Skip to main content

Advertisement

SpringerLink
Log in

The Key Role of 4-methyl-5-vinylthiazole in the Attraction of Scarab Beetle Pollinators: a Unique Olfactory Floral Signal Shared by Annonaceae and Araceae

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Cyclocephaline scarabs are specialised scent-driven pollinators, implicated with the reproductive success of several Neotropical plant taxa. Night-blooming flowers pollinated by these beetles are thermogenic and release intense fragrances synchronized to pollinator activity. However, data on floral scent composition within such mutualistic interactions are scarce, and the identity of behaviorally active compounds involved is largely unknown. We performed GC-MS analyses of floral scents of four species of Annona (magnoliids, Annonaceae) and Caladium bicolor (monocots, Araceae), and demonstrated the chemical basis for the attraction of their effective pollinators. 4-Methyl-5-vinylthiazole, a nitrogen and sulphur-containing heterocyclic compound previously unreported in flowers, was found as a prominent constituent in all studied species. Field biotests confirmed that it is highly attractive to both male and female beetles of three species of the genus Cyclocephala, pollinators of the studied plant taxa. The origin of 4-methyl-5-vinylthiazole in plants might be associated with the metabolism of thiamine (vitamin B1), and we hypothesize that the presence of this compound in unrelated lineages of angiosperms is either linked to selective expression of a plesiomorphic biosynthetic pathway or to parallel evolution.

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

Access this article

Log in via an institution

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

  • Armbruster, W. S., Keller, S., Matsuki, M., and Clausen, T. P. 1989. Pollination of Dalechampia magnoliifolia (Euphorbiaceae) by male euglossine bees. Am J. Bot. 76:1279–1285.

    Article  Google Scholar 

  • Azizian, M. F., Nelson, P. O., Thayumanavan, P., and Williamson, K. J. 2003. Environmental impact of highway construction and repair materials on surface and ground waters: Case study: crumb rubber asphalt concrete. Waste Manage. 23:719–728.

    Article  CAS  Google Scholar 

  • Azuma, H., Thien, L. B., and Kawano, S. 1999. Molecular phylogeny of Magnolia (Magnoliaceae) inferred from cpDNA sequences and evolutionary divergence of the floral scents. J. Plant Res. 112:291–306.

    Article  CAS  Google Scholar 

  • BEACH, J. H. 1982. Beetle pollination of Cyclanthus bipartitus (Cyclanthaceae). Am. J. Bot. 69:1074–1081.

    Article  Google Scholar 

  • Bengtsson, J. M., Wolde-Hawariat, Y., Khbaish, H., Negash, M., Jembere, B., Seyoum, E., Hansson, B. S., Larsson, M. C., and Hillbur, Y. 2009. Field attractants for Pachnoda interrupta selected by means of GC-EAD and single sensillum screening. J. Chem. Ecol. 35:1063–1076.

    Article  PubMed  CAS  Google Scholar 

  • Bernhardt, P. 2000. Convergent evolution and adaptive radiation of beetle-pollinated angiosperms. Plant Syst. Evol. 222:293–320.

    Article  Google Scholar 

  • Brodmann, J., Twele, R., Francke, W., Yi-Bo, L., Xi-Qiang, S., and Ayasse, M. 2009. Orchid mimics honey bee alarm pheromone in order to attract hornets for pollination. Curr. Biol. 19:1368–1372.

    Article  PubMed  CAS  Google Scholar 

  • CEPAGRI, 2012. Centro de Pesquisas Meteorológicas e Climáticas Aplicadas à Agricultura. <http://www.cpa.unicamp.br/>

  • Chen, C., Song, Q., Proffit, M., J-M, B., Li, Z., and Hossaert-Mckey, M. 2009. Private channel: a single unusual compound assures specific pollinator attraction in Ficus semicordata. Funct. Ecol. 23:941–950.

    Article  Google Scholar 

  • Chess, S. K. R., Raguso, R. A., and Lebuhn, G. 2008. Geographic divergence in floral morphology and scent in Linanthus dichotomus (Polemoniaceae). Am. J. Bot. 95:1652–1659.

    Article  PubMed  Google Scholar 

  • Dieringer, G., Cabrera, L., Lara, M., Loya, L., and Reyes-Castillo, P. 1999. Beetle pollination and floral thermogenicity in Magnolia tamaulipana. Int. J. Plant Sci. 160:64–71.

    Article  Google Scholar 

  • Dieringer, G. and Espinosa, S. J. E. 1994. Reproductive ecology of Magnolia schiedeana (Magnoliaceae), a threatened cloud forest tree species in Veracruz. Mexico. Bull. Torrey Bot. Club 121:154–159.

    Article  Google Scholar 

  • DOBSON, H. E. M. 2006. Relationship between floral fragrance composition and type of pollinator, pp. 147–198, in N. Dudareva and E. Pichersky (eds.), Biology of Floral Scent. CRC Press, Boca Raton.

    Chapter  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dötterl, S., Jürgens, A., Seifert, K., Laube, T., Weißbecker, B., and Schütz, S. 2006. Nursery pollination by a moth in Silene latifolia: the role of odours in eliciting antennal and behavioural responses. New Phytologist 169:707–718.

    Article  PubMed  Google Scholar 

  • Dötterl, S., Wolfe, L. M., and Jürgens, A. 2005. Qualitative and quantitative analyses of flower scent in Silene latifolia. Phytochemistry 66:203–213.

    Article  PubMed  Google Scholar 

  • Eltz, T., Roubik, D. W., and Lunau, K. 2005. Experience-dependent choices ensure species-specific fragrance accumulation in male orchid bees. Behav. Ecol. Sociobiol. 59:149–156.

    Article  Google Scholar 

  • Engel, K. H. and Tressl, R. 1991. Identification of new sulphur-containing volatiles in yellow (Passiflora edulis f. flavicarpa). J. Agric. Food Chem 39:2249–2252.

    Article  CAS  Google Scholar 

  • Ervik, F. and Knudsen, J. T. 2003. Water lilies and scarabs: faithful partners for 100 million years? Biol. J. Linn. Soc. 80:539–543.

    Article  Google Scholar 

  • Ervik, F., Tollsten, L., and Knudsen, J. T. 1999. Floral scent chemistry and pollination ecology in phytelephantoid palms (Arecaceae). Plant Syst. Evol. 217:279–297.

    Article  Google Scholar 

  • Faegri, K. and van der Pijl, L. 1979. The Principles of Pollination Ecology (2nd Edition). Pergamon Press, New York.

    Google Scholar 

  • FISCHER, N., Hammerschmidt, F.-J., and Brunke, E.-J. 1995. Analytical investigations of the flavor of cupuaçu (Theobroma grandiflorum Spreng.), pp. 8–20, in R. L. Rouseff and M. M. Leahy (eds.), Fruit Flavors: Biogenesis, Characterization, and Authentication (ACS Symposium Series Vol. 596). ACS Publications, Washington.

    Chapter  Google Scholar 

  • Gibernau, M., Barabé, D., Labat, D., Cerdan, P., and Dejean, A. 2003. Reproductive biology of Montrichardia arborescens (Araceae) in French Guiana. J. Trop. Ecol. 19:103–107.

    Article  Google Scholar 

  • Gibernau, M., Barabé, D., Cerdan, P., and Dejean, A. 1999. Beetle pollination of Philodendron solimoesense (Araceae) in French Guiana. Int. J. Plant Sci. 160:1135–1143.

    Article  PubMed  Google Scholar 

  • Goeke, A. 2002. Sulfur-containing odorants in fragrance chemistry. Sulfur Reports 23:243–278.

    CAS  Google Scholar 

  • GOODRICH, K. R. and Raguso, R. A. 2009. The olfactory component of floral display in Asimina and Deeringothamnus (Annonaceae). New Phytologist 183:457–469.

    Article  PubMed  CAS  Google Scholar 

  • Gottsberger, G. 1986. Some pollination strategies in neotropical savannas and forests. Plant Syst. Evol. 152:29–45.

    Article  Google Scholar 

  • Gottsberger, G. 1989. Beetle pollination and flowering rhythm of Annona spp. (Annonaceae) in Brazil. Plant Syst. Evol. 167:165–187.

    Google Scholar 

  • Gottsberger, G. 1990. Flowers and beetles in the South American tropics. Bot. Acta 103:360–365.

    Google Scholar 

  • Gottsberger, G. and Silberbauer-Gottsberger, I. 1991. Olfactory and visual attraction of Erioscelis emarginata (Cyclocephalini, Dynastinae) to the inflorescences of Philodendron selloum (Araceae). Biotropica 23:23–28.

    Article  Google Scholar 

  • GOTTSBERGER, G., and Silberbauer-G2, I. 2006. Life in the Cerrado, a South American Seasonal Ecosystem. Vol. I. Origin, Structure, Dynamics and Plant Use. Reta, Ulm.

  • Gottsberger, G., Silberbauer-Gottsberger, I., Seymour, R. S., and Dötterl, S. 2012. Pollination ecology of Magnolia ovata may explain the overall large flower size of the genus. Flora 207:107–118.

    Article  Google Scholar 

  • ITEP, 2012. Instituto de Tecnologia de Pernambuco–Laboratorio de Meteorologia de Pernambuco. <http://www.itep.br/LAMEPE.asp>

  • Johnson, S. D. and Jürgens, A. 2010. Convergent evolution of carrion and faecal scent mimicry in fly-pollinated angiosperm flowers and a stinkhorn fungus. S. Afr. J. Bot. 76:796–807.

    Article  CAS  Google Scholar 

  • Jürgens, A., Dötterl, S., and Meve, U. 2006. The chemical nature of fetid floral odors in stapeliads (Apocynaceae-Asclepiadoideae-Ceropegieae). New Phytologist 172:452–468.

    Article  PubMed  Google Scholar 

  • Jurgenson, C. T., Begley, T. P., and Ealick, S. E. 2009. The structural and biochemical foundations of thiamin biosynthesis. Annu. Rev. Biochem. 78:569–603.

    Article  PubMed  CAS  Google Scholar 

  • Kaiser, R. 1993. The Scent of Orchids: Olfactory and Chemical Investigations, 1st ed. Elsevier Science, Amsterdam.

    Google Scholar 

  • Kaiser, R. and Tollsten, L. 1995. An introduction to the scent of cacti. Flavour Fragr. J. 10:153–164.

    Article  CAS  Google Scholar 

  • Knudsen, J. T., Eriksson, R., Gershenzon, J., and Ståhl, B. 2006. Diversity and distribution of floral scent. Bot. Rev. 72:1–120.

    Article  Google Scholar 

  • Knudsen, J. T. and Tollsten, L. 1995. Floral scent in bat-pollinated plants - a case of convergent evolution. Bot. J. Linn. Soc. 119:45–57.

    Article  Google Scholar 

  • Maga, J. A. 1975. The role of sulfur compounds in food flavor. part I: Thiazoles. Crit. Rev. Food Sci 6:153–176.

    Article  CAS  Google Scholar 

  • MAIA, A. C. D. and Schlindwein, C. 2006. Caladium bicolor (Araceae) and Cyclocephala celata (Coleoptera, Dynastinae): a well-established pollination system in the northern Atlantic rainforest of Pernambuco, Brazil. Plant Biol. 8:529–534.

    Article  PubMed  CAS  Google Scholar 

  • Maia, A. C. D., Schlindwein, C., Navarro, D. M. A. F., and Gibernau, M. 2010. Pollination of Philodendron acutatum (Araceae) in the Atlantic Forest of northeastern Brazil: a single scarab beetle species guarantees high fruit set. Int. J. Plant Sci. 171:740–748.

    Article  Google Scholar 

  • Peakall, R., Ebert, D., Poldy, J., Barrow, R. A., Francke, W., Bower, C. C., and Schiestl, F. P. 2010. Pollinator specificity, floral odour chemistry and the phylogeny of Australian sexually deceptive Chiloglottis orchids: implications for pollinator-driven speciation. New Phytologist 188:437–450.

    Article  PubMed  CAS  Google Scholar 

  • Pichersky, E. and Lewinsohn, E. 2011. Convergent evolution in plant specialized metabolism. Annu. Rev. Plant Biol. 62:549–566.

    Article  PubMed  CAS  Google Scholar 

  • Pichersky, E., Noel, J. P., and Dudareva, N. 2006. Biosynthesis of plant volatiles: nature’s diversity and ingenuity. Science 311:808–811.

    Article  PubMed  CAS  Google Scholar 

  • Pino, J. A., Aguero, J., and Marbot, R. 2001. Volatile components of soursop (Annona muricata). J. Essent. Oil Res. 13:140–141.

    Article  CAS  Google Scholar 

  • Plepys, D., Ibarra, F., and Löfstedt, C. 2002. Volatiles from flowers of Platanthera bifolia (Orchidaceae) attractive to the silver Y moth, Autographa gamma (Lepidoptera: Noctuidae). Oikos 99:69–74.

    Article  CAS  Google Scholar 

  • RAGUSO, R. A. 2001. Floral scent, olfaction, and scent-driven foraging behavior, pp. 83–105, in L. Chittka and J. D. Thomson (eds.), Cognitive Ecology of Pollination. Cambridge University Press, Cambridge.

    Chapter  Google Scholar 

  • RAGUSO, R. A. 2008. Wake up and smell the roses: the ecology and evolution of floral scent. Annu. Rev. Ecol. Evol. Syst. 39:549–569.

    Article  Google Scholar 

  • Raguso, R. A. and Pellmyr, O. 1998. Dynamic headspace analysis of floral volatiles: a comparison of methods. Oikos 81:238–254.

    Article  CAS  Google Scholar 

  • Schatz, G. E. 1990. Some aspects of pollination biology in Central American forests, pp. 69–84, in K. S. Bawa and M. Hadley (eds.), Reproductive Ecology of Tropical Forest Plants. UNESCO/Parthenon, Paris.

    Google Scholar 

  • SCHIESTL, F. P. 2010. The evolution of floral scent and insect chemical communication. Ecol. Lett. 13:643–656.

    Article  PubMed  Google Scholar 

  • Schiestl, F. P., Ayasse, M., Paulus, H. F., Löfstedt, C., Hansson, B. S., Ibarra, F., and Francke, W. 1999. Orchid pollination by sexual swindle. Nature 399:421–422.

    Article  CAS  Google Scholar 

  • Schiestl, F. P., Peakall, R., Mant, J. G., Ibarra, F., Schulz, C., Franke, S., and Francke, W. 2003. The chemistry of sexual deception in an orchid-wasp pollination system. Science 302:437–438.

    Article  PubMed  CAS  Google Scholar 

  • Schultz, K., Kaiser, R., and KNUDSEN, J. T. 1999. Cyclanthone and derivatives, new natural products in the flower scent of Cyclanthus bipartitus Poit. Flavour Fragr. J. 14:185–190.

    Article  CAS  Google Scholar 

  • Schwab, W., Davidovich-Rikanati, R., and Lewinsohn, E. 2008. Biosynthesis of plant-derived flavor compounds. Plant J. 54:712–732.

    Article  PubMed  CAS  Google Scholar 

  • Schwerdtfeger, M., Gerlach, G., and Kaiser, R. 2002. Anthecology in the neotropical genus Anthurium (Araceae): a preliminary report. Selbyana 23:258–267.

    Google Scholar 

  • Seymour, R. S., White, C. R., and Gibernau, M. 2003. Heat reward for insect pollinators. Nature 426:243–244.

    Article  PubMed  CAS  Google Scholar 

  • Shuttleworth, A. and JOHNSON, S. D. 2010. The missing stink: sulphur compounds can mediate a shift between fly and wasp pollination systems. Proc. R. Soc. B 277:2811–2819.

    Article  PubMed  CAS  Google Scholar 

  • Stensmyr, M. C., Urru, I., Collu, I., Celander, M., Hansson, B. S., and Angioy, A. M. 2002. Rotting smell of dead-horse arum florets - These blooms chemically fool flies into pollinating them. Nature 420:625–626.

    Article  PubMed  CAS  Google Scholar 

  • Teichert, H., Dötterl, S., Zimma, B., Ayasse, M., and Gottsberger, G. 2009. Perfume-collecting male euglossine bees as pollinators of a basal angiosperm: the case of Unonopsis stipitata (Annonaceae). Plant Biol. 11:29–37.

    Article  PubMed  CAS  Google Scholar 

  • Valdes, H. and ZAROR, C. A. 2006. Heterogeneous and homogeneous catalytic ozonation of benzothiazole promoted by activated carbon: kinetic approach. Chemosphere 65:1131–1136.

    Article  PubMed  CAS  Google Scholar 

  • von Helversen, O., Winkler, L., and Bestmann, H. J. 2000. Sulphur-containing "perfumes" attract flower-visiting bats. J. Comp. Physiol. A 186:143–153.

    Article  Google Scholar 

  • Whitten, W. M., Williams, N. H., Armbruster, W. S., and Battiste, M. A. 1986. Carvone oxide: an example of convergent evolution in euglossine pollinated plants. Syst. Bot. 11:222–228.

    Article  Google Scholar 

  • Wong, K. C. and Khoo, K. H. 1993. Volatile components of Malaysian Annona fruits. Flavour Fragr. J. 8:5–10.

    Article  CAS  Google Scholar 

  • Yu, T. H., Wu, C. M., and Liou, Y. C. 1989. Volatile compounds from garlic. J. Agric. Food Chem. 37:725–730.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Paschoal Coelho Grossi, Brett Ratcliffe, and Antônio Carlos Webber for species identification; and Roger Seymour, Kyle Dexter, Cecília Meira and three anonymous reviewers for proofreading and valuable suggestions. This work was partly supported by grants from CAPES, CNPq and BMBF.

Author information

Authors and Affiliations

  1. Departamento de Química Fundamental, Universidade Federal de Pernambuco, Recife, 50740-560, Brazil

    Artur Campos Dália Maia & Daniela Maria do Amaral Ferraz Navarro

  2. Department of Plant Systematics, University of Bayreuth, Bayreuth, 95440, Germany

    Stefan Dötterl

  3. Givaudan Fragrance Research, Dübendorf, 8600, Switzerland

    Roman Kaiser

  4. Botanical Garden and Herbarium, University of Ulm, Ulm, 89081, Germany

    Ilse Silberbauer-Gottsberger & Gerhard Gottsberger

  5. Institute of Systematic Botany and Ecology, University of Ulm, Ulm, 89081, Germany

    Holger Teichert

  6. CNRS—Ecofog (UMR 8172), Campus Agronomique BP 316, 97379, Kourou cedex, France

    Marc Gibernau

  7. Departamento de Botânica, Universidade Federal de Minas Gerais, Belo Horizonte, 31270-901, Brazil

    Clemens Schlindwein

Authors
  1. Artur Campos Dália Maia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stefan Dötterl
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Roman Kaiser
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ilse Silberbauer-Gottsberger
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Holger Teichert
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marc Gibernau
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Daniela Maria do Amaral Ferraz Navarro
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Clemens Schlindwein
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Gerhard Gottsberger
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Artur Campos Dália Maia.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maia, A.C.D., Dötterl, S., Kaiser, R. et al. The Key Role of 4-methyl-5-vinylthiazole in the Attraction of Scarab Beetle Pollinators: a Unique Olfactory Floral Signal Shared by Annonaceae and Araceae. J Chem Ecol 38, 1072–1080 (2012). https://doi.org/10.1007/s10886-012-0173-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-012-0173-z

Keywords

Search

Navigation