Eating with the enemy? Mimic complex between a stingless bee and assassin bugs


  • Leopoldo Jesús Alvarez Universidad Nacional de La Plata (UNLP), Facultad de Ciencias Naturales y Museo (FCNyM), División Entomología - La Plata, Argentina.
  • Fernando Zamudio Universidad Nacional de Córdoba (UNC), Facultad de Ciencias Exactas, Físicas y Naturales (FCEFYN), Instituto Multidisciplinario de Biología Vegetal (IMBIV), Interacciones Ecológicas y Conservación - Córdoba, Argentina.
  • Maria Cecilia Melo Universidad Nacional de La Plata (UNLP), Facultad de Ciencias Naturales y Museo (FCNyM), División Entomología - La Plata, Argentina.



Harpactorinae, Meliponini, Notocyrtus, Bauhinia, Extrafloral nectaries


In this study, we record for the first time the genus Notocyrtus (Heteroptera, Reduviidae) from Argentina based on three species: Notocyrtus dorsalis (Gray), Notocyrtus dispersus Carvalho & Costa, and Notocyrtus foveatus Stål. We also describe and illustrate a mimetic complex comprising the three Notocyrtus species and Tetragona clavipes (Fabricius) (Apidae, Meliponini), that were collected on Bahuinia forficata Link (Leguminosae: Caesalpinioideae). We include biological comments on the plant-reduvid-bee interaction and hypothesize about the functionality of the mimetic complex described.


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Author Biographies

Leopoldo Jesús Alvarez, Universidad Nacional de La Plata (UNLP), Facultad de Ciencias Naturales y Museo (FCNyM), División Entomología - La Plata, Argentina.

Paseo del Bosque, 1900, La Plata, Argentina.
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET).

Fernando Zamudio, Universidad Nacional de Córdoba (UNC), Facultad de Ciencias Exactas, Físicas y Naturales (FCEFYN), Instituto Multidisciplinario de Biología Vegetal (IMBIV), Interacciones Ecológicas y Conservación - Córdoba, Argentina.

Av. Vélez Sarsfield 1611, 5000 Córdoba, Argentina.
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET).

Maria Cecilia Melo, Universidad Nacional de La Plata (UNLP), Facultad de Ciencias Naturales y Museo (FCNyM), División Entomología - La Plata, Argentina.

Paseo del Bosque, 1900, La Plata, Argentina.
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET).


Afkhami, M.E.; Rudgers, J.A. & Stachowicz, J.J. 2014. Multiple mutualist effects: conflict and synergy in multispecies mutualisms. Ecology, 95(4): 833‑844.

Almeida-Neto, M.; Izzo, T.J.; Raimundo, R.L.G. & Rossa-Feres, D.C. 2003. Reciprocal interference between ants and stingless bees attending the honeydew-producing homopteran Aetalion reticulatum (Homoptera: Aetalionidae). Sociobiology, 42: 369‑380.

Alves, L.H.; Nogueira Pereira, S.; Prezoto, F. & Rodrigues Cassino, P.C. 2015. Ecological Interaction Among Stingless Bees, Ants, and the Whitefly Aleurothrixus aepim (Goeldi). EntomoBrasilis, 8(2): 159‑161.

Aranda-Rickert, A.; Fracchia, S.; Yela, N. & Marazzi, B. 2017. Insights into a novel three-partner interaction between ants, coreids (Hemiptera: Coreidae) and extrafloral nectaries: implications for the study of protective mutualisms. Arthropod-Plant Interactions, 11: 525‑536.

Barônio, G.J.; Vieira Pires, A.C. & 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(2): 407‑414.

Beattie, A.J. 1985. The Evolutionary Ecology of Ant-Plant Mutualisms. Cambridge University Press.

Bérenger, J.M. & Pluot-Sigwalt, D. 1997. Relations privilégiées de certains Heteroptera Reduviidae prédateurs avec les végétaux. Premier casconnu d’un Harpactorinae phytophage. Comptes rendus de l’Académie des Sciences, Sciences de la Vie, Life Sciences, 320: 1007‑1012.

Biesmeijer, J.C. & Slaa, E.J. 2004. Information flow and organization of stingless bee foraging. Apidologie, 35: 143‑157.

Biesmeijer, J.C.; Richter, J.A.P.; Smeets, M.A.J.P. & Sommeijer, M.J. 1999. Niche differentiation in nectar-collecting stingless bees: the influence of morphology, floral choice and interference competition. Ecological Entomology, 24: 380‑388.

Bronstein, J.L.; Alarcón, R. & Geber, M. 2006. The evolution of plant-insect mutualisms. The New Phytologist, 172: 412‑428.

Camargo, J.M.F. & Pedro, S.R.M. 2007. Meliponini Lepeletier, 1836. In: Moure, J.S.; Urban, D. & Melo, G.A.R. (Eds.). Catalogue of bees (Hymenoptera, Apoidea) in the Neotropical Region. Curitiba, Sociedade Brasileira de Entomologia. p. 272‑578.

Campos, L.A.O.; Silveira, F.A.; Oliveira, M.L.; Abrantes, C.V.M.; Morato, E.F. & Melo, G.A.R. 1989. Utilização de armadilhas para a captura de machos de Euglossini (Hymenoptera, Apoidea). Revista Brasileira de Zoologia, 6: 621‑626.

Carvalho, J.C.M. & Costa, L.A.A. 1992. Descriptions of new species of Notocyrtus Burmeister, 1835 (Hemiptera-Heteroptera, Reduviidae, Harpactorinae). Anais da Academia Brasileira de Ciências, 64(1): 71‑78.

Carvalho, J.C.M. & Costa, L.A.A. 1993. Revision of the known species of Notocyrtus Burmeister, 1835 (Hemiptera-Heteroptera, Reduviidae; Harpactorinae). Revista Brasileira de Biologia, 53(3): 365‑384.

Champion, G.C. 1898. Biologia Centrali-americana: Insecta. Rhynchota. Hemiptera-Heteroptera. London, Goodman & Salvin. v. 2.

Chebez, J.C. 2005. Guía de las reservas naturales de la Argentina. Nordeste. Buenos Aires, Editorial Albatros. v. 3.

Dressler, R.L. 1982. Biology of the orchid bees (Euglossini). Annual Review of Ecology and Systematics, 13: 373‑394.

Font Quer, P. 1970. Diccionario de Botánica. 3. reimpresión. Barcelona, Labor.

Forero, D. & Giraldo-Echeverry, N. 2015. First record of the assassin bug genus Coilopus Elkins, 1969 (Hemiptera: Heteroptera: Reduviidae) from Colombia. Check List, 11(3): 1634.

Fortunato, R.H. 1986. Revisión del género Bauhinia (Cercideae, Caesalpinioideae, Fabaceae) para la Argentina. Darwiniana, 27: 527‑557.

Fowler, H.G. 1992. Aethalionidae: functional equivalents of extrafloral nectaries in Bauhinia (Cesalpinionidea). Anales de Biología, Murcia, 18(7): 155‑159.

Gastauer, M.; Campos, L.A.O. & Wittmann, D. 2011. Handling sticky resin by stingless bees (Hymenoptera, Apidae). Revista Brasileira de Entomología, 55(2): 234‑240.

Gil-Santana, H.R. 2007. New records of Reduviidae (Hemiptera: Heteroptera) from Brazil. Zootaxa, 1390: 59‑68.

Gil-Santana, H.R. 2008. New records, and nomenclatural and biological notes on Reduviidae (Hemiptera: Heteroptera) from Bolivia and Brazil. Zootaxa, 1785: 43‑53.

Gil-Santana, H.R. & Alves, R.J.V. 2011. Association between Zelus versicolor (Herrich-Schäffer) (Hemiptera, Reduviidae, Harpactorinae) and Bidens rubifolia Kunth (Asterales, Asteraceae). EntomoBrasilis, 4(1): 30‑32.

Gil-Santana, H.R. & Forero, D. 2009. A new species of Notocyrtus, a new synonym of Coilopus, and new records and notes on other Harpactorini (Hemiptera: Heteroptera: Reduviidae: Harpactorinae) from South America. Zootaxa, 2148: 55‑67.

Gil-Santana, H.R.; Forero, D. & Weirauch, C. 2015. Assassin Bugs (Reduviidae Excluding Triatominae). In: Panizzi, A.R. & Grazia, J. (Eds.). True Bugs (Heteroptera) of the Neotropics. Dordrecht, Springer Science+Business Media. p. 307‑351 (Entomology in Focus 2)

Gonzalez, A.M. & Marazzi, B. 2018. Extrafloral nectaries in Fabaceae: filling gaps in structural and anatomical diversity in the family. Botanical Journal of the Linnean Society, 187: 26‑45.

Gray, G.R. 1832. [New genera and species] In: Griffith, E. The Animal Kingdom arranged in accordance to its organization by the Baron Cuvier. Paris. v. 15, part 2.

Guillermo-Ferreira, R.; Cardoso-Leite, R. & Gandolfo, R. 2012. First observation of alternative food usage (extrafloral nectar) by the assassin bug Atopozelus opsimus (Hemiptera, Reduviidae). Revista Brasileira de Entomologia, 56(4): 489‑491.

Haviland, M.D. 1931. The Reduviidae of Kartabo (Bartica District). Zoologica, New York, 7(1): 129‑154.

Howard, J.J. 1985. Observations on Resin Collecting by Six Interacting Species of Stingless Bees (Apidae: Meliponinae). Journal of the Kansas Entomological Society, 58(2): 337‑345.

Jackson, J.F. 1973. Mimicry of Trigona Bees by a Reduviid (Hemiptera) from British Honduras. Florida Entomologist, 56(3): 200‑202.

Janzen, D.H. 1966. Coevolution of mutualism between Ants and Acacias in Central America. Evolution, 20(3): 249‑265.

Koptur, S. 1992. Extrafloral nectary-mediated interactions between insects and plants. In: Bernays, E. (Ed.). Insect-plant interactions, Boca Raton, Boca Raton Press. v. 4, p. 81‑129.

Leonhardt, S.D. & Blüthgen, N. 2009. A Sticky Affair: Resin Collection by Bornean Stingless Bees. Biotropica, 41(6): 730‑736.

Lethierry, L.F. & Severin, G. 1896. Catalogue général des hémiptères. Hétéroptères. Bruxelles, F. Hayez. v. 2.

Maldonado Capriles, J. 1990. Systematic catalogue of the Reduviidae of the world (Insecta: Heteroptera). Mayaguez, University of Puerto Rico. 694p.

Maldonado Capriles, J. & Lozada Robles, PW. 1992. Key to the group of Neotropical wasp-mimetic harpactorine genera and the description of a new species (Hemiptera: Reduviidae). Proceedings of the Entomological Society of Washington, 94(1): 162‑165.

Melo, G.A.R. 1995. Fragrance gathering by Euglossa males in flowers of Ternstroemia dentate (Theaceae) (Hymenoptera: Apidae: Euglossinae). Entomologia Generalis, 19: 281‑283.

Melo, M.C.; Dellapé, G.; Olivera, L.; Varela, P.S.; Montemayor, S.I. & Dellapé, P.M. 2017. Biodiversity of true bugs from Iguazú National Park, Argentina. Check List, 13(5): 479‑511.

Michener, C.D. 2007.The Bees of the world. 2. ed. Baltimore, Johns Hopkins University Press.

Michener, C.D. 2013. The meliponini. In: Vit, P; Pedro, S.R.M. & Roubik, D.W. (Eds.). Pot-honey: a legacy of stingless bees. Berlin, Springe. p. 3‑17.

Miller, N.C.E. 1956. The Biology of the Heteroptera. London, Leonard Hill (Books) Limited. 162p.

Nagamitsu, T. & Inoue, T. 1997. Aggressive foraging of social bees as a mechanism of floral resource partitioning in an Asian tropical rainforest. Oecologia, 110: 432‑439.

Nelson, X.J. 2014. Evolutionary implications of deception in mimicry and masquerade. Current Zoology, 60(1): 6‑15.

Nemésio, A. & Siqueira, E.L. 2011. Acanthopus excellens Schrottky, 1902 (Hymenoptera: Apidae: Ericrocidini) attracted to eugenol in southeastern Brazil. North-Western Journal of Zoology, 7: 164‑166.

Nemésio, A.; Seixas, D.P. & Rasmussen, C. 2013. Trigona pallens (Fabricius, 1798) (Hymenoptera: Apidae) strongly attracted to vanillin in north-eastern Peru. Brazilian Journal of Biology, 73(3): 677‑678.

Oda, F.H.; Aoki, C.; Oda, T.M.; Da 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.

Oda, F.H.; Oliveira, A.F. & Aoki, C. 2014. Oxytrigona tataira (Smith) (Hymenoptera: Apidae: Meliponini) as a collector of honey dew from Erechtia carinata (Funkhouser) (Hemiptera: Membracidae) on Caryocar brasiliense Cambessédes (Malpighiales: Caryocaraceae) in the Brazilian Savanna. Sociobiology, 61(4): 566‑569.

Paine, R.T. 1980. Food Webs: Linkage, Interaction Strength and Community Infrastructure. Journal of Animal Ecology, 49(3): 666‑685.

Rainey, M.M. & Grether, G.F. 2007. Competitive mimicry: synthesis of a neglected class of mimetic relationships. Ecology, 88(10): 2440‑2448.

Roubik, D.W. 1989. Ecology and natural history of tropical bees. New York, Cambridge University Press.

Stål, C. 1872. Enumeratio Reduviidarum Americae. Konglinga Vetenskaps-Akedemiens Handlingar, 10(4): 66‑128.

Trager, M.D.; Bhotika, S.; Hostetler, J.A.; Andrade, G.V.; Rodriguez-Cabal, M.A.; McKeon, C.S.; Osenberg, C.W. & Bolker, B.M. 2010. Benefits for plants in ant-plant protective mutualisms: a meta-analysis. PLoS One, 5(12): e14308.

Walker, F. 1873. Catalogue of the specimens of Hemiptera Heteroptera in the collection of the British Museum. London, Trustees of the British Museum. v. 8.

Wattanachaiyingcharoen, W. & Jongjitvimol, T. 2007. First Record of the Predator, Pahabengkakia piliceps Miller, 1941 (Reduviidae, Harpactorinae) in the Stingless Bee, Trigona collina Smith, 1857 (Apidae, Meliponinae) in Thailand. The Natural History Journal of Chulalongkorn University, 7(1): 71‑74.

Weber, M.G. & Keeler, K.H. 2013. The phylogenetic distribution of extrafloral nectaries in plants. Annals of Botany, 111: 1251‑1261.

Wygodzinsky, P. 1949. Elenco sistemático de lo reduviformes americanos. Instituto Medicina Regional Tucumán. 102p.

Zamudio, F. & Alvarez, L.J. 2016. Abejas sin aguijón de Misiones: Guía etnotaxonómica. Córdoba, Ar. Editorial de la UNC.




How to Cite

Alvarez, L. J., Zamudio, F., & Melo, M. C. (2019). Eating with the enemy? Mimic complex between a stingless bee and assassin bugs. Papéis Avulsos De Zoologia, 59, e20195927.



Original Article

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