allowed the observation of wasps preying on Lepidoptera pupae.

The wasps were collected, placed in 500 mL plastic pots, and transported to the UFVJM Cytology and Histology laboratory. They were photographed using a Canon EOS Rebel T7I camera and LED Segurimax^© lights.

A taxonomist confirmed the identification of the lepidopteran as D. juno juno. Voucher specimens were sent and deposited in the entomological collection of the Department of Zoology at the Federal University of Paraná. Wasp specimens, collected with an entomological net, were identified as P. satan. Voucher species were deposited in the Coleção Biológica de Vespas Sociais (CBVS) of the IFSULDEMINAS, Campus Inconfidentes, registration number 06530-2021.

Polistes satan (Figure 1A) captured and fed on D. juno juno pupae on P. edulis plants. This wasp used its mandible to separate the thorax from the abdomen of the prey pupae and consumed the interior contents of its abdomen.

Figure 1
Polistes satan (Hymenoptera: Vespidae), side (A and B) and frontal (C) views, head in dorsal view (D), antenna (E), view of the tegula (F), Midleg (G), pronotal with visualization of the keel (H).

The average length of P. satan is 21.0 to 22.0 mm with black color and head and thorax with light ferruginous traces. Antennae with the first three and the last three segments ferruginous darkened. Black leg, distally narrow femurs, tibiae, ferruginous anterior tarsi, and yellow mid and posterior tarsi. Dark brown tegulae. Black wings and venation, moderate or small pronotal fovea, moderately elevated pronotal keel, elevated metanotum above the anterior scutellum, strong propodal striations, long, narrow, pointed muscle above, and Strong mesepistemal punctures are characteristic of this wasp (Figure 1) (Richards, 1978RICHARDS, O.W., 1978. Social wasps of the Americas excluding the Vespinae. London: British Museum (Natural History), 580 p.).

Polistes satan has been reported preying on Diatraea saccharalis Fabricius 1794 (Lepidoptera: Crambidae) and Spodoptera frugiperda J.E. Smith (Lepidoptera: Noctuidae) caterpillars exposed or protected inside the corn or sugarcane stalks, in the state of São Paulo, Brazil (Southon et al., 2019SOUTHON, R.J., FERNANDES, O.A., NASCIMENTO, F.S. and SUMNER, S., 2019. Social wasps are effective biocontrol agents of key lepidopteran crop pests. Proceedings of the Royal Society B: Biological Sciences, vol. 286, no. 1914, pp. 20191676. http://dx.doi.org/10.1098/rspb.2019.1676.
http://dx.doi.org/10.1098/rspb.2019.1676... ). This confirms the importance and the predatory habit of this wasp, such as that reported for Mischocyttarus angulatus Richards, 1945 (Hymenoptera: Vespidae), in the province of Coclé, Panama and Polybia fastidiosuscula Saussure, 1854, and Polybia scutellaris White, 1841 (Hymenoptera: Vespidae) in the municipality of Viçosa, Minas Gerais, Brazil, also feeding on D. juno juno caterpillars and pupae (Murgas et al., 2020MURGAS, A.S., MARTÍNEZ, A. and RODRÍGUEZ, L.M., 2020. Enemigos naturales de Dione juno (Cramer, 1779) (Lepidoptera: Nymphalidae) en cultivo de Passiflora edulis Sims, J. (1818). Centro Regional Universitario de Cocle, Universidad de Panamá. Tecnociencia, vol. 22, no. 1, pp. 97-108. http://dx.doi.org/10.48204/j.tecno.v22n1a7.
http://dx.doi.org/10.48204/j.tecno.v22n1... ; Moura et al., 2000MOURA, M.F.D., PICANÇO, M., GONRING, A.H.R. and BRUCKNER, C.H., 2000. Seletividade de inseticidas a três Vespidae predadores de Dione juno juno (Lepidoptera: heliconidae). Pesquisa Agropecuária Brasileira, vol. 35, no. 2, pp. 251-257. http://dx.doi.org/10.1590/S0100-204X2000000200003.
http://dx.doi.org/10.1590/S0100-204X2000... ). Protonectarina sylveirae Saussure, 1854 (Hymenoptera: Vespidae) preyed on caterpillars and pupae of D. juno juno and of Bedellia somnulentella Zeller, 1847 (Lepidoptera: Bedelliidae), whereas P. satan preyed only on pupae of this prey (Moura et al., 2000MOURA, M.F.D., PICANÇO, M., GONRING, A.H.R. and BRUCKNER, C.H., 2000. Seletividade de inseticidas a três Vespidae predadores de Dione juno juno (Lepidoptera: heliconidae). Pesquisa Agropecuária Brasileira, vol. 35, no. 2, pp. 251-257. http://dx.doi.org/10.1590/S0100-204X2000000200003.
http://dx.doi.org/10.1590/S0100-204X2000... ; Cabral et al., 2022CABRAL, M.J.S., SILVA, I.M., PINHEIRO, R.A., SANTOS, M.M., SOARES, M.A., PLATA-RUEDA, A., CASTRO, B.M.C., SILVA, W.M., SILVA, E.S. and ZANUNCIO, J.C., 2022. Protonectarina sylveirae (Hymenoptera: Vespidae): first report preying Bedellia somnulentella (Lepidoptera: Bedelliidae) in Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 84, no. 5, p. e256779. http://dx.doi.org/10.1590/1519-6984.256779. PMid:35239790.
http://dx.doi.org/10.1590/1519-6984.2567... ). However, prey handling by social Vespidae varies as Synoeca cyanea Fabricius, 1775 (Hymenoptera: Vespidae) that removed Zaprionus indianus Gupta, 1970 (Diptera: Drosophilidae) larvae from the fruit and macerated it into a food mass, to facilitate feeding (Prezoto and Braga, 2013PREZOTO, F. and BRAGA, N., 2013. Predation of Zaprinus indianus (Diptera: Drosophilidae) by the social wasp Synoeca cyanea (Hymenoptera: Vespidae). The Florida Entomologist, vol. 96, no. 2, pp. 670-672. http://dx.doi.org/10.1653/024.096.0243.
http://dx.doi.org/10.1653/024.096.0243... ) and Agelaia testacea Fabricius, 1804 (Hymenoptera: Vespidae) that immobilized with its legs and pierced the abdomen of Parascudderia sp. (Orthoptera: Tettigoniidae) to feed (Pinedo Garcia et al., 2022PINEDO GARCIA, R.B., ROJAS, R.R., SÁNCHEZ, C., MENDES, D.M.M. and SOMAVILLA, A., 2022. Hunting from the air: a new record of predation of Agelaia testacea (Fabricius, 1804) (Vespidae: Polistinae) on a katydid Parascudderia sp. (Orthoptera: Tettigoniidae: Phaneropterinae) in the Peruvian Amazon. Entomological Communications, vol. 4, no. 1, pp. ec04006. http://dx.doi.org/10.37486/2675-1305.ec04006.
http://dx.doi.org/10.37486/2675-1305.ec0... ).

Lepidoptera pupae predation is more common because they are immobile. In contrast, caterpillars can be aggressive, with defensive behaviors such as those of Thyrinteina arnobia Stoll, 1782 (Lepidoptera: Geometridae) camouflaging themselves, attacking with their jaws or hanging from silk threads to reduce predation by Podisus fuscescens (Dallas, 1851) (Hemiptera: Pentatomidae) (reported as P. distinctus) (Soares et al., 2009aSOARES, M.A., ZANUNCIO, J.C., LEITE, G.L.D., WERMELINGER, E.D. and SERRÃO, J.E., 2009a. Does Thyrinteina arnobia (Lepidoptera: Geometridae) use different defense behaviours against predators? Journal of Plant Diseases and Protection, vol. 116, no. 1, pp. 30-33. http://dx.doi.org/10.1007/BF03356283.
http://dx.doi.org/10.1007/BF03356283... ). In addition, pupae of T. arnobia rotate, difficulting their attack by natural enemies (Soares et al., 2009bSOARES, M.A., TORRES-GUTIERREZ, C., COLA-ZANUNCIO, J., PEDROSA, A.R.P. and LORENZON, A.S., 2009b. Superparasitismo de Palmistichus elaeisis (Hymenoptera: Eulophidae) y comportamiento de defensa de dos hospederos. Revista Colombiana de Entomologia, vol. 35, no. 1, pp. 62-65. http://dx.doi.org/10.25100/socolen.v35i1.9191.
http://dx.doi.org/10.25100/socolen.v35i1... ). Mormidea noulata Herrich Schaeffer, 1844 and Podisus nigrispinus Dallas, 1851 (Hemiptera: Pentatomidae) also fed on D. juno juno caterpillars and pupae in the municipality of Viçosa, State of Minas Gerais, Brazil (Murgas et al., 2020MURGAS, A.S., MARTÍNEZ, A. and RODRÍGUEZ, L.M., 2020. Enemigos naturales de Dione juno (Cramer, 1779) (Lepidoptera: Nymphalidae) en cultivo de Passiflora edulis Sims, J. (1818). Centro Regional Universitario de Cocle, Universidad de Panamá. Tecnociencia, vol. 22, no. 1, pp. 97-108. http://dx.doi.org/10.48204/j.tecno.v22n1a7.
http://dx.doi.org/10.48204/j.tecno.v22n1... ; Moreira et al., 1998MOREIRA, L.A., ZANUNCIO, J.C. and MOLINA-RUGAMA, A.J., 1998. Dados biológicos de Podisus nigrispinus (Dallas) alimentado com a lagarta do maracujazeiro Dione juno juno (Cramer). Anais da Sociedade Entomológica do Brasil, vol. 27, no., 4, pp. 645-647. http://dx.doi.org/10.1590/S0301-80591998000400018.
http://dx.doi.org/10.1590/S0301-80591998... ). Palmistichus elaeisis Delvare & LaSalle, 1993 (Hymenoptera: Eulophidae) parasitized pupae of D. juno juno in the State of Rio de Janeiro, Brazil (Gil-Santana and Tavares, 2006GIL-SANTANA, H.R. and TAVARES, M.T., 2006. Palmistichus elaeisis Delvare & LaSalle (Hymenoptera, Eulophidae): a new parasitoid of Dione juno juno (Cramer) (Lepidoptera, Nymphalidae). Revista Brasileira de Zoologia, vol. 23, no. 3, pp. 891-892. http://dx.doi.org/10.1590/S0101-81752006000300040.
http://dx.doi.org/10.1590/S0101-81752006... ) and Chetogena aff. scutellaris (Wulp, 1890) (Diptera: Tachinidae) parasitized pupae of D. juno juno with records of the first interaction of Brachymeria koehleri Blanchard, 1935 (Hymenoptera: Chalcididae) as a hyperparasitoid in Diamantina, State of Minas Gerais, Brazil (Pinheiro et al., 2022PINHEIRO, R.A., ZANUNCIO, J.C., TOMA, R., ISAAC JUNIOR, J.B., SOARES, M.A., SANTOS, C.A., SERRÃO, J.E., CABRAL, M.J.S. and TAVARES, M.T., 2022. Brachymeria koehleri (Hymenoptera: Chalcididae): first record as hyperparasitoid in Dione juno juno (Lepidoptera: Nymphalidae) pupae. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 82, pp. e260645. https://doi.org/10.1590/1519-6984.260645.
https://doi.org/10.1590/1519-6984.260645... ). The lack of defensive movements (Lindstedt et al., 2010LINDSTEDT, C., TALSMA, J.H.R., IHALAINEN, E., LINDSTRÖM, L. and MAPPES, J., 2010. Diet quality affects warning coloration indirectly: excretion costs in a generalist herbivore. Evolution, vol. 64, no. 1, pp. 68-78. http://dx.doi.org/10.1111/j.1558-5646.2009.00796.x. PMid:19659593.
http://dx.doi.org/10.1111/j.1558-5646.20... ) may facilitate the predation of D. juno juno pupae by P. satan.

This is the first report of the predation and feeding process of P. satan on D. juno juno pupae. The record of P. satan feeding on D. juno juno pupae increases the number of natural enemies of this lepidopteran and the importance of Vespidae species in managing populations of this pest in the P. edulis crops.

Acknowledgements

We thank the “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq), the “Fundação de Amparo à Pesquisa do Estado de Minas Gerais” (FAPEMIG), Instituto Federal de Educação, Ciência e Tecnologia do Sul de Minas Gerais - Campus Inconfidentes” and “Programa de Proteção Florestal do Instituto de Pesquisas e Estudos Florestais (PROTEF- IPEF)” for financial support. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES - Finance Code 001). To Olaf Hermann Hendrik Mielke for the taxonomic identifications of the lepidopteran “D. juno juno”.

References

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