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Perfume production in flowers of Angelonia salicariifolia attracts males of Euglossa annectans which do not promote pollination

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Abstract

Male Euglossini bees (Apidae) forage for floral and non-floral perfumes. Although the use of these perfumes has not yet been clearly reported, there are indications of using perfume from varied exogenous sources as a pheromone analogue since male orchid bees do not produce it. Here, we report an interaction between male Euglossa annectans and flowers of Angelonia salicariifolia (Plantaginaceae). Floral anatomy analysis and a histological study of two different sets of trichomes indicate the presence of aromatic oils (perfume) in one set of these trichomes. The other set of trichomes produce resins. Both sets of trichomes are found in the same floral area of the flower where the male orchid bees were seen. The male orchid bees studied forage for perfumes but do not promote pollination since they do not reach the reproductive structures during their visit. Our records show that only male E. annectans were attracted to the volatile fragrance although we know that other orchid bee species also occur in the area.

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References

  • Armbuster, W.S., Webster, G.L. (1979) Pollination of two species of Dalechampia (Euphorbiaceae) in Mexico by euglossine bees. Biotropica 11, 278–283

    Article  Google Scholar 

  • Buchanan, B.B., Gruissem, W., Jones, R.L. (2000) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville

    Google Scholar 

  • Buchmann, S. (1987) The ecology of oil flowers and their bees. Annu Rev Ecol Syst 18, 343–369

    Article  Google Scholar 

  • Cain, A.J. (1947) The use of Nile blue in the examination of lipoids. Q J Microsc Sci 88, 383–392

    Google Scholar 

  • Cappellari, S.C., Harter-Marques, B. (2010) First report of scent collection by male orchid bees (Hymenoptera: Apidae: Euglossini) from terrestrial mushrooms. J Kansas Entomol Soc 83, 264–266

  • Cappellari, S.C., Harter-Marques, B., Aumeier, P., Engels, W. (2009) Mercadomia tenella (Plantaginaceae) attracts oil-, perfume-, and pollen-gathering bees in Southern Brazil. Biotropica 41, 721–729

    Article  Google Scholar 

  • Cappellari, S.C., Haleem, M.A., Marsaioli, A.J., Tidon, R., Simpson, B.B. (2011) Pterandra pyroidea: a case of pollination shift within Neotropical Malighiaceae. Ann Bot-London 107, 1323–1334

  • Carvalho Filho, F.S. (2010) Scent-robbing and fighting among male orchid bees, Eulaema (Apeulaema) nigrita Lepeletier, 1841 (Hymenoptera: Apidae: Euglossini). Biota Neotrop 10, 405–408

  • Carvalho, R., Webber, A.C. (2000) Biologia floral de Unonopsis guatterioides (A.D.C.) R.E. Fr., uma Annonaceae polinizada por Euglossini. Revta bras Bot 23, 421–425

    Google Scholar 

  • Cordeiro, G.D., Boff, S., Caetano, T.A., Fernandes, P.C., Alves dos Santos, I. (2013) Euglossine bees (Apidae) in Atlantic forest areas of São Paulo State, southeastern Brazil. Apidologie 44, 254–267

    Article  Google Scholar 

  • David, R., Carde, J.P. (1964) Coloration différentielle des inclusions lipidique et terpeniques des pseudophylles du Pin maritime au moyen du reactif Nadi. C R Acad Sci (Paris) 258, 1338–1340

    CAS  Google Scholar 

  • Dodson, C.H., Dressler, R.L., Hills, H.G., Adams, R.M., Williams, N.H. (1969) Biologically active compounds in orchid fragrances. Science 164, 1243–1249

    Article  CAS  PubMed  Google Scholar 

  • Dressler, R.L. (1982) Biology of the orchid bees (Euglossini). Annu Rev Ecol Syst 13, 373–394

    Article  Google Scholar 

  • Eltz, T., Roubik, D.W., Lunau, K. (2005a) Experience-dependent choices ensure species-specific fragrance accumulation in male orchid bee. Behav Ecol Sociobiol 59, 129–156

    Article  Google Scholar 

  • Eltz, T., Sager, A., Lunau, K. (2005b) Juggling with volatiles: exposure of perfumes by displaying male orchid bees. J Comp Physiol 191, 575–581

    Article  Google Scholar 

  • Eltz, T., Zimmermann, Y., Pfeiffer, C., Ramírez Pech, J., Twele, R., Francke, W., Quezada-Euan, J.J.G., Lunau, K. (2008) An olfactory shift is associated with male perfume differentiation and species divergence in orchid bees. Curr Biol 18, 1844–1848

    Article  CAS  PubMed  Google Scholar 

  • Faegri, K., van der Pijl, L. (1979) The principles of pollination ecology, 3rd revised edition. Pergamon Press, Oxford

  • Furr, M., Mahlberg, P.G. (1981) Histochemical analyses of laticifers and glandular trichomes in Cannabis sativa. J Nat Prod 44, 153–159

    Article  Google Scholar 

  • Ganter, P., Jollés, G. (1969) Histologie normale et pathologique, vol. 1. Gauthier-Villars, Paris

    Google Scholar 

  • Ganter, P., Jollés, G. (1970) Histologie normale et pathologique, vol. 2. Gauthier-Villars, Paris

    Google Scholar 

  • Gregory, M., Baas, P. (1989) A survey of mucilage cells in vegetative organs of the dicotyledons. Isr J Bot 38, 125–174

    Google Scholar 

  • Jensen, W.A. (1962) Botanical histochemistry: principles and practice. Freeman, San Francisco

    Google Scholar 

  • Johansen, D.A. (1940) Plant microtechnique. McGraw-Hill, New York

    Google Scholar 

  • Kirk Jr., P.W. (1970) Neutral red as a lipid fluorochrome. Stain Technol 45, 1–4

    CAS  PubMed  Google Scholar 

  • Langenheim, J.H. (2003) Plant resins: chemistry, evolution, ecology, and ethnobotany. Timber Press, Cambridge

    Google Scholar 

  • Machado, I.C., Vogel, S., Lopes, A.V. (2002) Pollination of Angelonia cornigera Hook. (Scrophulariaceae) by long-legged, oil collecting bees in NE Brazil. Plant Biol 4, 352–359

    Article  Google Scholar 

  • Martins, A.C., Aguiar, A.J.C., Alves dos Santos, I. (2013) Interaction between oil-collecting bees and seven species of Plantaginaceae. Flora 208, 401–411

    Article  Google Scholar 

  • Matozzo, V.C., Faria, L.R.R., Melo, G.A.R. (2011) Orchid bees (Hymenoptera: Apidae) in the coastal forest of southern Brazil: diversity, efficiency of sampling methods and comparison with other Atlantic forest surveys. Pap Avulsos Zool 51, 505–515

    Google Scholar 

  • Pearse, A.G.E. (1985) Histochemistry: theoretical and applied, vol. 2. 4th ed. C. Livingstone, Edinburgh

  • Pearson, D.L., Dressler, R.L. (1985) Two-year study of male orchid bee (Hymenoptera: Apidae: Euglossini) attraction to chemical baits in lowland southeastern Peru. J Trop Ecol 1, 37–54

    Article  Google Scholar 

  • Pemberton, R.W., Wheeler, G.S. (2006) Orchid bees don’t need orchids: evidence from the naturalization of an orchid bee in Florida. Ecology 87, 1995–2001

    Article  PubMed  Google Scholar 

  • Peter, C.I., Johnson, S.D. (2014) A pollinator shift explains floral divergence in an orchid species complex in South Africa. Ann Bot-London 113, 277–288

  • Pokorny, T., Hannibal, M., Quezada-Euan, J.J.G., Hedenström, E., Sjöberg, N., Bång, J., Eltz, T. (2013) Acquisition of species-specific perfume blends: influence of habitat-dependent compound availability on odour choices of male orchid bees (Euglossa spp.). Oecologia 172, 417–425

    Article  CAS  PubMed  Google Scholar 

  • Ramírez, S., Dressler, R.L., Opsina, M. (2002) Abejas euglossinas (Hymenoptera:Apidae) de la Región Neotropical: Listado de espeices con notea sobre su biología. Biot Colomb 3, 7–118

    Google Scholar 

  • Ramírez, S., Eltz, T., Fujiwara, M.K., Gerlach, G., Goldman-Huertas, B., Tsutsui, N.D., Pierce, N.E. (2011) Asynchronous diversification in a specialized plant-pollinator mutualism. Science 333, 1742–1746

    Article  PubMed  Google Scholar 

  • Rebêlo, J.M.M., Garófalo, C.A. (1991) Diversidade e sazonalidade de machos de Euglossini (Hymenoptera, Apidae) e preferências por iscasodores em um fragmento de floresta no sudeste do Brasil. Rev Bras Biol 51, 787–799

    Google Scholar 

  • Rosas-Guerrero, V., Aguilar, R., Martén-Rodríguez, S., Ashworth, L., Lopezaraiza-Mikel, M., Bastida, J.M., Quesada, M. (2014) A quantative review of pollination syndrome: do floral traits predict effective pollinators? Ecol Lett 17, 388–400

  • Roubik, D.W., Hanson, P.E. (2004) Abejas de orquídeas de a América tropical: biologia y guia de campo. Orchid bees of tropical America: biology and field guide, San José

    Google Scholar 

  • Sazima, M., Vogel, S., Cocucci, A., Hausner, G. (1993) The perfume flowers of Cyphomandra (Solanaceae): pollination by euglossine bees, bellows mechanism, osmophores, and volatiles. Plant Syst Evol 187, 51–88

    Article  CAS  Google Scholar 

  • Smith, S.D., Ané, C., Baum, D.A. (2009) Macroevolutionary tests of pollination syndromes: a reply to Fenster et al. Evolution 63, 2763–2767

    Article  Google Scholar 

  • Vogel, S. (1966) Parfümsammelnde Bienen als Bestäuber von Orchidaceen und Gloxinia Osterr. Bot Zs 113, 302–361

    Article  Google Scholar 

  • Vogel, S. (1974) Ölblumen und ölsammelnde Bienen. Trop Subtrop Pflanzenwelt 7, 1–267

    Google Scholar 

  • Vogel, S. (1990) The role of scent glands in pollination. Amerind Publishing, New Delhi

    Google Scholar 

  • Vogel, S., Machado, I.C. (1991) Pollination of four sympatric species of Angelonia (Scrophulariaceae) by oil-collecting bees in NE Brazil. Plant Syst Evol 178, 153–178

    Google Scholar 

  • Waser, N.M., Chittka, L., Price, M.V., Williams, N.M., Ollerton, J. (1996) Generalization in pollination systems, and why it matters. Ecology 77, 1043–1060

    Article  Google Scholar 

  • Whitten, W.M., Young, A.M., Stern, D.L. (1993) Non-floral sources of chemicals that attract male euglossine bees (Apidae: Euglossini). J Chem Ecol 19, 3017–3027

    Article  CAS  PubMed  Google Scholar 

  • Williams, N.H., Dressler, R.L. (1976) Euglossine pollination of Spathiphyllum (Araceae). Selbyana 1, 349–356

    Google Scholar 

  • Williams, N.H., Whitten, W.M. (1983) Orchid floral fragrances and male Euglossine bees: methods advances in the last sesquidecade. Biol Bull 164, 355–395

Download references

Acknowledgments

We thank Claudia Saito and Sheina Koffler for their help and additional observations in the field, Paulo César Fernandes for providing pictures and Antonella Soro and the two reviewers for helpful comments. Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) funded the first author.

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Authors and Affiliations

  1. Programa de Pós-Graduação em Entomologia, Faculdade de Filosofia Ciências e Letras de Ribeirão Preto, Universidade de São Paulo (USP), Av. Bandeirantes 3900, Bloco 2, Ribeirão Preto, SP, 14040-901, Brazil

    Samuel Boff

  2. General Zoology, Institute for Biology, Martin-Luther-University Halle-Wittenberg, Hoher Weg 8, 06120, Halle Saale, Germany

    Samuel Boff

  3. Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, 05508-090, Brazil

    Diego Demarco

  4. Departamento Ecologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, 05508-900, Brazil

    Paola Marchi & Isabel Alves-Dos-Santos

Authors
  1. Samuel Boff
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  2. Diego Demarco
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  3. Paola Marchi
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  4. Isabel Alves-Dos-Santos
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Correspondence to Samuel Boff.

Additional information

Handling Editor: Bernd Grünewald

La production de parfum dans les fleurs d’ Angelonia salicariifolia attire les mâles d’ Euglossa annectans bien qu’ils ne participent pas à la pollinisation

Euglossini / analyse histochimique / voleur de parfum / trichomes / parfum volatile

Duftproduktion in Blüten von Angelonia salicariifolia wirken anziehend auf Männchen von Euglossa annectans , die nicht als Bestäuber fungieren

Euglossa annectans / Euglossini / histochemische Analyse / Duft Räuber / Trichom / flüchtige Duftstoffe

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Boff, S., Demarco, D., Marchi, P. et al. Perfume production in flowers of Angelonia salicariifolia attracts males of Euglossa annectans which do not promote pollination. Apidologie 46, 84–91 (2015). https://doi.org/10.1007/s13592-014-0305-2

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