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Issue: Vol. 4299 No. 2: 27 Jul. 2017
Type: Article
Published: 2017-07-27
DOI: 10.11646/zootaxa.4299.2.2
Page range: 191–220
Abstract views: 226
PDF downloaded: 2

The neotropical stingless bee genus Nannotrigona Cockerell (Hymenoptera: Apidae: Meliponini): An illustrated key, notes on the types, and designation of lectotypes

Aquatic Biology, Department of Bioscience, Aarhus University, Ole Worms Allé 1, DK-8000 Aarhus C, Denmark.
Undergraduate Biology Program and Department of Ecology and Evolutionary Biology, Haworth Hall, 1200 Sunnyside Avenue, University of Kansas, Lawrence, Kansas 66045, USA.
Hymenoptera Anthophila Meliponiculture Taxonomy

Abstract

We provide comparative comments on the morphology and provenance of the primary types of the species in the stingless bee genus Nannotrigona Cockerell. We offer an illustrated key to workers of all presently known species and designate lectotypes for the following species to stabilize their names: N. dutrae (Friese), N. mellaria (Smith), N. punctata (Smith), and N. schultezi (Friese). The type of Melipona minuta Lepeletier de Saint Fargeau could not be located and it remains an incertae sedis, but a possible member of Nannotrigona. A distinctive new species from western Ecuador, Nannotrigona camargoi n. sp. (type locality Ecuador, Pichincha) is also described and figured.

 

References

  1. Ayala, R., Gonzalez, V.H. & Engel, M.S. (2013) Mexican stingless bees (Hymenoptera: Apidae): diversity, distribution and indigenous knowledge. In: Vit, P., Pedro, S.R.M. & Roubik, D.W. (Eds.), Pot-Honey: a Legacy of Stingless Bees. Springer, New York, pp. 135–152.
    https://doi.org/10.1007/978-1-4614-4960-7_9

    Baker, D.B. (1994) Type material in the University Museum, Oxford, of bees described by Comte Amédée Lepeletier de Saint-Fargeau and Pierre André Latreille (Hymenoptera: Apoidea). Journal of Natural History, 28, 1189–1204.
    https://doi.org/10.1080/00222939400770591

    Bates, H.W. (1863) The naturalist on the River Amazons, a record of adventures, habits of animals, sketches of Brazilian and Indian life and aspects of nature under the Equator during eleven years of travel. John Murray, London, 351 + 423 pp. https://doi.org/10.5962/bhl.title.103298

    Batista, M.A., Ramalho, M. & Soares, A.E.E. (2003) Nesting sites and abundance of Meliponini (Hymenoptera: Apidae) in heterogeneous habitats of the Atlantic Rain Forest, Bahia, Brazil. Lundiana, 4, 19–23.

    Bego, L.R., Maeta, Y., Tezuka, T. & Ishida, K. (1989) Floral preference and flower constancy of a Brazilian stingless bee Nannotrigona testaceicornis kept in a greenhouse (Hymenoptera Apidae). Bulletin of the Faculty of Agriculture Shimane University, 23, 46–54.

    Bradley, J.C. (1957) The types of Hymenoptera described by Amedée Lepeletier, comte de Saint-Fargeau. Annali del Museo Civico di Storia Naturale di Genova, 69, 36–50.

    Cabral de Castro, L., Netto Silva, P. & Prezoto, F. (2009) Unusual nesting behavior in a Neotropical stingless bee, Nannotrigona testaceicornis (Hymenoptera: Apidae). Sociobiology, 53, 569–572.

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

    Camargo, J.M.F. & Pedro, S.R.M. (2009) Neotropical Meliponini: the genus Celetrigona Moure (Hymenoptera: Apidae, Apinae). Zootaxa, 2155, 37–54.

    Carpenter, J.M. (2011) Notes on types of some American wasps in the Spinola collection. Entomologica Americana, 117, 121–126.
    https://doi.org/10.1664/11-RA-002.1

    Casolari, C. & Moreno, R.C. (1979) Catalogo della collezione imenotterologica di Massimiliano Spinola 3a parte. Bollettino del Museo di Zoologia dell'Università di Torino, 4, 91–129.

    Cauich, O., Quezada-Euan, J.J.G., Macias-Macias, J.O., Reyes-Oregel, V., Medina-Peralta, S. & Parra-Tabla, V. (2004) Behavior and pollination efficiency of Nannotrigona perilampoides (Hymenoptera: meliponini) on greenhouse tomatoes (Lycopersicon esculentum) in subtropical Mexico. Journal of Economic Entomology, 97, 475–481.

    Cauich, O., Quezada Euan, J.J.G., Melendez Ramírez, V., Valdovinos-Nuñez, G.R. & Moo-Valle, H. (2006) Pollination of habanero pepper (Capsicum chinense) and production in enclosures using the stingless bee Nannotrigona perilampoides. Journal of Apicultural Research, 45, 125–130.
    https://doi.org/10.1080/00218839.2006.11101330

    Cockerell, T.D.A. (1922) Bees in the collection of the United States National Museum, 4. Proceedings of the United States National Museum, 60, 1–20.
    https://doi.org/10.5479/si.00963801.60-2413.1

    Couvillon, M.J., Wenseleers, T., Imperatriz-Fonseca, V.L., Nogueira-Neto, P. & Ratnieks, F.L.W. (2008) Comparative study in stingless bees (Meliponini) demonstrates that nest entrance size predicts traffic and defensivity. Journal of Evolutionary Biology, 21, 194–201.

    Craigan, I. (2008) America 1860: a young Englishman's diary: Ian Craigan & David Owen, Unknown City, 98 pp.

    Cresson, E.T. (1878) Descriptions of new species of North American bees. Proceedings of the Academy of Natural Sciences of Philadelphia, 30, 181–221.

    Cresson, E.T. (1916) The Cresson types of Hymenoptera. Memoirs of the American Entomological Society, 1, 1–141.

    Dardon, M.J. & Enriquez, E. (2008) Caracterización fisicoquímica y antimicrobiana de la miel de nueve especies de abejas sin aguijón (Meliponini) de Guatemala. Interciencia, 33, 916–922.

    de Almeida-Anacleto, D., Marchini, L.C., Souza, B.d.A. & de Camargo Carmello Moreti, A.C. (2011) Microbiological content and water activity of meliponine (Hymenoptera: Apidae) honey samples from Piracicaba, SP, Brazil. Sociobiology, 58, 489–497.

    Ducke, A. (1901a) Beiträge zur Kenntnis der geographischen Verbreitung der Chrysididen und Beschreibung von drei neuer Arten. Zeitschrift für systematische Hymenopterologie und Dipterologie, 1, 353–361.

    Ducke, A. (1901b) Zur Kenntnis einiger Sphegiden von Pará (Hym.). Zeitschrift für systematische Hymenopterologie und Dipterologie, 1, 241–242.

    Ducke, A. (1902a) As espécies Paraenses do gênero Euglossa Latr. Boletim do Museu Paraense de Historia Natural e Ethnographia, 3, 561–579.

    Ducke, A. (1902b) Beobachtungen über Blütenbesuch, Erscheinungszeit etc. der bei Pará vorkommenden Bienen. Allgemeine Zeitschrift für Entomologie, 7, 321–326, 360–368, 400–405, 417–422.

    Ducke, A. (1903) Die stachellosen Bienen (Melipona Ill.) von Pará. Zoologische Jahrbücher, Abteilung für Systematik, Geographie und Biologie der Tiere, 17, 285–328, pl. 211.

    Egler, W. (1963) Adolpho Ducke [27.x.1876-5.i.1959] - traços biográficos, viagens e trabalhos. Boletim do Museu Paraense Emílio Goeldi, Botânica, 18, 1–129.

    Friese, H. (1901) Neue Arten der Bienengattung Trigona Jur. (Hym.). Zeitschrift für systematische Hymenopterologie und Dipterologie, 1, 265–271.

    Gonçalves, A.L., Alves Filho, A. & Menezes, H. (2005) Atividade antimicrobiana do mel da abelha nativa sem ferrão Nannotrigona testaceicornis (Hymenoptera: Apidae, Meliponini). Arquivos do Instituto Biológico, 72, 455–459.

    Gonzalez, V.H. & Roubik, D.W. (2008) Especies nuevas y filogenia de las abejas del fuego, Oxytrigona (Hymenoptera: Apidae, Meliponini). Acta Zoológica Mexicana, 24, 43–71.

    Gonzalez, V.H., Griswold, T. & Engel, M.S. (2013) Obtaining a better taxonomic understanding of native bees: where do we start? Systematic Entomology, 38, 645–653.
    https://doi.org/10.1111/syen.12029

    Harris, R. A. (1979) A glossary of surface sculpturing. Occasional Papers in Entomology (State of California), 28, 1–31.

    Jarau, S., Hrncir, M., Schmidt, V.M., Zucchi, R. & Barth, F.G. (2003) Effectiveness of recruitment behavior in stingless bees (Apidae, Meliponini). Insectes Sociaux, 50, 365–374.
    https://doi.org/10.1007/s00040-003-0684-2

    Lepeletier de Saint Fargeau, A.L.M. (1836) Histoire naturelle des insectes. Hyménoptères. Vol. 1. Librairie encyclopédique de Roret, Paris, pp. 547.

    Lichtenberg, E.M., Imperatriz-Fonseca, V.L. & Nieh, J.C. (2010) Behavioral suites mediate group-level foraging dynamics in communities of tropical stingless bees. Insectes Sociaux, 57, 105–113.
    https://doi.org/10.1007/s00040-009-0055-8

    Mann, W.M. (1925) [Explorations and field-work of the Smithsonian Institution in 1922] The Mulford Biological Exploration. Smithsonian Miscellaneous Collections, 74, 54–62.

    Michener, C.D. (1990) Classification of the Apidae (Hymenoptera). Appendix: Trigona genalis Friese, a hitherto unplaced New Guinea species. University of Kansas Science Bulletin, 54, 75–163.

    Michener, C.D. (2007) The bees of the world. Second Edition. Johns Hopkins University Press, Baltimore, xviii + 953 pp.,

    Nascimento, W.M., Gomes, E.M.L., Batista, E.A. & Freitas, R.A. (2012) Utilização de agentes polinizadores na produção de sementes de cenoura e pimenta doce em cultivo protegido. Horticultura Brasileira, 30, 494–498.
    https://doi.org/10.1590/S0102-05362012000300023

    Nates-Parra, G., Rodriguez-C, A. & Velez, E.D. (2007) Abejas sin aguijón (Hymenoptera: Apidae: Meliponini) en cementerios de la cordillera oriental de Colombia. Acta Biologica Colombiana, 11, 25–35.

    Nogueira Neto, P. (1948) Bionomic notes on Meliponinae. I. On the ventilation of the nests and the structures related to them. Revista Brasileira de Biologia, 8, 465–488.

    O'Hare, J.E. (1995) Henry Walter Bates—his life and contributions to biology. Archives of Natural History, 22, 195–219.
    https://doi.org/10.3366/anh.1995.22.2.195

    Palma, G., Quezada-Euan, J.J.G., Reyes-Oregel, V., Melendez, V. & Moo-Valle, H. (2008a) Production of greenhouse tomatoes (Lycopersicon esculentum) using Nannotrigona perilampoides, Bombus impatiens and mechanical vibration (Hym.: Apoidea). Journal of Applied Entomology, 132, 79–85.
    https://doi.org/10.1111/j.1439-0418.2007.01246.x

    Palma, G., Quezada-Euán, J.J.G., Meléndez-Ramirez, V., Irigoyen, J., Valdovinos-Nuñez, G.R. & Rejón, M. (2008b) Comparative efficiency of Nannotrigona perilampoides, Bombus impatiens (Hymenoptera: Apoidea), and mechanical vibration on fruit production of enclosed habanero pepper. Journal of Economic Entomology, 101, 132–138.
    https://doi.org/10.1093/jee/101.1.132

    Papavero, N. (1971) Essays on the history of neotropical dipterology, with special reference to the collectors (1750–1905). Vol. 1. Museo de Zoologia, São Paulo, 216 pp.
    https://doi.org/10.5962/bhl.title.101715

    Papavero, N. & Ibáñez-Bernal, S. (2001) Contributions to a history of Mexican dipterology.-Part I. Entomologists and their works before the Biologia Centrali-Americana. Acta Zoológica Mexicana, New Series, 84, 65–173.

    Paynter, R.A. & Traylor, M.A. (1991) Ornithological Gazetteer of Brazil. Harvard University, Cambridge, 789 pp.

    Ramos-Elorduy, J. & Pino, J.M. (2002) Edible insects of Chiapas, Mexico. Ecology and Food Nutrition, 41, 271–299.
    https://doi.org/10.1080/03670240214081

    Rasmussen, C. & Ascher, J.S. (2008) Heinrich Friese (1860-1948): Names proposed and notes on a pioneer melittologist (Hymenoptera, Anthophila). Zootaxa, 1833, 1–118.

    Rasmussen, C. & Cameron, S.A. (2010) Global stingless bee phylogeny supports ancient divergence, vicariance, and long distance dispersal. Biological Journal of the Linnean Society, 99, 206–232.
    https://doi.org/10.1111/j.1095-8312.2009.01341.x

    Rasmussen, C., Garcete-Barrett, B.R. & Gonçalves, R.B. (2009) Curt Schrottky (1874–1937): South American entomology at the beginning of the 20th century (Hymenoptera, Lepidoptera, Diptera). Zootaxa, 2282, 1–50.

    Reyes-González, A., Camou-Guerrero, A., Reyes-Salas, O., Argueta, A. & Casas, A. (2014) Diversity, local knowledge and use of stingless bees (Apidae: Meliponini) in the municipality of Nocupétaro, Michoacan, Mexico. Journal of Ethnobiology and Ethnomedicine, 10, 47.
    https://doi.org/10.1186/1746-4269-10-47

    Rodriguez-Malaver, A.J., Rasmussen, C., Gutierrez, M.G., Gil, F., Nieves, B. & Vit, P. (2009) Properties of honey from ten species of Peruvian stingless bees. Natural Product Communications, 4, 1221–1226.

    Roselino, A.C., Santos, S.B., Hrncir, M. & Bego, L.R. (2009) Differences between the quality of strawberries (Fragaria x ananassa) pollinated by the stingless bees Scaptotrigona aff. depilis and Nannotrigona testaceicornis. Genetics and Molecular Research, 8, 539–545.
    https://doi.org/10.4238/vol8-2kerr005

    Roubik, D.W. (1983) Nest and colony characteristics of stingless bees from Panamá (Hymenoptera: Apidae). Journal of the Kansas Entomological Society, 56, 327–355.

    Roubik, D.W. (1992) Stingless bees: a guide to Panamanian and Mesoamerican species and their nests (Hymenoptera: Apidae: Meliponinae). In: Quintero, D. & Aiello, A. (Eds.), Insects of Panama and Mesoamerica. Oxford University Press, Oxford, pp. 495–524,

    Saint-Hilaire, A.F.C.P. (1823) Rapport fait à l'Académie royale des Sciences, sur le voyage au Brésil et dans les Missions du Paraguay. Annales de la Société Royale des Sciences, Belles-Lettres et Arts d'Orléans, 5, 151–162.

    Saint-Hilaire, A.F.C.P. (1847-1848) [Voyages dans l'interieur du Brésil. Troisième Partie] Voyage aux sources du Rio de S. Francisco et dans la province de Goyaz. Arthus Bertrand, Paris, 380 + 349 pp.

    Santos, S.A.B. dos, Roselino, A.C. & Bego, L.R. (2008) Pollination of cucumber, Cucumis sativus L. (Cucurbitales: Cucurbitaceae), by the stingless bees Scaptotrigona aff. depilis Moure and Nannotrigona testaceicornis Lepeletier (Hymenoptera: Meliponini) in greenhouses. Neotropical Entomology, 37, 506–512.
    https://doi.org/10.1590/S1519-566X2008000500002

    Schmidt, V.M., Hrncir, M., Schorkopf, D.L.P., Mateus, S., Zucchi, R. & Barth, F.G. (2008) Food profitability affects intranidal recruitment behaviour in the stingless bee Nannotrigona testaceicornis. Apidologie, 39, 260–272.
    https://doi.org/10.1051/apido:2008004

    Schmidt, V.M., Zucchi, R. & Barth, F.G. (2005) Scent marks left by Nannotrigona testaceicornis at the feeding site: cues rather than signals. Apidologie, 36, 285–291.
    https://doi.org/10.1051/apido:2005002

    Schwarz, H.F. (1938) The stingless bees (Meliponidae) of British Guiana and some related forms. Bulletin of the American Museum of Natural History, 74, 437–508.

    Silva, M.D., Monteiro, D., Silva, M., Oliveira, R.B., Queiroz, M.V.M. & Santos, J.F. (2012) Padrão de distribuição espacial de ninhos de Meliponini (Hymenoptera: Apidae) em função da disponibilidade de recursos para nidificação em um fragmento de Mata Atlântica em Salvador, Bahia, Brasil. Magistra, 24, 91–98.

    Slaa, E.J., van Nieuwstadt, M.G.L., Pisa, L.W. & Sommeijer, M.J. (1997) Foraging strategies of stingless bees (Apidae, Meliponinae): the relation between precision of recruitment, competition and communication. Acta Horticulturae (Wageningen), 437, 193–197.
    https://doi.org/10.17660/ActaHortic.1997.437.19

    Smith, F. (1854) Catalogue of the Hymenopterous insects in the collection of the British Museum. Part II, Apidæ. British Museum (Natural History), London, 465 pp.

    Smith, F. (1862) Descriptions of new species of aculeate Hymenoptera, collected at Panama by R. W. Stretch, Esq., with a list of described species, and the various localities where they have previously occured. Transactions of the Entomological Society of London, 11, 29–44.

    Snyder, T.E. (1926) Termites collected on the Mulford Biological Exploration to the Amazon Basin, 1921–1922. Proceedings of the United States National Museum, 68, 1–76.
    https://doi.org/10.5479/si.00963801.68-2615.1

    Stort, A.C. & Moraes-Alves, M.M.B. (1998) Sensory structures of the antennae of Nannotrigona testaceicornis (Apidae: Meliponinae). Journal of the New York Entomological Society, 105, 230–235.

    Valente, D., Marques, L.A.C. & Mendes, E.G. (1981) The acetylcholine contents of honeys from different bees as determined in 4-point-assays. Comparative Biochemistry and Physiology C-Pharmacology Toxicology & Endocrinology, 69, 161–164. https://doi.org/10.1016/0306-4492(81)90121-0

    van Nieuwstadt, M.G.L. & Iraheta, C.E.R. (1996) Relation between size and foraging range in stingless bees (Apidae, Meliponinae). Apidologie, 27, 219–228.
    https://doi.org/10.1051/apido:19960404

    Vit, P., Pedro, S.R.M. & Roubik, D.W. (2013) Pot-Honey: a legacy of stingless bees. Springer, New York, 654 pp.
    https://doi.org/10.1007/978-1-4614-4960-7

    Vit, P., Vargas, O., López, T. & Maza, F. (2015) Meliponini biodiversity and medicinal uses of pot-honey from El Oro province in Ecuador. Emirates Journal of Food and Agriculture 27, 502–506.
    https://doi.org/10.9755/ejfa.2015.04.079

    Vollet-Neto, A., Menezes, C. & Imperatriz-Fonseca, V.L. (2011) Brood production increases when artificial heating is provided to colonies of stingless bees. Journal of Apicultural Research, 50, 242–247.
    https://doi.org/10.3896/IBRA.1.50.3.09

    Wille, A. & Michener, C.D. (1973) The nest architecture of stingless bees with special reference to those of Costa Rica. Revista de Biología Tropical, 21 (Supplement), 9–278.

    Zamudio, F. & Alvarez, L.J. (2016) Abejas sin Aguijón de Misiones. Una guía etnotaxonómica para su identificación en el campo. Editorial de la Universidad Nacional de Córdoba, Córdoba, 218 pp.