Skip to main content
Log in

An arthropod deterrent attracts specialised bees to their host plants

  • Plant-Animal interactions - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Many bee species are adapted to just a few specific plants in order to collect pollen (oligolecty). To reproduce successfully, it is important for oligolectic bees to find and recognise the specific host flowers. In this study, we investigated the role of floral volatiles used by an oligolectic bee to recognise its host plants. We compared the attractiveness of natural and synthetic scent samples of host flowers to foraging-naïve and -experienced Hoplitis adunca (Megachilidae) bees that are specialised on Echium and Pontechium (Boraginaceae) plants. The investigations showed that naïve H. adunca females are attracted to 1,4-benzoquinone. During their lifetime, bees learn additional floral cues while foraging on host flowers. In contrast to naïve ones, experienced H. adunca females use, in addition to 1,4-benzoquinone, other compounds to recognise their host plants. 1,4-Benzoquinone is an uncommon floral compound only known from the host plants of H. adunca, and is therefore ideally suited to be used as a plant-specific recognition cue. Several arthropods use this compound to deter insect predators. Therefore, 1,4-benzoquinone as an attractant in Echium flowers may have evolved from a primary function as a defensive compound against insect herbivores.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectrometry. Allured, Carol Stream

    Google Scholar 

  • Ayasse M (2006) Floral scent and pollinator attraction in sexually deceptive orchids. In: Dudareva N, Pichersky E (eds) Biology of floral scent. CRC, Boca Raton, pp 219–242

    Chapter  Google Scholar 

  • 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 Lond B 270:517–522. doi:10.1098/rspb.2002.2271

    Article  CAS  Google Scholar 

  • Ayasse M, Schiestl FP, Paulus HF, Löfstedt C, Hansson B, Ibarra F, Francke W (2000) Evolution of reproductive strategies in the sexually deceptive orchid Ophrys sphegodes: how does flower-specific variation of odor signals influence reproductive success? Evolution 54:1995–2006. doi:10.1554/0014-3820(2000)054[1995:EORSIT]2.0.CO;2

    PubMed  CAS  Google Scholar 

  • Ayasse M, Stökl J, Francke W (2011) Chemical ecology and speciation in sexually deceptive orchids. Phytochemistry doi:10.1016/j.phytochem.2011.03.023

  • Blum MS (1981) 1, 4-Quinones and hydroquinones. In: Blum MS (ed) Chemical defenses of arthropods. Academic, New York, pp 183–205

    Google Scholar 

  • Brodmann J, Twele R, Francke W, Hoelzler G, Zhang Q-H, Ayasse M (2008) Orchids mimic green-leaf volatiles to attract prey-hunting wasps for pollination. Curr Biol 18:740–744. doi:10.1016/j.cub.2008.04.040

    Article  PubMed  CAS  Google Scholar 

  • Brodmann J, Twele R, Francke W, Yi-bo L, Xi-qiang S, Ayasse M (2009) Orchid mimics honey bee alarm pheromone in order to attract hornets for pollination. Curr Biol 19:1368–1372. doi:10.1016/j.cub.2009.06.067

    Article  PubMed  CAS  Google Scholar 

  • 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 76:788–795. doi:10.1016/j.sajb.2010.08.003

    Article  CAS  Google Scholar 

  • Burger H, Dötterl S, Ayasse M (2008) Importance of olfactory and visual cues of Echium for host plant finding of the oligolectic bee Osmia adunca (Megachilidae). Mitt Dtsch Ges Allg Angew Entomol 16:163–166

    Google Scholar 

  • Burger H, Dötterl S, Ayasse M (2010b) Host plant finding and recognition by visual and olfactory floral cues in an oligolectic bee. Funct Ecol 24:1234–1240. doi:10.1111/j.1365-2435.2010.01744.x

    Article  Google Scholar 

  • Chambliss OL, Jones CM (1966) Chemical and genetic basis for insect resistance in cucurbits. Proc Am Soc Hort Sci 89:394–405

    CAS  Google Scholar 

  • Cane JH, Sipes SD (2006) Characterizing floral specialization by bees: analytical methods and a revised lexicon for oligolecty. In: Waser NM, Ollerton J (eds) Plant–pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago, pp 99–122

    Google Scholar 

  • Chen C, Song Q, Proffit M, Bessière J-M, Li Z, Hossaert-McKey M (2009) Private channel: a single unusual compound assures specific pollinator attraction in Ficus semicordata. Funct Ecol 23:941–950. doi:10.1111/j.1365-2435.2009.01622.x

    Article  Google Scholar 

  • Corbet SA (1978) Bee visits and the nectar of Echium vulgare L. and Sinapis alba L. Ecol Entomol 3:25–37. doi:10.1111/j.1365-2311.1978.tb00900.x

    Article  Google Scholar 

  • Corey EJ, Schmidt G (1979) Useful procedures for the oxidation of alcohols involving pyridinium dichromate in approtic media. Tetrahedron Lett 20:399–402. doi:10.1016/S0040-4039(01)93515-4

    Article  Google Scholar 

  • Da Costa CP, Jones CM (1971) Cucumber beetle resistance and mite susceptibility controlled by the bitter gene in Cucumis sativus L. Science 172:1145–1146. doi:10.1126/science.172.3988.1145

    Article  PubMed  CAS  Google Scholar 

  • Dobson HEM (1987) Role of flower and pollen aromas in host plant recognition by solitary bees. Oecologia 72:618–623. doi:10.1007/BF00378991

    Article  Google Scholar 

  • Dobson HEM (2006) Relationship between floral fragrance composition and type of pollinator. In: Dudareva N, Pichersky E (eds) Biology of floral scent. CRC, Boca Raton, pp 147–198

    Chapter  Google Scholar 

  • Dobson HEM, Bergström G (2000) The ecology and evolution of pollen odors. Plant Syst Evol 222:63–87. doi:10.1007/BF00984096

    Article  CAS  Google Scholar 

  • Dobson HEM, Danielson EM, van Wesep ID (1999) Pollen odor chemicals as modulators of bumble bee foraging on Rosa rugosa Thunb. (Rosaceae). Plant Species Biol 14:153–166. doi:10.1046/j.1442-1984.1999.00020.x

    Article  Google Scholar 

  • 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 31:2993–2998. doi:10.1007/s10886-005-9152-y

    Article  PubMed  Google Scholar 

  • Dötterl S, Jürgens A (2005) Spatial fragrance patterns in flowers of Silene latifolia: lilac compounds as olfactory nectar guides? Plant Syst Evol 255:99–109. doi:10.1007/s00606-005-0344-2

    Article  Google Scholar 

  • 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 169:707–718. doi:10.1111/j.1469-8137.2005.01509.x

    Article  PubMed  Google Scholar 

  • Dötterl S, Schäffler I (2007) Flower scent of floral oil-producing Lysimachia punctata as attractant for the oil-bee Macropis fulvipes. J Chem Ecol 33:441–445. doi:10.1007/s10886-006-9237-2

    Article  PubMed  Google Scholar 

  • Dötterl S, Vereecken NJ (2010) The chemical ecology and evolution of bee–flower interactions: a review and perspectives. Can J Zool 88:668–697. doi:10.1139/Z10-031

    Article  Google Scholar 

  • Dötterl S, Wolfe LM, Jürgens A (2005b) Qualitative and quantitative analyses of flower scent in Silene latifolia. Phytochemistry 66:203–213. doi:10.1016/j.phytochem.2004.12.002

    Article  PubMed  Google Scholar 

  • Giurfa M, Núñez J, Chittka L, Menzel R (1995) Colour preferences of flower-naive honeybees. J Comp Physiol A Sens Neural Behav Physiol 177:247–259. doi:10.1007/BF00192415

    Article  Google Scholar 

  • Hegnauer R (1992) Chemotaxonomie der Pflanzen. Birkhäuser, Basel

    Google Scholar 

  • Jetter R (2006) Examination of the process involved in the emission of scent volatiles from flowers. In: Dudareva N, Pichersky E (eds) Biology of floral scent. CRC, Boca Raton, pp 125–144

    Chapter  Google Scholar 

  • Joulain D, König WA (1998) The atlas of spectral data of sesquiterpene hydrocarbons. EB, Hamburg

    Google Scholar 

  • Kessler A, Halitschke R (2009) Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predections and case study. Funct Ecol 23:901–912. doi:10.1111/j.1365-2435.2009.01639.x

    Article  Google Scholar 

  • Klinkhamer PGL, de Jong TJ, Wesselingh RA (1991) Implications of differences between hermaphrodite and female flowers for attractiveness to pollinators and seed production. Neth J Zool 41:130–143. doi:10.1163/156854291X00081

    Article  Google Scholar 

  • Knudsen JT, Eriksson R, Gershenzon J, Stahl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120. doi:10.1663/0006-8101(2006)72[1:DADOFS]2.0.CO;2

    Article  Google Scholar 

  • 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. University of Chicago Press, Chicago, pp 69–98

    Google Scholar 

  • Müller A, Diener S, Schnyder S, Stutz K, Sedivy C, Dorn S (2006) Quantitative pollen requirements of solitary bees: implications for bee conservation and the evolution of bee-flower relationships. Biol Conserv 130:604–615. doi:10.1016/j.biocon.2006.01.023

    Article  Google Scholar 

  • Müller A, Kuhlmann M (2008) Pollen hosts of western palaearctic bees of the genus Colletes (Hymenoptera: Colletidae): the Asteraceae paradox. Biol J Linn Soc 95:719–733. doi:10.1111/j.1095-8312.2008.01113.x

    Article  Google Scholar 

  • Norris DM (1970) Quinol stimulation and quinone deterrency of gustation by Scolytus multistriatus (Coleoptera: Scolytidae). Ann Entomol Soc Am 63:476–478

    CAS  Google Scholar 

  • Pellmyr O, Thien L (1986) Insect reproduction and floral fragrances: keys to the evolution of the angiosperms? Taxon 35:76–85

    Google Scholar 

  • Raguso RA (2008a) Start making scents: the challenge of integrating chemistry into pollination ecology. Entomol Exp Appl 128:196–207. doi:10.1111/j.1570-7458.2008.00683.x

    Article  CAS  Google Scholar 

  • Raguso RA (2008b) Wake up and smell the roses: the ecology and evolution of floral scent. Annu Rev Ecol Evol Syst 39:549–569. doi:10.1146/annurev.ecolsys.38.091206.095601

    Article  Google Scholar 

  • Reese JC, Beck SD (1976) Effects of allelochemics on the Black Cutworm, Agrotis ipsilon; effects of p-benzoquinone, hydroquinone, and duroquinone on larval growth, development, and utilization of food. Ann Entomol Soc Am 69:59–67

    CAS  Google Scholar 

  • Robertson C (1925) Heterotropic bees. Ecology 6:412–436. doi:10.2307/1929107

    Article  Google Scholar 

  • Schaefer HM, Schaefer V, Levey DJ (2004) How plant-animal interactions signal new insights in communication. Trends Ecol Evol 19:577–584. doi:10.1016/j.tree.2004.08.003

    Article  Google Scholar 

  • Schiestl FP (2005) On the success of a swindle: pollination by deception in orchids. Naturwissenschaften 92:255–264. doi:10.1007/s00114-005-0636-y

    Article  PubMed  CAS  Google Scholar 

  • Schiestl FP (2010) The evolution of floral scent and insect chemical communication. Ecol Lett 13:643–656. doi:10.1111/j.1461-0248.2010.01451.x

    Article  PubMed  Google Scholar 

  • Schiestl FP, Ayasse M (2001) Post-pollination emission of a repellent compound in a sexually deceptive orchid: a new mechanism for maximising reproductive success? Oecologia 126:531–534. doi:10.1007/s004420000552

    Article  Google Scholar 

  • Schiestl FP, Ayasse M, Paulus HF, Löfstedt C, Hansson BS, Ibarra F, Francke W (1999) Orchid pollination by sexual swindle. Nature 399:421–422. doi:10.1038/20829

    Article  CAS  Google Scholar 

  • Schulz S, Gross J, Hilker M (1997) Origin of the defensive secretion of the leaf beetle Chrysomela lapponica. Tetrahedron 53:9203–9212. doi:10.1016/S0040-4020(97)00618-2

    Article  CAS  Google Scholar 

  • da Silva UF, Borbac EL, Semir J, Marsaioli AJ (1999) A simple solid injection device for the analyses of Bulbophyllum (Orchidaceae) volatiles. Phytochemistry 50:31–34. doi:10.1016/S0031-9422(98)00459-2

    Article  Google Scholar 

  • Svensson GP, Okamoto T, Kawakita A, Goto R, Kato M (2010) Chemical ecology of obligate pollination mutualisms: testing the ‘private channel’ hypothesis in the BreyniaEpicephala association. New Phytol 186:995–1004. doi:10.1111/j.1469-8137.2010.03227.x

    Article  PubMed  CAS  Google Scholar 

  • Thomson JD (2003) When it is mutualism? Am Nat 162:S1–S9. doi:10.1086/378683

    Article  PubMed  Google Scholar 

  • Thomson RH (1997) Naturally occuring quinones IV. Chapman and Hall, London

    Google Scholar 

  • Watanabe N, Watanabe S, Nakajima R, Moon J-H, Shimokihara K, Inagaki J, Etoh H, Asai T, Sakata K, Ina K (1993) Formation of flower fragrance compounds from their precursors by enzymic action during flower opening. Biosci Biotech Biochem 57:1101–1106

    Article  CAS  Google Scholar 

  • Whitehead MR, Peakall R (2009) Integrating floral scent, pollination ecology and population genetics. Funct Ecol 23:863–874. doi:10.1111/j.1365-2435.2009.01620.x

    Article  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge Paulo Milet-Pinheiro for his critical reading, David Ponting for his linguistic advice, and two anonymous reviewers gave valuable comments on earlier versions of this manuscript. H.B. wishes to thank the Studienstiftung des deutschen Volkes for financial support. All experiments comply with the current laws of the country in which they were performed: in this case, Germany.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Manfred Ayasse.

Additional information

Communicated by Diethart Matthies.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Burger, H., Dötterl, S., Häberlein, C.M. et al. An arthropod deterrent attracts specialised bees to their host plants. Oecologia 168, 727–736 (2012). https://doi.org/10.1007/s00442-011-2136-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-011-2136-4

Keywords

Navigation