Journal of Chemical Ecology

, Volume 31, Issue 11, pp 2581–2600 | Cite as

The Effect Of Pollination On Floral Fragrance in Thistles

  • Nina Theis
  • Robert A. Raguso


We investigated postpollination changes in fragrance composition and emission rates, as well as pollinator discrimination in hand-pollinated flower heads of two thistle species: Canada thistle (Cirsium arvense) and sandhill thistle (C. repandum). Following pollination, neither species emitted any novel compounds that could function as repellents. Scent emission rates declined in pollinated plants of both species by approximately 89% within 48 hr. This decline was evident in all 13 scent components of C. arvense. Apis mellifera, the dominant pollinator in the study population of C. arvense, was nearly three times more likely to visit an unpollinated rather than a pollinated flower head. A more complex pattern was observed for C. repandum, whose scent comprised 42 compounds. Quantities of aromatic and sesquiterpenoid volatiles declined after pollination, whereas two classes of scent compounds, fatty acid derivatives and monoterperpenoids, continued to be emitted. In C. repandum, discrimination against pollinated flower heads by Papilio palamedes (its primary pollinator) was not as marked. Unpollinated control plants of both species maintained moderate levels of scent production throughout this experiment, demonstrating that senescence and floral advertisement may be delayed until pollination has occurred. We expect postpollination changes in floral scent contribute to communication between plants with generalized pollinator spectra and their floral visitors. This study provides the first field study of such a phenomenon outside of orchids.

Key Words

Asteraceae Canada thistle Cirsium arvense Cirsium repandum dioecious fragrance herbivory pollination floral volatiles 



The authors thank the staff from Clemson University at the Belle Baruch Lab in Georgetown, SC, especially Alreda Grate and Jeffery Vernon. We also thank the staff at the Wallkill Fish & Wildlife National Refuge in Sussex, NJ. For the use of laboratory facilities in New Jersey, we thank Martha Hughes and Vicky Acosta at Sussex Community College, and David Slaymaker of William Patterson University. For field assistance, we thank Sarah Brice, Daniel McManus, Laurel Reid, and Eileen Rios. Many thanks are also due to Bill Dougherty and John Craig of Shimadzu Scientific, Inc., for technical expertise with GC-MS. For support at all stages of this work, we are grateful to Manuel Lerdau and Karsten Theis. This research was supported by an NSF Doctoral Dissertation Improvement Grant (DEB# 0206300), Sigma Xi Grants-in-Aid of Research, American Museum of Natural History Theodore Roosevelt Memorial Fund, US Department of Education GAANN Fellowship, Stony Brook University, Department of Ecology and Evolution, Sokal Travel Award, The Explorers Club Exploration Fund.


  1. Andersson, S., Nilsson, L. A., Groth, I., Bergström, G. 2002Floral scents in butterfly-pollinated plants: possible convergence in chemical compositionBot. J. Linn. Soc.140129153CrossRefGoogle Scholar
  2. Arditti, J. 1979Aspects of the physiology of orchidsWoolhouse, H. W. eds. Advances in Botanical Research 7Academic PressLondon422697Google Scholar
  3. Ashman, T.-L., Schoen, D. J. 1996Floral longevity: Fitness consequences and resource costsLloyd, D. G.Barrett, S. C. H. eds. Floral Biology Studies on Floral Evolution in Animal-Pollinated PlantsChapman & HallNew York112139Google Scholar
  4. Augspurger, C. K. 1980Mass flowering of a tropical shrub (Hybanthus prunifolius)—influence on pollinator attraction and movementEvolution34475488Google Scholar
  5. Baldwin, I. T., Preston, C., Euler, M., Gorham, D. 1997Patterns and consequences of benzyl acetone floral emissions from Nicotiana attenuata plantsJ. Chem. Ecol.2323272343CrossRefGoogle Scholar
  6. Bate, N. J., Rothstein, S. J. 1998C-6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genesPlant J.16561569CrossRefPubMedGoogle Scholar
  7. Bergström, G., Tengo, J. 1974Studies on natural odoriferous compounds. 9. Farnesyl esters and geranyl esters as main volatile constituents of secretion from dufours gland in 6 species of Andrena (Hymenoptera, Apidae)Chem. Scr.52838Google Scholar
  8. Bierzychudek, P., Eckhart, V. 1988Spatial segregation of the sexes of dioecious plantsAm. Nat.1323443CrossRefGoogle Scholar
  9. Borg-Karlson, A. K. 1990Chemical and ethological studies of pollination in the genus Ophrys (Orchidaceae)Phytochemistry2913591387CrossRefGoogle Scholar
  10. Casper, B. B., Lapine, T. R. 1984Changes in corolla color and other floral characteristics in Cryptantha humilis (Boraginaceae) cues to discourage pollinatorsEvolution38128141Google Scholar
  11. Chang, H. S., Jones, M. L., Banowetz, G. M., Clark, D. G. 2003Overproduction of cytokinins in petunia flowers transformed with P-SAG12-IPT delays corolla senescence and decreases sensitivity to ethylenePlant Physiol.13221742183CrossRefPubMedGoogle Scholar
  12. Delph, L. F., Lively, C. M. 1989The evolution of floral color change: Pollinator attraction versus physiological constraints in Fuchsia excorticataEvolution4312521262Google Scholar
  13. Dobson, H. E. M. 1994Floral volatiles in insect biologyBernays, E. A. eds. Insect–Plant InteractionsCRC PressBoca Raton4781Google Scholar
  14. Dornhaus, A., Chittka, L. 1999Insect behaviour—Evolutionary origins of bee dancesNature40138CrossRefGoogle Scholar
  15. Dötterl, S., Wolfe, L. M., Jürgens, A. 2005Qualitative and quantitative analyses of flower scent in Silene latifoliaPhytochemistry66203213CrossRefPubMedGoogle Scholar
  16. Dudareva, N., Pichersky, E. 2000Biochemical and molecular genetic aspects of floral scentsPlant Physiol.122627633CrossRefPubMedGoogle Scholar
  17. Dudareva, N., D'Auria, J. C., Nam, K. H., Raguso, R. A., Pichersky, E. 1998Acetyl-CoA: benzyl alcohol acetyltransferase—an enzyme involved in floral scent production in Clarkia breweriPlant J.14297304CrossRefPubMedGoogle Scholar
  18. Euler, M., Baldwin, I. T. 1996The chemistry of defense and apparency in the corollas of Nicotiana attenuataOecologia107102112CrossRefGoogle Scholar
  19. Galen, C., Butchart, B. 2003Ants in your plants: effects of nectar-thieves on pollen fertility and seed-siring capacity in the alpine wildflower, Polemonium viscosumOikos101521528CrossRefGoogle Scholar
  20. Gori, D. 1983Post-pollination phenomena and adaptive floral changesJones and, C. E.Little, R. J. eds. Handbook of Experimental Pollination BiologyScientific and Academic EditionsNew York3149Google Scholar
  21. Gori, D. F. 1989Floral color change in Lupinus argenteus (Fabaceae): Why should plants advertise the location of unrewarding flowers to pollinatorsEvolution43870881Google Scholar
  22. Grison-Pige, L., Salager, J. L., Hossaert-Mckey, M., Roy, J. 2001Carbon allocation to volatiles and other reproductive components in male Ficus carica (Moraceae)Am. J. Bot.8822142220Google Scholar
  23. Hatanaka, A. 1993The biogeneration of green odor by green leavesPhytochemistry3412011218CrossRefGoogle Scholar
  24. Honda, K., Ômura, H., Hayashi, N. 1998Identification of floral volatiles from Ligustrum japonicum that stimulate flower-visiting by cabbage butterfly, Pieris rapaeJ. Chem. Ecol.2421672180CrossRefGoogle Scholar
  25. Krupnick, G. A., Wheis, A. E., Campbell, D. R. 1999The consequences of floral herbivory for pollinator service to Isomeris arboreaEcology80125134Google Scholar
  26. Louda, S. M., Potvin, M. A. 1995Effect of inflorescence feeding insects on the demography and lifetime fitness of a native plantEcology76229245Google Scholar
  27. Loughrin, J. H., Hamilton-kemp, T. R., Burton, H. R., Andersen, R. A., Hildebrand, D. F. 1992Glycosidically bound volatile components of Nicotiana sylvestris and N. suaveolens flowersPhytochemistry3115371540CrossRefGoogle Scholar
  28. Marden, J. H. 1984Remote perception of floral nectar by bumblebeesOecologia64232240CrossRefGoogle Scholar
  29. Metcalf, R. L., Metcalf, E. R. 1992Plant Kairomones in Insect Ecology and ControlChapman & HallNew YorkGoogle Scholar
  30. Negre, F., Kish, C. M., Boatright, J., Underwood, B., Shibuya, K., Wagner, C., Clark, D. G., Dudareva, N. 2003Regulation of methylbenzoate emission after pollination in snapdragon and petunia flowersPlant Cell1529923006CrossRefPubMedGoogle Scholar
  31. Niesenbaum, R. A., Patselas, M. G., Weiner, S. D. 1999Does flower color change in Aster vimineus cue pollinators?Am. Midl. Nat.1415968Google Scholar
  32. Ômura, H., Honda, K., Hayashi, N. 1999Chemical and chromatic bases for preferential visiting by the cabbage butterfly, Pieris rapae, to rape flowersJ. Chem. Ecol.2518951906CrossRefGoogle Scholar
  33. Ômura, H., Honda, K., Hayashi, N. 2000Floral scent of Osmanthus fragrans discourages foraging behavior of cabbage butterfly, Pieris rapaeJ. Chem. Ecol.26655666CrossRefGoogle Scholar
  34. Peschken, D. P., Derby, J. L. 1992Effect of Urophora cardui (L) (Diptera, Tephritidae) and Ceutorhynchus litura (F) (Coleoptera, Curculionidae) on the weed Canada thistle, Cirsium arvense (L) ScopCan. Entomol.124145150Google Scholar
  35. Pichersky, E., Raguso, R. A., Lewinsohn, E., Croteau, R. 1994Floral scent production in Clarkia (Onagraceae). 1. Localization and developmental modulation of monoterpene emission and linalool synthase activityPlant Physiol.10615331540PubMedGoogle Scholar
  36. Primack, R. B. 1985Longevity of individual flowersAnnu. Rev. Ecol. Syst.161538CrossRefGoogle Scholar
  37. Proctor, M., Yeo, P., Lack, A. 1996The Natural History of PollinationTimber PressPortland479Google Scholar
  38. Radford, A. E., Ahles, H. E., Bell, C. R. 1968Manual of the Vascular Flora of the CarolinasThe University of North Carolina PressChapel HillGoogle Scholar
  39. Raguso, R. A. 2003Olfactory landscapes and deceptive pollination: Signal, noise and convergent evolution in floral scentBlomquist, G. J.Vogt, R. eds. Insect Pheromone Biochemistry and Molecular BiologyAcademic PressNew York631650Google Scholar
  40. Raguso, R. A., Levin, R. A., Foose, S. E., Holmberg, M. W., McDade, L. A. 2003Fragrance chemistry, nocturnal rhythms and pollination “syndromes” in NicotianaPhytochemistry63265284CrossRefPubMedGoogle Scholar
  41. Schiestl, F. P., Ayasse, M. 2001Post-pollination emission of a repellent compound in a sexually deceptive orchid: A new mechanism for maximising reproductive success?Oecologia126531534CrossRefGoogle Scholar
  42. Sokal, R. S., Rohlf, F. J. 1995Biometry3W. H. Freeman and Co.New YorkGoogle Scholar
  43. Strauss, S. Y. 1997Floral characters link herbivores, pollinators, and plant fitnessEcology7816401645Google Scholar
  44. Theis, N. 2003. Targeting pollinators and evading herbivores: Floral scent emission in two species of Cirsium. Ph.D. dissertation, State University of New York at Stony Brook.Google Scholar
  45. Tollsten, L. 1993A multivariate approach to post-pollination changes in the floral scent of Platanthera bifolia (Orchidaceae)Nord. J. Bot.13495499Google Scholar
  46. Tollsten, L., Bergström, J. 1989Variation and post-pollination changes in floral odors released by Platanthera bifolia (Orchidaceae)Nord. J. Bot.9359362Google Scholar
  47. Tollsten, L., Ovstedal, D. O. 1994Differentiation in floral scent chemistry among populations of Conopodium majus (Apiaceae)Nord. J. Bot.14361367Google Scholar
  48. Doorn, W. G. 1997Effects of pollination on floral attraction and longevityJ. Exp. Bot.4816151622CrossRefGoogle Scholar
  49. Staden, J., Cook, E., Noodén, L. D. 1988Cytokinins and senescenceNoodén, L. D.Leopold, A. C. eds. Senescence and Aging in PlantsAcademic PressSan Diego281328Google Scholar
  50. Wheiss, M. R. 1995Floral color-change—a widespread functional convergenceAm. J. Bot.82167185Google Scholar
  51. WHeiss, M. R. 1997Innate colour preferences and flexible colour learning in the pipevine swallowtailAnim. Behav.5310431052CrossRefGoogle Scholar
  52. WHeiss, M. R. 2001Vision and learning in some neglected pollinators: Beetles, flies, moths, and butterfliesChittka, L.Thomson, J. D. eds. Cognitive Ecology of PollinationCambridge University PressCambridge171190Google Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  1. 1.Department of Ecology and EvolutionState University of New YorkStony BrookUSA
  2. 2.Department of BiologyUniversity of South CarolinaColumbiaUSA
  3. 3.Department of Plant, Soil and Insect Sciences University of Massachusetts at AmherstAmherstUSA

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