Experience-dependent choices ensure species-specific fragrance accumulation in male orchid bees

Original Article

Abstract

Male neotropical orchid bees (Euglossini) collect volatile chemicals from orchid flowers and other sources and store them in hind leg cavities. The accumulated fragrance bouquets are later emitted at mating sites. Although most other insects synthesize pheromone blends de novo, specific euglossine perfumes are derived from active choices in a changing fragrance market. Male bees of three species of Euglossa possessed distinctive fragrance phenotypes showing little variation by locality and habitat in mainland Central America. In cage experiments, fragrance choice by male Euglossa imperialis was influenced markedly by a bee's collection history. Collection of a given chemical strongly reduced its attractiveness on subsequent occasions, an effect that was retained over days. Experimentally adding the chemicals directly to bee hind legs produced no effect. We conclude that bees learn and remember chemicals they collect. Innate odor preferences, memory and the avoidance of overcollecting by negative feedback may be the primary mechanisms that ensure unique blends of pheromone analogs in these tropical forest bees.

Keywords

Methyl Salicylate Benzyl Benzoate Flight Cage Male Euglossines Fragrance Bouquet 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

Work and manuscript benefited substantially from discussions held within the Sensory Ecology Group seminar in Düsseldorf. Randolf Menzel, Bertram Gerber, and an anonymous reviewer provided insights concerning learning mechanisms. The chemical–analytical part of the study was substantiated by Roman Kaiser, who cross-checked reference samples and identified critical fragrance compounds. Günter Gerlach provided chemical baits and access to his wealth of baiting data. Georg Pohland and Peter Mullen helped to collect bee samples in Costa Rica and Panama. The study was sponsored by DFG grant EL 249/2-1

Supplementary material

265_2005_21_Fig5_ESM.gif (182 kb)
S1

Incidence, average relative abundance, and contribution to within-species similarity of fragrance components in hind-leg extracts of three species of Euglossa in mainland Panama (pooled across localities 2, 3, and 4).

265_2005_21_Fig6_ESM.gif (148 kb)
S2

Incidence, average relative abundance, and contribution to within-species similarity of fragrance components in hind-leg extracts of Euglossa tridentata at six localities in Panama and Costa Rica.

References

  1. Ackerman JD (1983) Specificity and mutual dependency of the orchid-euglossine bee interaction. Biol J Linn Soc 20:301–314CrossRefGoogle Scholar
  2. Ackerman JD (1989) Geographic and seasonal variation in fragrance choice and preferences of male euglossine bees. Biotropica 21:340–347CrossRefGoogle Scholar
  3. Ackerman JD, Montalvo AM (1985) Longevity of euglossine bees. Biotropica 17:79–81CrossRefGoogle Scholar
  4. Adams RP (2001) Identification of essential oil components by Gas Chromatography/Quadrupole Mass Spectroscopy. Allured Publishing Corporation, Carol Stream, USAGoogle Scholar
  5. Ayasse M, Paxton RJ, Tengo J (2001) Mating behavior and chemical communication in the order hymenoptera. Annu Rev Entomol 46:31–78CrossRefPubMedGoogle Scholar
  6. Bergman P, Bergstrom G (1997) Scent marking, scent origin, and species specificity in male premating behavior of two Scandinavian bumblebees. J Chem Ecol 23:1235–1251CrossRefGoogle Scholar
  7. Bjostad LB, Wolf WA, Roelofs WL (1987) Pheromone biosynthesis in Lepidopterans: desaturation and chain shortening. In: Prestwich GD, Blomquist GJ (eds) Pheromone biochemistry. Academic Press, Orlando, pp 77–119Google Scholar
  8. Cameron SA (2004) Phylogeny and biology of neotropical orchid bees (Euglossini). Annu Rev Entomol 49:377–404CrossRefPubMedGoogle Scholar
  9. Cardé RT, Baker TC (1984) Sexual communication with pheromones. In: Bell WJ, Cardé RT (eds) Chemical ecology of insects. Chapman and Hall, London New York, pp 355–376Google Scholar
  10. Carew TJ, Pinsker HM, Kandel ER (1972) Long-term habituation of a defensive withdrawal reflex in Aplysia. Science 175:451–454PubMedCrossRefGoogle Scholar
  11. Chandra S, Smith BH (1998) An analysis of synthetic processing of odor mixtures in the honeybee (Apis mellifera). J Exp Biol 201:3113–3121PubMedGoogle Scholar
  12. Chandra SBC, Hosler JS, Smith BH (2000) Heritable variation for latent inhibition and its correlation with reversal learning in honeybees (Apis mellifera). J Comp Psychol 114:86–97CrossRefPubMedGoogle Scholar
  13. Clarke KR (1993) Nonparametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143CrossRefGoogle Scholar
  14. Clarke KR (1999) Nonmetric multivariate analysis in community-level ecotoxicology. Environ Toxicol Chem 18:118–127CrossRefGoogle Scholar
  15. Clarke KR, Gorley RN (2001) PRIMER v5: user manual/tutorial. Primer-E Ltd, PlymouthGoogle Scholar
  16. Clarke KR, Green RH (1988) Statistical design and analysis for a ‘biological effects‘ study. Mar Ecol Progr Ser 46:213–226CrossRefGoogle Scholar
  17. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E Ltd, PlymouthGoogle Scholar
  18. Cromarty SI, Derby CD (1997) Multiple excitatory receptor types on individual olfactory neurons: implications for coding of mixtures in the spiny lobster. J Comp Physiol A 180:481–491CrossRefPubMedGoogle Scholar
  19. Dodson CH (1975) Coevolution of orchids and bees. In: Gilbert LC, Raven PH (eds) Coevolution of animals and plants. University of Texas Press, Austin, pp 91–99Google Scholar
  20. Dodson CH, Dressler RL, Hills HG, Adams RM, Williams NH (1969) Biologically active compounds in orchid fragrances. Science 164:1243–1249PubMedCrossRefGoogle Scholar
  21. Dressler RL (1968) Pollination by euglossine bees. Evolution 22:202–210CrossRefGoogle Scholar
  22. Dressler RL (1982) Biology of the orchid bees (Euglossini). Ann Rev Ecol Syst 13:373–394CrossRefGoogle Scholar
  23. Eltz T, Roubik DW, Whitten WM (2003) Fragrances, male display and mating behaviour of Euglossa hemichlora—a flight cage experiment. Phys Entomol 28:251–260CrossRefGoogle Scholar
  24. Eltz T, Sager A, Lunau K (2005) Juggling with volatiles: exposure of perfumes by displaying male orchid bees. J Comp Physiol A, 191:575–581Google Scholar
  25. Eltz T, Whitten WM, Roubik DW, Linsenmair KE (1999) Fragrance collection, storage, and accumulation by individual male orchid bees. J Chem Ecol 25:157–176CrossRefGoogle Scholar
  26. Engel MS (1999) The first fossil Euglossa and the phylogeny of the orchid bees (Hymenoptera: Apidae: Euglossini). Am Mus Novit 3272:1–14Google Scholar
  27. Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals—role of plant secondary compounds. Am Nat 108:269–289CrossRefGoogle Scholar
  28. Gerlach G, Schill R (1989) Fragrance analyses, an aid to taxonomic relationships of the genus Coryanthes (Orchidaceae). Plant Syst Evol 168:159–165CrossRefGoogle Scholar
  29. Gerlach G, Schill R (1991) Composition of orchid scents attracting euglossine bees. Bot Acta 104:379–391Google Scholar
  30. Hosler JS, Smith BH (2000) Blocking and the detection of odor components in blends. J Exp Biol 203:2797–2806PubMedGoogle Scholar
  31. Janzen DH (1971) Euglossine bees as long-distance pollinators of tropical plants. Science 171:203–205PubMedCrossRefGoogle Scholar
  32. Janzen DH (1981) Reduction in euglossine bee species richness on Isla del Cano, a Costa Rican offshore island. Biotropica 13:238–240CrossRefGoogle Scholar
  33. Janzen DH, DeVries PJ, Higgins ML, Kimsey LS (1982) Seasonal and site variation in Costa Rican euglossine bees at chemical baits in lowland decidous and evergreen forest. Ecology 63:66–74CrossRefGoogle Scholar
  34. Kaiser R (1993) The scent of orchids—olfactory and chemical investigations. Hoffmann La Roche, BaselGoogle Scholar
  35. Kimsey LS (1980) The behaviour of male orchid bees (Apidae, Hymenoptera, Insecta) and the question of leks. Anim Behav 28:996–1004CrossRefGoogle Scholar
  36. Krehbiel MD, Nagel PJ (1998) A comparison of euglossine species diversity between Isla del Cano, a Costa Rican offshore island, and the adjacent mainland. Online publication http://www.educationabroad.com/body_alumni_projects_ spring97_5.htm
  37. Legendre P, Legendre L (1998) Numerical ecology, 2nd edn. Elsevier, AmsterdamGoogle Scholar
  38. Linn CE, Roelofs WL (1995) Pheromone communication in moths and its role in the speciation process. In: Lambert DM, Spencer HG (eds) Speciation and the recognition concept. The Johns Hopkins University Press, Baltimore, pp 263–300Google Scholar
  39. Minckley RL, Buchmann SL, Wcislo WT (1991) Bioassay evidence for a sex attractant pheromone in the large carpenter bee, Xylocopa varipuncta (Anthophoridae, Hymenoptera). J Zool 224:285–291Google Scholar
  40. Morse D, Meighen E (1987) Pheromone biosynthesis: enzymatic studies in Lepidoptera. In: Prestwich GD, Blomquist GJ (eds) Pheromone biochemistry. Academic Press, Orlando, pp 121–158Google Scholar
  41. Murren CJ (2002) Effects of habitat fragmentation on pollination: pollinators, pollinia viability and reproductive success. J Ecol 90:100–107CrossRefGoogle Scholar
  42. Pearson DL, Dressler RL (1985) Two-year study of male orchid bee (Hymenoptera: Apidae: Euglossini) attraction to chemical baits in lowland south-eastern Peru. J Trop Ecol 1:37–54CrossRefGoogle Scholar
  43. Provenza FD (1996) Acquired aversions as the basis for varied diets of ruminants foraging on rangelands. J Anim Sci 74:2010–2020PubMedGoogle Scholar
  44. Ramirez S, Dressler RL, Ospina M (2002) Abejas euglosinas (Hymenoptera: Apidae) de la Región Neotropical: Listado de especies con notas sobre su biología. Biota Colombiana 3:7–118Google Scholar
  45. Roelofs WL (1995) The chemistry of sex sex attraction. In: Eisner T, Meinwald J (eds) Chemical Ecology. National Academy Press, Washington, DC, pp 103–118Google Scholar
  46. Roelofs WL, Liu WT, Hao GX, Jiao HM, Rooney AP, Linn CE (2002) Evolution of moth sex pheromones via ancestral genes. Proc Natl Acad Sci USA 99:13621–13626CrossRefPubMedGoogle Scholar
  47. Roelofs WL, Rooney AP (2003) Molecular genetics and evolution of pheromone biosynthesis in Lepidoptera. Proc Natl Acad Sci USA 100:9179–9184CrossRefPubMedGoogle Scholar
  48. Roubik DW, Hanson PE (2004) Orchid bees of tropical America: Biology and field guide. Instituto Nacional de Biodiversidad (INBio), Heredia, Costa RicaGoogle Scholar
  49. Smith BH, Getz WM (1994) Nonpheromonal olfactory processing in insects. Annu Rev Entomol 39:351–375CrossRefGoogle Scholar
  50. Stern DL (1991) Male territoriality and alternative male behaviors in the euglossine bee, Eulaema meriana (Hymenoptera: Apidae). J Kansas Entomol Soc 64:421–437Google Scholar
  51. Stopfer M, Chen XH, Tai YT, Huang GS, Carew TJ (1996) Site specificity of short-term and long-term habituation in the tail-elicited siphon withdrawal reflex of Aplysia. J Neurosci 16:4923–4932PubMedGoogle Scholar
  52. Vogel S (1966) Parfümsammelnde Bienen als Bestäuber von Orchidaceen und Gloxinia. Österr Botan Zeit 113:302–361CrossRefGoogle Scholar
  53. Wasserman EA, Miller RR (1997) What's elementary about associative learning? Annu Rev Psychol 48:573–607CrossRefPubMedGoogle Scholar
  54. White CS, Lambert DM, Foster SP (1995) Chemical signals and the recognition concept. In: Lambert DM, Spencer HG (eds) Speciation and the recognition concept. The Johns Hopkins University Press, Baltimore, pp 301–326Google Scholar
  55. Whitten WM, Williams NH (1992) Floral fragrances of Stanhopea (Orchidaceae). Lindleyana 7:130–153Google Scholar
  56. Whitten WM, Williams NH, Armbruster WS, Battiste MA, Strekowski L, Lindquist N (1986) Carvone oxide: an example of convergent evolution in euglossine pollinated plants. Syst Bot 11:222–228CrossRefGoogle Scholar
  57. Whitten WM, Young AM, Stern DL (1993) Nonfloral sources of chemicals that attract male euglossine bees (Apidae: Euglossini). J Chem Ecol 19:3017–3027CrossRefGoogle Scholar
  58. Whitten WM, Young AM, Williams NH (1989) Function of glandular secretions in fragrance collection by male euglossine bees. J Chem Ecol 15:1285–1295CrossRefGoogle Scholar
  59. Williams NH (1982) The biology of orchids and euglossine bees. In: Arditti J (ed) Orchid biology: reviews and perspectives. Cornell University Press, Ithaca, NY, pp 119–171Google Scholar
  60. Williams NH, Dodson CH (1972) Selective attraction of male euglossine bees to orchid floral fragrances and its importance in long distance pollen flow. Evolution 26:84–95CrossRefGoogle Scholar
  61. Williams NH, Whitten WM (1983) Orchid floral fragrances and male euglossine bees: methods and advances in the last sesquidecade. Biol Bull 164:355–395CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Department of Neurobiology, Sensory Ecology GroupUniversity of DüsseldorfDüsseldorfGermany
  2. 2.Smithsonian Tropical Research InstituteBalboaPanama

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