Advertisement

Journal of Chemical Ecology

, Volume 39, Issue 11–12, pp 1347–1360 | Cite as

The Chemical Basis of Host-Plant Recognition in a Specialized Bee Pollinator

  • Paulo Milet-Pinheiro
  • Manfred Ayasse
  • Heidi E. M. Dobson
  • Clemens Schlindwein
  • Wittko Francke
  • Stefan Dötterl
Article

Abstract

Many pollinators specialize on a few plants as food sources and rely on flower scents to recognize their hosts. However, the specific compounds mediating this recognition are mostly unknown. We investigated the chemical basis of host location/recognition in the Campanula-specialist bee Chelostoma rapunculi using chemical, electrophysiological, and behavioral approaches. Our findings show that Ca. trachelium flowers emit a weak scent consisting of both widespread and rare (i.e., spiroacetals) volatiles. In electroantennographic analyses, the antennae of bees responded to aliphatics, terpenes, aromatics, and spiroacetals; however, the bioassays revealed a more complex response picture. Spiroacetals attracted host-naive bees, whereas spiroacetals together with aliphatics and terpenes were used for host finding by host-experienced bees. On the intrafloral level, different flower parts of Ca. trachelium showed differences in the absolute and relative amounts of scent, including spiroacetals. Scent from pollen-presenting flower parts elicited more feeding responses in host-naive bees as compared to a scentless control, whereas host-experienced bees responded more to the nectar-presenting parts. Our study demonstrates the occurrence of learning (i.e., change in the bee’s innate chemical search-image) after bees gain foraging experience on host flowers. We conclude that highly specific floral volatiles play a key role in host-flower recognition by this pollen-specialist bee, and discuss our findings into the broader context of host-recognition in oligolectic bees.

Keywords

Chelostoma Campanula Floral scents Host location/recognition Oligolectic bees Spiroacetals 

Notes

Acknowledgments

We thank Hannah Burger and Irmgard Schäffler for methodological support and constructive discussions, Hans-Joachim Flügel (Lebendiges Bienenmuseum Knüllwald) and Jochen Fründ (University of Göttingen, Germany) for providing nests of Chelostoma rapunculi, Gregor Aas for use of a greenhouse in the Ecological Botanical Garden of the University of Bayreuth for flight cage experiments, and the team from the Botanical Garden of the University of Ulm for providing Campanula fields to rear Chelostoma rapunculi bees used in our experiments. We also are thankful to Heather Carew, Jana Seaman, Michael Peterson, Debrakaye Nelson, Jennifer Telfer, Jamie Williamson, and Robert Davey for conducting multiple-choice behavioral experiments, the Station Linné in Sweden for its research facilities, and Whitman College for faculty-student Research funding, including two Perry Awards. Grants were provided to PM-P (Deutscher Akademischer Austauschdienst - A/08/71732) and to CS (Conselho Nacional de Desenvolvimento Científico e Tecnológico - 305692/2009-7 and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - BEX/4236/08-4).

Supplementary material

10886_2013_363_MOESM1_ESM.docx (24 kb)
ESM 1 Electronic Supplementary Material includes details on structure elucidation and synthesis of spiroacetals and preparation of synthetic mixtures for behavioral experiments (DOC 24.3 kb)

References

  1. Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectrometry. Allured Publishing Corporation, Carol Stream, p 804Google Scholar
  2. Andrews ES, Theis N, Adler LS (2007) Pollinator and herbivore attraction to Curcubita floral volatiles. J Chem Ecol 33:1682–1691PubMedCrossRefGoogle Scholar
  3. Ayasse M, Schiestl FP, Paulus HF, Ibarra F, Francke W (2003) Pollinator attraction in a sexually deceptive orchid by means of unconventional chemicals. Proc R Soc B 270:517–522PubMedCrossRefGoogle Scholar
  4. Balao F, Herrera J, Talavera S, Dötterl S (2011) Spatial and temporal patterns of floral scent emission in Dianthus inoxianus and electroantennographic responses of its hawkmoth pollinator. Phytochemistry 72:601–609PubMedCrossRefGoogle Scholar
  5. Bergström G, Tengö J, Reith W, Francke W (1982) Multicomponent mandibular gland secretions in three species of Andrena bees (Hym., Apoidea). Z Naturforsch C 37:1124–1129Google Scholar
  6. Blionis GJ, Vokou D (2001) Pollination ecology of Campanula species on Mt Olympos, Greece. Ecography 24:287–297Google Scholar
  7. Burger BV (2005) Mammalian semiochemicals. Top Curr Chem 240:231–278Google Scholar
  8. Burger H, Ayasse M, Häberlein CM, Schulz S, Dötterl S (2010a) Echium and Pontechium specific floral cues for host-plant recognition by the oligolectic bee Hoplitis adunca. S Afr J Bot 76:788–795CrossRefGoogle Scholar
  9. Burger H, Dötterl S, Ayasse M (2010b) Host-plant finding and recognition by visual and olfactory floral cues in an oligolectic bee. Funct Ecol 24:1234–1240CrossRefGoogle Scholar
  10. Burger H, Dötterl S, Häberlein C, Schulz S, Ayasse M (2012) An arthropod deterrent attracts specialised bees to their host plants. Oecologia 168:727–736PubMedCrossRefGoogle Scholar
  11. Cane JH, Sipes S (2006) Characterizing floral specialization by bees: analytical methods and revised lexicon for oligolecty. In: Waser NM, Ollerton J (eds) Plant-pollinator interactions: from specialization to generalization. The University of Chicago Press, Chicago, pp 99–121Google Scholar
  12. Chen C, Song Q, Proffit M, Bessiíre JM, Li Z, Hossaert-Mckey M (2009) Private channel: a single unusual compound assures specific pollinator attraction in Ficus semicordata. Funct Ecol 23:941–950CrossRefGoogle Scholar
  13. Chittka L, Raine NE (2006) Recognition of flowers by pollinators. Curr Opin Plant Biol 9:428–435PubMedCrossRefGoogle Scholar
  14. Clarke KR, Gorley RN (2006) Primer v6: user manual/tutorial. Primer-E, Plymouth, p 91Google Scholar
  15. Dobson HEM (1987) Role of flower and pollen aromas in host-plant recognition by solitary bees. Oecologia 72:618–623CrossRefGoogle Scholar
  16. Dobson HEM (2006) Relationship between floral frangrance composition and type of pollinator. In: Dudareva N, Pichersky E (eds) Biology of floral scent. CRC Press, Boca Raton, pp 147–198CrossRefGoogle Scholar
  17. Dobson HEM, Bergström G (2000) The ecology of pollen odors. Plant Syst Evol 222:63–87CrossRefGoogle Scholar
  18. Dötterl S, Füssel U, Jürgens A, Aas G (2005a) 1,4-Dimethoxybenzene, a floral scent compound in willows that attracts an oligolectic bee. J Chem Ecol 31:2993–2998PubMedCrossRefGoogle Scholar
  19. Dötterl S, Jürgens A (2005) Spatial fragrance patterns in flowers of Silene latifolia: Lilac compounds as olfactory nectar guides? Plant Syst Evol 255:99–109CrossRefGoogle Scholar
  20. Dötterl S, Jürgens A, Seifert K, Laube T, Weißbecker B, Schütz S (2006) Nursery pollination by a moth in Silene latifolia: the role of odours in eliciting antennal and behavioural responses. New Phytol 169:707–718PubMedCrossRefGoogle Scholar
  21. Dötterl S, Milchreit K, Schäffler I (2011) Behavioural plasticity and sex differences in host finding of a specialized bee species. J Comp Physiol A 197:1119–1126CrossRefGoogle Scholar
  22. Dötterl S, Schäffler I (2007) Flower scent of floral oil-producing Lysimachia punctata as attractant for the oil-bee Macropis fulvipes. J Chem Ecol 33:441–445PubMedCrossRefGoogle Scholar
  23. Dötterl S, Vereecken JN (2010) The chemical ecology and evolution of bee-flower interactions: a review and perspectives. Can J Zool 88:668–697CrossRefGoogle Scholar
  24. Dötterl S, Wolfe LM, Jürgens A (2005b) Qualitative and quantitative analyses of flower scent in Silene latifolia. Phytochemistry 66:203–213PubMedCrossRefGoogle Scholar
  25. Feulner M, Schuhwerk F, Dötterl S (2009) Floral scent analysis in Hieracium subgenus Pilosella and its taxonomical implications. Flora 204:495–505CrossRefGoogle Scholar
  26. Fletcher MT, Jacobs MF, Kitching W, Krohn S, Drew RAI, Haniotakis GE, Francke W (1992) Absolute stereochemistry of the 1,7-dioxaspiro[5.5]undecanols in fruit-fly species, including the olive-fly. J Chem Soc Chem Commun 19:1457–1459CrossRefGoogle Scholar
  27. Francke W, Bartels J, Meyer H, Schröder F, Kohnle U, Baader E, Vité JP (1995) Semiochemicals from bark beetles: new results, remarks, and reflections. J Chem Ecol 21:1043–1063PubMedCrossRefGoogle Scholar
  28. Francke W, Kitching W (2001) Spiroacetals in insects. Curr Org Chem 5:233–251CrossRefGoogle Scholar
  29. Francke W, Reith W, Bergström G, Tengö J (1981) Pheromone bouquet of the mandibular glands in Andrena haemorrhoa F. (Hym., Apoidea). Z Naturforsch C 36:928–932Google Scholar
  30. Grison-Pigé L, Bessière J-M, Hossaert-Mckey M (2002) Specific attraction of fig-pollinating wasps: role of volatile compounds released by tropical figs. J Chem Ecol 28:283–295PubMedCrossRefGoogle Scholar
  31. Heiduk A, Brake I, Tolasch T, Frank J, Jürgens A, Meve U, Dötterl S (2010) Scent chemistry and pollinator attraction in the deceptive trap flowers of Ceropegia dolichophylla. S Afr J Bot 76:762–769CrossRefGoogle Scholar
  32. Howell AD, Alarcón R (2007) Osmia bees (Hymenoptera: Megachilidae) can detect nectar-rewarding flowers using olfactory cues. Anim Behav 74:199–205CrossRefGoogle Scholar
  33. Huber DPW, Gries R, Borden JH, Pierce HD (1999) Two pheromones of coniferophagous bark beetles found in the bark of nonhost angiosperms. J Chem Ecol 25:805–816CrossRefGoogle Scholar
  34. Jost L (1918) Die Griffelhaare der Campanulablüte. Flora 111:478–489Google Scholar
  35. Kessler A, Heil M (2011) The multiple faces of indirect defences and their agents of natural selection. Funct Ecol 25:348–357CrossRefGoogle Scholar
  36. Kirchner O (1897) Blüteneinrichtungen der Campanulaceen. Jahresh Ver Vaterl Naturkd Württemb 53:193–228Google Scholar
  37. Knudsen JT, Eriksson R, Gershenzon J, Stahl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120CrossRefGoogle Scholar
  38. Kunze J, Gumbert A (2001) The combined effect of color and odor on flower choice behavior of bumblebees in flower mimic systems. Behav Ecol 12:447–456CrossRefGoogle Scholar
  39. Lunau K (1995) Notes on the colour of pollen. Plant Syst Evol 198:235–252CrossRefGoogle Scholar
  40. Lunau K, Maier EJ (1995) Innate colour preferences of flower visitors. J Comp Physiol A 177:1–19CrossRefGoogle Scholar
  41. Mcdonald JH (2009) Handbook of biological statistics. Sparky House Publishing, Baltimore, p 313Google Scholar
  42. Milet-Pinheiro P, Ayasse M, Schlindwein C, Dobson HEM, Dötterl S (2012) Host location by visual and olfactory floral cues in an oligolectic bee: innate and learned behavior. Behav Ecol 23:531–538CrossRefGoogle Scholar
  43. Minckley RL, Roulston TH (2006) Incidental mutualisms and pollen specialization among bees. In: Waser NM, Ollerton J (eds) Plant-pollinator interactions: from specialization to generalization. The University of Chicago Press, Chicago, pp 69–98Google Scholar
  44. Müller A, Kuhlmann M (2008) Pollen hosts of western palaearctic bees of the genus Colletes (Hymenoptera: Colletidae): the Asteraceae paradox. Biol J Linn Soc 95:719–733CrossRefGoogle Scholar
  45. Peakall R, Ebert D, Poldy J, Barrow RA, Francke W, Bower CC, Schiestl FP (2010) Pollinator specificity, floral odour chemistry and the phylogeny of Australian sexually deceptive Chiloglottis orchids: implications for pollinator-driven speciation. New Phytol 188:437–450PubMedCrossRefGoogle Scholar
  46. Pernal SF, Currie RW (2002) Discrimination and preferences for pollen-based cues by foraging honeybees, Apis mellifera L. Anim Behav 63:369–390CrossRefGoogle Scholar
  47. Praz CJ, Müller A, Dorn S (2008) Specialized bees fail to develop on non-host pollen: do plants chemically protect their pollen. Ecology 89:795–804PubMedCrossRefGoogle Scholar
  48. Raguso RA (2004) Why are some floral nectars scented? Ecology 85:1486–1494CrossRefGoogle Scholar
  49. Raguso RA (2008) Wake up and smell the roses: the ecology and evolution of floral scent. Annu Rev Ecol Evol Syst 39:549–569CrossRefGoogle Scholar
  50. Robertson C (1925) Heterotropic bees. Ecology 6:412–436CrossRefGoogle Scholar
  51. Schiestl FP, Ayasse M (2001) Post-pollination emission of a repellent compound in a sexually deceptive orchid: a new mechanism for maximizing reproductive success? Oecologia 126:531–534CrossRefGoogle Scholar
  52. Schiestl FP, Ayasse M, Paulus HF, Löfstedt C, Hansson BS, Ibarra F, Francke W (1999) Orchid pollination by sexual swindle. Nature 399:421–422CrossRefGoogle Scholar
  53. Schiestl FP, Peakall R (2005) Two orchids attract different pollinators with the same floral odour compound: ecological and evolutionary implications. Funct Ecol 19:674–680CrossRefGoogle Scholar
  54. Schlindwein C, Wittmann D, Martins CF, Hamm A, Siqueira JA, Schiffler D, Machado IC (2005) Pollination of Campanula rapunculus L. (Campanulaceae): how much pollen flows into pollination and into reproduction of oligolectic pollinators? Plant Syst Evol 250:147–156CrossRefGoogle Scholar
  55. STATSOFT, I. 2004. STATISTICA (data analysis software system). Version version 7. www.statsoft.com.
  56. Svensson GP, Okamoto T, Kawakita A, Goto R, Kato M (2010) Chemical ecology of obligate pollination mutualisms: testing the ‘private channel’ hypothesis in the Breynia-Epicephala association. New Phytol 186:995–1004PubMedCrossRefGoogle Scholar
  57. Tengö J, Bergström G, Borgkarlson AK, Groth I, Francke W (1982) Volatile compounds from cephalic secretions of females in two cleptoparasite bee genera, Epeolus (Hym., Anthophoridae) and Coelioxys (Hym., Megachilidae). Z Naturforsch C 37:376–380Google Scholar
  58. Weiss MR (1991) Floral colour changes as cues for pollinators. Nature 35:227–229CrossRefGoogle Scholar
  59. Westrich P (1989) Die Wildbienen Baden-Württembergs: Spezieller Teil: Die Gattungen und Arten. Eugen Ulmer, Stuttgart, pp 437–972Google Scholar
  60. Williams NH (1983) Floral fragrances as cues in animal behavior. In: Jones EC, Little RJ (eds) Handbook of experimental pollination biology. Van Nostrand Reinhold, New York, pp 50–72Google Scholar
  61. Wright GA, Schiestl FP (2009) The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Funct Ecol 23:841–851CrossRefGoogle Scholar
  62. Zhang Q, Liu G, Schlyter F, Birgersson G, Anderson P, Valeur P (2001) Olfactory responses of Ips duplicatus from inner Mongolia, china to nonhost leaf and bark volatiles. J Chem Ecol 27:995–1009PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Paulo Milet-Pinheiro
    • 1
    • 2
  • Manfred Ayasse
    • 1
  • Heidi E. M. Dobson
    • 3
  • Clemens Schlindwein
    • 4
  • Wittko Francke
    • 5
  • Stefan Dötterl
    • 6
    • 7
  1. 1.Institute for Experimental BiologyUniversity of UlmUlmGermany
  2. 2.Laboratório de Ecologia Química, Departamento de Química FundamentalUniversidade Federal de PernambucoRecifeBrazil
  3. 3.Department of BiologyWhitman CollegeWalla WallaUSA
  4. 4.Departamento de BotânicaUniversidade Federal de Minas GeraisBelo HorizonteBrazil
  5. 5.Institut für Organische ChemieUniversity of HamburgHamburgGermany
  6. 6.Department of Plant SystematicUniversity of BayreuthBayreuthGermany
  7. 7.Organismic Biology, Plant EcologyUniversity of SalzburgSalzburgAustria

Personalised recommendations