Abstract
Male orchid bees (Euglossini, Apidae, Hymenoptera) expose species-specific blends of volatile chemicals (perfume bouquets) during their courtship display. The perfumes are acquired by collecting fragrant substances from environmental sources, which are then accumulated in specialised hind leg pouches. To balance the perfume composition, the males need to find and collect the required substances in specific relative amounts while facing seasonal, local or habitat-dependent differences in compound availability. Experience-dependent choice of odours, i.e. ‘learned avoidance’ of recently collected components, has been proposed as the mechanism that mediates the accumulation of the stereotypical compound ratios. In the present study, we used the presence of certain compounds in male hind leg pouches as proxy for the respective local compound availability, and investigated whether differences in content are correlated with differences in chemical choice assays. Our results suggest that volatile availability differs between localities (n = 16) as well as habitats (n = 2; coastal vs. inland) across the Yucatán peninsula, Mexico, for both studied species. Male Euglossa dilemma showed a pronounced preference for benzyl benzoate and eugenol at locations where those compounds were rare in hind leg extracts, as predicted by the learned avoidance model. No equivalent correlations were found for Euglossa viridissima. This is the first study to combine chemical analyses of perfumes with bioassays of odour choice. It strengthens the view that negative feedback from collected odours modifies future chemical choice and helps males to acquire specific perfume blends.
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References
Abrahamczyk S, Gottleuber P, Kessler M (2012) Seasonal changes in odour preferences by male euglossine bees (Hymenoptera: Apidae) and their ecological implications. Apidologie 43:212–217
Ackerman JD (1989) Geographic and seasonal variation in fragrance choices and preferences of male euglossine bees. Biotropica 21(4):340–347
Adams RP (2001) Identification of essential oil components by gas chromatography/quadrupole mass spectroscopy. Allured, Carol Stream
Bembé B (2004) Functional morphology in male euglossine bees and their ability to spray fragrances (Hymenoptera, Apidae, Euglossini). Apidologie 35:283–291
Cappellari SC, Harter-Marques B (2010) First report of scent collection by male orchid bees (Hymenoptera: Apidae: Euglossini) from terrestrial mushrooms. J Kans Entomol Soc 83(3):264–266
Clarke KR (1993) Non-parametric multivatiate analyses of changes in community structure. Aust J Ecol 18:117–143
Clarke KR, Gorley RN (2006) PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth
Dodson CH, Dressler RL, Hills HG, Adams RM, Williams NH (1969) Biologically active compounds in orchid fragrances. Science 164:1243–1249
Dressler RL (1982) Biology of the orchid bees (Euglossini). Annu Rev Ecol Syst 13:373–394
El-Sayed AM (2012) The pherobase: database of pheromones and semiochemicals. http://www.pherobase.com. Accessed 1 October 2012
Eltz T, Whitten MW, Roubik DW, Linsenmair KE (1999) Fragrance collection, storage, and accumulation by individual male orchid bees. J Chem Ecol 25(1):157–176
Eltz T, Roubik DW, Whitten MW (2003) Fragrances, male display and mating behaviour of Euglossa hemichlora: a flight cage experiment. Physiol Entomol 28:251–260
Eltz T, Roubik DW, Lunau K (2005a) Experience-dependent choices ensure species-specific fragrance accumulation in male orchid bees. Behav Ecol Sociobiol 59:149–156
Eltz T, Sager A, Lunau K (2005b) Juggling with volatiles: exposure of perfumes by displaying male orchid bees. J Comp Physiol A 191:575–581
Eltz T, Zimmermann Y, Haftmann J, Twele R, Francke W, Quezada-Euan JJG, Lunau K (2007) Enfleurage, lipid recycling and the origin of perfume collection in orchid bees. Proc R Soc Lond B 274:2843–2848
Eltz T, Zimmermann Y, Pfeiffer C, Ramirez Pech J, Twele R, Francke W, Quezada-Euan JJG, Lunau K (2008) An olfactory shift is associated with male perfume differentiation and species divergence in orchid bees. Curr Biol 18:1844–1848
Eltz T, Fritzsch F, Ramírez Pech J, Zimmermann Y, Ramírez SR, Quezada-Euan JJG, Bembé B (2011) Characterization of the orchid bee Euglossa viridissima (Apidae: Euglossini) and a new cryptic sibling species, by morphological, chemical, and genetic characters. Zool J Linn Soc 163:1064–1076
Flores JS (1990) The flowering periods of Leguminosae in the Yucatan peninsula in relation to honey flows. J Apic Res 29:82–88
Hartter J, Lucas C, Gaughan AE, Aranda LL (2008) Detecting tropical dry forest succession in a shifting cultivation mosaic of the Yucatán Peninsula, Mexico. Appl Geogr 28:134–149
Honda Y, Honda K, Ômura H (2006) Major components in the hairpencil secretion of a butterfly, Euploea mulciber (Lepidoptera, Danaidae): their origins and male behavioral responses to pyrrolizidine alkaloids. J Insect Physiol 52:1043–1053
Pemberton RW, Wheeler GS (2006) Orchid bees don’t need orchids: evidence from the naturalization of an orchid bee in Florida. Ecology 87(8):1995–2001
Ramírez SR, Eltz T, Fritzsch F, Pemberton R, Pringle EG, Tsutsui ND (2010) Intraspecific geographic variation of fragrances acquired by orchid bees in native and introduced populations. J Chem Ecol 36(8):873–884
Ramírez SR, Eltz T, Fujiwara MK, Gerlach G, Goldman-Huertas B, Tsutsui ND, Pierce NE (2011) Asynchronous diversification in a specialized plant–pollinator mutualism. Science 333:742–746
Rejmánková E, Pope KO, Post R, Maltby E (1996) Herbaceous wetlands of the Yucatán peninsula: communities at extreme ends of environmental gradients. Int Rev Gesamten Hydrobiol Hydrogr 81(2):223–252
R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org. Accessed 6 September 2012
Roubik DW, Hanson PE (2004) Orchid bees of tropical America. Instituto Nacional de Biodiversidad (INBio), Heredia, Costa Rica
Schneider D, Boppré M, Schneider H, Thompson WR, Boriack CJ, Petty RL, Meinwald J (1975) A pheromone precursor and its uptake in male Danaus butterflies. J Comp Physiol A 97(3):245–256
Schulz S, Beccaloni G, Brown KS Jr, Boppré M, Freitas AVL, Ockenfels P, Trigo JR (2004) Semiochemicals derived from pyrrolizidine alkaloids in male ithomiine butterflies (Lepidoptera: Nymphalidae: Ithomiinae). Biochem Syst Ecol 32:699–713
Skov C, Wiley J (2005) Establishment of the neotropical orchid bee Euglossa viridissima (Hymenoptera: Apidae) in Florida. Fla Entomol 88(2):225–227
Trejo-Torres JC, Durán R, Olmsted I (1993) Manglares de la península de Yucatán. In: Salazar-Vallejo S, Gonzaléz NE (eds) Biodiversidad marina y costera de México. Comisión Nacional para el Conocimiento y Aprovechamiento de la Biodiversidad, Centro de Investigaciones de Quintana Roo, pp 660–672
Vogel S (1966) Parfümsammelnde Bienen als Bestäuber von Orchidaceen und Gloxinia. Österr bot Z 113:302–361
Whitten MW, Young AM, Stern DL (1993) Nonfloral sources of chemicals that attract male euglossine bees (Apidae: Euglossini). J Chem Ecol 19(12):3017–3027
Williams NH, Whitten MW (1983) Orchid floral fragrances and male euglossine bees: methods and advances in the last sesquidecade. Biol Bull 164:355–395
Wilson EM, Williams A (1987) A coastal ecosystem in northwestern Yucatán. sites.maxwell.syr.ecu/clag/yearbook1987/wilson.htm. Accessed 12 October 2012
Zimmermann Y, Ramírez SR, Eltz T (2009) Chemical niche differentiation among sympatric species of orchid bees. Ecology 90:2994–3008
Zimmermann Y, Schorkopf DL, Moritz RFA, Pemberton RW, Quezada-Euan JJG, Eltz T (2011) Population genetic structure of orchid bees (Euglossini) in anthropogenically altered landscapes. Conserv Genet 12:1183–1194
Acknowledgments
Jorge Ramirez-Pech helped with sample collection. Funding was provided by the PROALMEX program (120989) of the German Academic Exchange Service and the Consejo Nacional de Ciencia y Tecnología (103341) to T.E. and J.Q.E., and the German Science Foundation (EL 249/6). Santiago Ramírez, Florian Leese, the Evolutionary Ecology journal club group (Bochum), and two anonymous reviewers helped to improve the manuscript. E.H., J.B. and N.S. would like to thank the European Union European Regional Development Fund and the County Administrative Board of Västernorrland for financing. All experiments comply with the current laws of Mexico and were performed with the necessary permits.
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Communicated by Richard Karban.
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Pokorny, T., Hannibal, M., Quezada-Euan, J.J.G. et al. 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 (2013). https://doi.org/10.1007/s00442-013-2620-0
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DOI: https://doi.org/10.1007/s00442-013-2620-0