DOI: 10.13102/sociobiology.v61i4.566-569Sociobiology 61(4): 566-569 (December 2014) Open access journal: http://periodicos.uefs.br/ojs/index.php/sociobiology ISSN: 0361-6525 Oxytrigona tataira (Smith) (Hymenoptera: Apidae: Meliponini) as a collector of honeydew from Erechtia carinata (Funkhouser) (Hemiptera: Membracidae) on Caryocar brasiliense Cambessèdes (Malpighiales: Caryocaraceae) in the Brazilian Savanna FH Oda1, AF Oliveira2, C Aoki3 Mutualisms are interspecific interactions where individuals of two species experience higher fitness when they occur together than when they occur alone (Bronstein, 1998). This interaction is an important process for the structure and composition of communities (Bascompte & Jordano, 2007; Lange & Del-Claro, 2014). Many species of phytophagous hemipterans (e.g. aphids, coccids and treehoppers) are mutualistically associated with ants (Flatt & Weisser, 2000; Offenberg, 2001; Fagundes et al., 2013). In these relationships, ants protect their hemipteran partners against predators and parasites (Schultz & McGlynn, 2000; Fagundes et al., 2013) and often rely on honeydew as one of their most important food source (Davidson et al., 2003), besides extrafloral nectar (Del-Claro et al., 2013) and lepidopteran secretions (Alves-Silva et al., 2013). Abstract Trophobiont insects are of general interest to behavioral ecology due to the fact that the outcomes of their interactions with hymenopterans can result in strong facultative mutualisms. In this paper we present observations of Oxytrigona tataira (Smith) collecting honeydew from Erechtia carinata (Funkhouser) on Caryocar brasiliense Cambessèdes in a cerrado sensu stricto fragment from Brazilian Savanna. Our observations showed that these bees stimulate E. carinata individuals touching them with the antennas in the gaster to collect honeydew. O. tataira has not been previously recorded collecting honeydew on E. carinata. Thus, we present these observations as a novel bee-treehopper interaction. Sociobiology An international journal on social insects 1 Universidade Estadual de Maringá (UEM), Maringá, PR, Brazil 2 Universidade Federal de Mato Grosso do Sul (UFMS), Campo Grande, MS, Brazil 3 Universidade Federal de Mato Grosso do Sul (UFMS), Aquidauana, MS, Brazil Article History Edited by Cândida Maria L. Aguiar, UEFS – Brazil Received: 22 September 2014 Initial acceptance: 29 October 2014 Final acceptance: 18 November 2014 Keywords Hemipterans, Exudate, Feeding behavior, "Pequi", Stingless bee Corresponding author Fabrício Hiroiuki Oda Laboratório de Ictioparasitologia Núcleo de Pesquisas em Limnologia Ictiologia e Aqüicultura Universidade Estadual de Maringá Bloco G-90 Avenida Colombo, 5.790 87020-900, Maringá, PR, Brazil E-Mail: fabricio_oda@hotmail.com Although ants are the most common hymenopteran interacting with treehoppers, bees and wasps can also be associated with them (Lin, 2006). Mutualistic interactions have been reported involving the aetalionid treehopper Aetalion reticulatum (Linnaeus) with wasps or ants (Letourneau & Choe, 1987; Ramoni-Perazzi et al., 2006), and even Trigona Jurine, a stingless bee, which take advantage of treehoppers sugary excretions, the honeydew (Castro, 1975; Vieira et al., 2007; Oda et al., 2009; Barônio et al., 2012). Godoy et al. (2006) reported eight associations between membracids and bees, including the interaction between Potnia Stål and Oxytrigona tataira (Smith). Azevedo et al. (2007) reported the associations between Trigona spinipes (Fabricius) and five membracids species, and observed that the bees repelled some insects that approached the membracids, although with low aggressiveness. SHORT NOTE Sociobiology 61(4): 566-569 (December 2014) 567 This kind of interaction has not been reported between the stingless bee O. tataira (Apidae: Meliponini) and the treehopper Erechtia carinata (Funkhouser) (Auchenorrhyncha: Membracidae). This membracid belongs to the tribe Talipedini and it was recently reassessed, and Trinarea Goding is considered a junior synonym of Erechtia Walker (Sakakibara, 2012). Oxytrigona tataira has a wide distribution, occurring in eight Brazilian States (Silveira et al., 2002; Lima et al., 2013). Oxytrigona Cockerell is commonly known in Brazil as “tataíra” or “cospe-fogo” (fire spitting), due to caustic substance (formic acid) produced by worker bees for defense. These bees are highly aggressive, and also cleptobiotic, being colony’s robbers of other meliponine species (Roubik et al., 1987; Roubik, 1992). Caryocar brasiliense Cambessèdes has a wide distribution, occurring in 15 Brazilian States and Paraguay (Lopes et al., 2006). It is commonly known as "pequi", found from shrubs to trees of 1.5 to 11 meters high, with semi-deciduous behavior of foliar change (Lopes et al., 2006). Although the use of secretions from sucking insects (Hemiptera) by species of Trigona and Oxytrigona has been reported before (Cortopassi-Laurino, 1977; Letourneau & Choe, 1987), herein we present first observations of interaction between O. tataira and E. carinata on C. brasiliense in the Brazilian Savanna. During three non-consecutive days in January 2012, individuals of O. tataira were observed collecting honeydew from E. carinata in a cerrado sensu stricto fragment (17º 21’ S, 53º 18’ W) at Alto Araguaia municipality, State of Mato Grosso, mid-western Brazil. The observations were carried out once per day, between 7:00 and 10:00 h. Each observation lasted 15 to 20 minutes. Voucher specimens were collected, processed and given to specialists for identification and deposition in the Entomological Collection Padre Jesus S. Moure (DZUP) of the Department of Zoology at the Universidade Federal do Paraná (UFPR). We observed variable numbers of individuals of O. tataira (mean = 55 individuals ± 42.7 SD) collecting honeydew of approximately 130 nymphs and one adult of E. carinata. The number of O. tataira was lower during the second day of observations after heavy rain. The bees stimulated E. carinata individuals by primarily touching the treehoppers at the proximal upper abdomen with their front legs and antennas. The bees repeated the stimulus toward the distal part of the abdomen where the exudate droplet was collected with aid of the first pair of legs and quickly sucked. This behavior of the bees was recorded mainly in the treehoppers nymphs because only one adult was with the nymphs on the branch (Fig 1). As a result of our presence the bees defended the food source by beating their wings as a warning sign (Fig 2), and some individuals started a short flight over the E. carinata colony. In the first day of observations, inattentive researchers were attacked by the bees. We did not record the presence of ants patrolling the treehoppers. The behavior of E. carinata stimulation by O. tataira resembles that observed in species of Trigona in association with A. reticulatum: the bees touch their antennas to the head of the treehoppers, and then the first two pairs of legs on the back of the abdomen, after that touching the antennas on the distal part of the abdomen and quickly sucking the honeydew droplet released after stimulation (Vieira et al., 2007; Oda et al., 2009; Barônio et al., 2012). This behavior is also similar to that reported between ants and honeydew-producing hemipterans, including membracids, in which the ants actively touch the body of the insects with their antennae to stimulate the releasing of honeydew droplets (Stefani et al., 2000; Pfeiffer & Linsenmair, 2007; Guerra et al., 2011; Gjonov & Gjonova-Lapeva, 2013). Previous studies suggest that this possibly facultative mutualistic association is beneficial for both species (Vieira et al., 2007; Oda et al., 2009; Barônio et al., 2012), promoting a protection against natural enemies of the treehoppers, and supplying part of the bees diet with the honeydew rich in carbohydrates (Way, 1963; Fagundes et al., 2013). Additionally, the association with the bees can reduce fungus attack because of the removal of the contaminant honeydew (Way, 1963; Buckley, 1987), decreasing the chances of local extinction of these hemipterans (Buckley, 1987). On ant-tending, the mortality risks of the tended insects can be considerably reduced due to protection against predators and parasitoids (Flatt & Weisser, 2000; Fagundes et al., 2013). However, we did not test it. Thus, it is important to emphasize the necessity of future studies, which are essential to know the true nature of this interaction. Fig 1. Oxytrigona tataira (Smith) (Hymenoptera: Apidae: Meliponini) collecting honeydew from Erechtia carinata (Funkhouser) (Hemiptera: Membracidae) on branch of Caryocar brasiliense Cambessèdes (Malpighiales: Caryocaraceae). FH Oda, AF Oliveira, C Aoki - A bee-treehopper interaction 568 Acknowledgements We are grateful to Albino M. Sakakibara and Sebastião Laroca for the identification of treehopper and bee species, respectively. To editor and two anonymous reviewers for their constructive comments, that helped us to improve the manuscript. Guilherme H. Barbosa, Frederico Pereira, Vinícius Cerqueira and Patrícia G. Ferreira for field assistance. Mariana F. Felismino reviewed the English language. The Biocev provided logistical support during fieldwork. References Alves-Silva, E., Bächtold, A., Barônio, G. J. & Del-Claro, K. (2013). Influence of Camponotus blandus (Formicinae) and flower buds on the occurrence of Parrhasius polibetes (Lepidoptera: Lycaenidae) in Banisteriopsis malifolia (Malpighiaceae). Sociobiology, 60: 30-34. Azevedo, R. L., Carvalho, C. A. L., Bomfim, Z. V. & Vicente, M. A. A. (2007). Interações entre auquenorrincos (Aethalionidae e Membracidae), abelhas (Apidae) e formigas (Formicidae) em plantas de feijão guandu. Rev. Ecossistema, 32: 81-86. Barônio, G. J., Pires, A. C. V. & Aoki, C. (2012). Trigona branneri (Hymenoptera: Apidae) as a collector of honeydew from Aethalion reticulatum (Hemiptera: Aethalionidae) on Bauhinia forficata (Fabaceae: Caesalpinoideae) in a Brazilian Savanna. Sociobiology, 59: 1-8. Bascompte, J. & Jordano, P. (2007). Plant-animal mutualistic networks: The architecture of biodiversity. Annu. Rev. Ecol. Evol. Syst., 38: 567-593. doi: 10.1146/annurev. ecolsys.38.091206.095818 Bronstein, J. L. (1998). The contribution of ant-plant protection studies to our understanding of mutualism. Biotropica, 30: 150-161. Buckley, R. C. (1987). Interactions involving plants, Homoptera and ants. Ann. Rev. Ecol. Syst., 18: 111-135. Castro, P. R. C. (1975). Mutualismo entre Trigona spinipes (Fabricius 1793) e Aethalion reticulatum (L. 1767) em Cajanus indicus Spreng. na presença de Camponotus spp. Cienc. Cult., 27: 537-539. Cortopassi-Laurino, M. (1977). Notas sobre associações de Trigona (Oxytrigona) tataira (Apidae, Meliponinae). Bol. Zool., 2: 183-187. Davidson, D. W., Cook, S. C., Snelling, R. R. & Chua, T. C. (2003). Explaining the abundance of ants in lowland tropical rainforest canopies. Science, 300: 969-972. doi:10.1126/science.1082074 Del-Claro, K., Guillermo-Ferreira, R., Almeida, E. M., Zardini, H. & Torezan-Silingardi, H. M. (2013). Ants visiting the post-floral secretions of pericarpial nectaries in Palicourea rigida (Rubiaceae) provide protection against leaf herbivores but not against seed parasites. Sociobiology, 60: 217-221. doi:10.13102/sociobiology.v60i3.217-221. Fagundes, R., Ribeiro, S. P. & Del-Claro, K. (2013). Tending- ants increase survivorship and reproductive success of Calloconophora pugionata Drietch (Hemiptera, Membracidae), a trophobiont herbivore of Myrcia obovata O.Berg (Myrtales, Myrtaceae). Sociobiology, 60: 11-19. Flatt, T. & Weisser, W. W. (2000). The effects of mutualistic ants on aphid life history traits. Ecology, 81: 3522-3529. doi: 10.1890/0012-9658(2000)081[3522:TEOMAO]2.0.CO;2 Godoy, C., Miranda, X. & Nishida, K. (2006). Treehoppers of America Tropical. Costa Rica: INBio, 352 p. Gjonov, I. & Gjonova-Lapeva, A. (2013). New data on ant- attendance in leafhoppers (Hemiptera: Cicadellidae). North- West J. Zool., 9: 433-437. Guerra, T. J., Camarota, F., Castro, F. S., Schwertner, C. F. & Grazia, J. (2011). Trophobiosis between ants and Eurystethus microlobatus Ruckes (Hemiptera: Heteroptera: Pentatomidae) a cryptic, gregarious and subsocial stinkbug. J. Nat. Hist., 45: 1101-1117. doi: 10.1080/00222933.2011.552800 Lange, D. & Del-Claro, K. (2014). Ant-plant interaction in a Tropical Savanna: May the network structure vary over time and influence on the outcomes of associations? PLoS ONE, 9(8): 1-10. doi:10.1371/journal.pone.0105574 Letourneau, D. K. & Choe, J. C. (1987). Homopteran attendance by wasps and ants: the stochastic nature of interactions. Psyche, 94: 81-91. doi: 10.1155/1987/12726 Lima, F. V. O., Silvestre, R. & Balestieri, J. B. P. (2013). Nest entrance types of stingless bees (Hymenoptera: Apidae sensu lato) in a Tropical Dry Forest of mid-Western Brazil. Sociobiology, 60: 421-428. doi: 10.13102/sociobiology.v60i4.421-428 Lin, C-P. (2006). Social behaviour and life history of membracine treehoppers. J. Nat. Hist., 40: 1887-1907. doi: 10.1080/00222930601046618 Fig 2. Agonistic behavior displayed by Oxytrigona tataira (Smith) (Hymenoptera: Apidae: Meliponini) as a result of feeling threatened by the presence of the researchers. Sociobiology 61(4): 566-569 (December 2014) 569 Lopes, P. S. N., Pereira, A. V., Pereira, E. B. C., Martins, E. R. & Fernandes, R. C. (2006). Pequi. In R. F. Vieira, T. S. A. Costa, D. B. Silva, F. R. Ferreira & S. M.Sano (Eds.), Frutas nativas da região Centro-Oeste do Brasil (pp. 248- 287). Brasília: Embrapa Recursos Genéticos e Biotecnologia. Oda, F. H., Aoki, C., Oda, T. M., Silva, R. A. & Felismino, M. F. (2009). Interação entre abelha Trigona hyalinata (Lepeletier, 1836) (Hymenoptera: Apidae) e Aethalion reticulatum Linnaeus 1767 (Hemiptera: Aethalionidae) em Clitoria fairchildiana Howard (Papilionoideae). Entomobrasilis, 2: 58-60. Offenberg, J. (2001). Balancing between mutualism and exploitation: the symbiotic interaction between Lasius ants and aphids. Behav. Ecol. Sociobiol., 49: 304-310. doi: 10.1007/s002650000303 Pfeiffer, M. & Linsenmair, K. E. (2007). Trophobiosis in a tropical rainforest on Borneo: giant ants Camponotus gigas (Hymenoptera: Formicidae) herd wax cicadas Bythopsyrna circulata (Auchenorrhyncha: Flatidae). Asian Myrmecol., 1: 105-119. Ramoni-Perazzi, P., Bianchi-Pérez, G. & Bianchi- Ballestereos, G. (2006). Primer registro de asociación entre Aetalion reticulatum (Linné) (Hemiptera: Aetalionidae) y Synoeca septentrionalis Richards (Hymenoptera: Vespidae). Entomotropica, 21: 129-132. Roubik, D. W., Smith, B. H. & Carlson, R. L. (1987). Formic acid in caustic cephalic secretions of stingless bee Oxytrigona (Hymenoptera, Apidae). J. Chem. Ecol., 13: 1079-1086. doi: 10.1007/BF01020539 Roubik, D. W. (1992). Stingless bees: A guide to Panamanian and Mesoamerican species and their nests (Hymenoptera, Apidae, Meliponinae). In D. Quintero & A. Aiello (Eds.), Insects of Panamá and Mesoamerica (pp. 495-524). Oxford: Oxford University Press. Sakakibara, A. M. (2012). Taxonomic reassessment of the treehopper tribe Talipedini with nomenclatural changes and descriptions of new taxa (Hemiptera: Membracidae: Membracinae). Zoologia, 29: 563- 576. doi: 10.1590/S1984-46702012000600008 Schultz, T. R. & McGlynn, T. P. (2000). The interactions of ants with other organisms. In D. Agosti, J. D. Majer, L. E. Alonso & T. R. Schultz, (Eds) Ants. Standard methods for measuring and monitoring biodiversity (pp. 35-44). Washington and London: Smithsonian Institution Press. Silveira, F. A., Melo, G. A. R. & Almeida E. A. B. (2002). Abelhas Brasileiras, Sistemática e Identificação. Belo Horizonte: Fundação Araucária, 253 p. Stefani, V., Sebaio, F. & Del-Claro, K. (2000). Desenvolvimento de Enchenopa brasiliensis Strumpel (Homoptera, Membracidae) em plantas de Solanum lycocarpum St.Hill. (Solanaceae) no cerrado e as formigas associadas. Rev. Bras.. Zoociênc., 2(1): 21-30. Vieira, C. U., Rodovalho, C. M., Almeida, L. O., Siqueroli, A. C. S. & Bonetti, A. M. (2007). Interação entre Trigona spinipes Fabricius 1793 (Hymenoptera: Apidae) e Aethalion reticulatum Linnaeus 1767 (Hemiptera: Aethalionidae) em Mangifera indica (Anacardiaceae). Biosci. J., 23: 10-13. Way, M. J. (1963). Mutualism between ants and honeydew- producing Homoptera. Annu. Rev. Entomot., 8: 307-344. doi: 10.1146/annurev.en.08.010163.001515