The Effect Of Pollination On Floral Fragrance in Thistles
Article First Online: 25 October 2005 Received: 21 January 2005 Revised: 25 May 2005 Accepted: 30 June 2005 Abstract
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 References Andersson, S., Nilsson, L. A., Groth, I., Bergström, G. 2002 Floral scents in butterfly-pollinated plants: possible convergence in chemical composition Bot. J. Linn. Soc. 140 129 153 CrossRef Google Scholar Arditti, J. 1979 Aspects of the physiology of orchids Woolhouse, H. W. eds. Advances in Botanical Research 7 Academic Press London 422 697 Google Scholar Ashman, T.-L., Schoen, D. J. 1996 Floral longevity: Fitness consequences and resource costs Lloyd, D. G. Barrett, S. C. H. eds. Floral Biology Studies on Floral Evolution in Animal-Pollinated Plants Chapman & Hall New York 112 139 Google Scholar Augspurger, C. K. 1980 Mass flowering of a tropical shrub ( Hybanthus prunifolius)—influence on pollinator attraction and movement Evolution 34 475 488 Google Scholar Baldwin, I. T., Preston, C., Euler, M., Gorham, D. 1997 Patterns and consequences of benzyl acetone floral emissions from Nicotiana attenuata plants J. Chem. Ecol. 23 2327 2343 CrossRef Google Scholar Bate, N. J., Rothstein, S. J. 1998 C-6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes Plant J. 16 561 569 CrossRef PubMed Google Scholar Bergström, G., Tengo, J. 1974 Studies 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. 5 28 38 Google Scholar Bierzychudek, P., Eckhart, V. 1988 Spatial segregation of the sexes of dioecious plants Am. Nat. 132 34 43 CrossRef Google Scholar Borg-Karlson, A. K. 1990 Chemical and ethological studies of pollination in the genus Ophrys (Orchidaceae) Phytochemistry 29 1359 1387 CrossRef Google Scholar Casper, B. B., Lapine, T. R. 1984 Changes in corolla color and other floral characteristics in Cryptantha humilis (Boraginaceae) cues to discourage pollinators Evolution 38 128 141 Google Scholar Chang, H. S., Jones, M. L., Banowetz, G. M., Clark, D. G. 2003 Overproduction of cytokinins in petunia flowers transformed with P-SAG12-IPT delays corolla senescence and decreases sensitivity to ethylene Plant Physiol. 132 2174 2183 CrossRef PubMed Google Scholar Delph, L. F., Lively, C. M. 1989 The evolution of floral color change: Pollinator attraction versus physiological constraints in Fuchsia excorticata Evolution 43 1252 1262 Google Scholar Dobson, H. E. M. 1994 Floral volatiles in insect biology Bernays, E. A. eds. Insect–Plant Interactions CRC Press Boca Raton 47 81 Google Scholar Dornhaus, A., Chittka, L. 1999 Insect behaviour—Evolutionary origins of bee dances Nature 401 38 CrossRef Google Scholar Dötterl, S., Wolfe, L. M., Jürgens, A. 2005 Qualitative and quantitative analyses of flower scent in Silene latifolia Phytochemistry 66 203 213 CrossRef PubMed Google Scholar Dudareva, N., Pichersky, E. 2000 Biochemical and molecular genetic aspects of floral scents Plant Physiol. 122 627 633 CrossRef PubMed Google Scholar Dudareva, N., D'Auria, J. C., Nam, K. H., Raguso, R. A., Pichersky, E. 1998 Acetyl-CoA: benzyl alcohol acetyltransferase—an enzyme involved in floral scent production in Clarkia breweri Plant J. 14 297 304 CrossRef PubMed Google Scholar Euler, M., Baldwin, I. T. 1996 The chemistry of defense and apparency in the corollas of Nicotiana attenuata Oecologia 107 102 112 CrossRef Google Scholar Galen, C., Butchart, B. 2003 Ants in your plants: effects of nectar-thieves on pollen fertility and seed-siring capacity in the alpine wildflower, Polemonium viscosum Oikos 101 521 528 CrossRef Google Scholar Gori, D. 1983 Post-pollination phenomena and adaptive floral changes Jones and, C. E. Little, R. J. eds. Handbook of Experimental Pollination Biology Scientific and Academic Editions New York 31 49 Google Scholar Gori, D. F. 1989 Floral color change in Lupinus argenteus (Fabaceae): Why should plants advertise the location of unrewarding flowers to pollinators Evolution 43 870 881 Google Scholar Grison-Pige, L., Salager, J. L., Hossaert-Mckey, M., Roy, J. 2001 Carbon allocation to volatiles and other reproductive components in male Ficus carica (Moraceae) Am. J. Bot. 88 2214 2220 Google Scholar Hatanaka, A. 1993 The biogeneration of green odor by green leaves Phytochemistry 34 1201 1218 CrossRef Google Scholar Honda, K., Ômura, H., Hayashi, N. 1998 Identification of floral volatiles from Ligustrum japonicum that stimulate flower-visiting by cabbage butterfly, Pieris rapae J. Chem. Ecol. 24 2167 2180 CrossRef Google Scholar Krupnick, G. A., Wheis, A. E., Campbell, D. R. 1999 The consequences of floral herbivory for pollinator service to Isomeris arborea Ecology 80 125 134 Google Scholar Louda, S. M., Potvin, M. A. 1995 Effect of inflorescence feeding insects on the demography and lifetime fitness of a native plant Ecology 76 229 245 Google Scholar Loughrin, J. H., Hamilton-kemp, T. R., Burton, H. R., Andersen, R. A., Hildebrand, D. F. 1992 Glycosidically bound volatile components of Nicotiana sylvestris and N. suaveolens flowers Phytochemistry 31 1537 1540 CrossRef Google Scholar Marden, J. H. 1984 Remote perception of floral nectar by bumblebees Oecologia 64 232 240 CrossRef Google Scholar Metcalf, R. L., Metcalf, E. R. 1992Plant Kairomones in Insect Ecology and Control Chapman & Hall New York Google Scholar Negre, F., Kish, C. M., Boatright, J., Underwood, B., Shibuya, K., Wagner, C., Clark, D. G., Dudareva, N. 2003 Regulation of methylbenzoate emission after pollination in snapdragon and petunia flowers Plant Cell 15 2992 3006 CrossRef PubMed Google Scholar Niesenbaum, R. A., Patselas, M. G., Weiner, S. D. 1999 Does flower color change in Aster vimineus cue pollinators? Am. Midl. Nat. 141 59 68 Google Scholar Ômura, H., Honda, K., Hayashi, N. 1999 Chemical and chromatic bases for preferential visiting by the cabbage butterfly, Pieris rapae, to rape flowers J. Chem. Ecol. 25 1895 1906 CrossRef Google Scholar Ômura, H., Honda, K., Hayashi, N. 2000 Floral scent of Osmanthus fragrans discourages foraging behavior of cabbage butterfly, Pieris rapae J. Chem. Ecol. 26 655 666 CrossRef Google Scholar Peschken, D. P., Derby, J. L. 1992 Effect of Urophora cardui (L) (Diptera, Tephritidae) and Ceutorhynchus litura (F) (Coleoptera, Curculionidae) on the weed Canada thistle, Cirsium arvense (L) Scop Can. Entomol. 124 145 150 Google Scholar Pichersky, E., Raguso, R. A., Lewinsohn, E., Croteau, R. 1994 Floral scent production in Clarkia (Onagraceae). 1. Localization and developmental modulation of monoterpene emission and linalool synthase activity Plant Physiol. 106 1533 1540 PubMed Google Scholar Primack, R. B. 1985 Longevity of individual flowers Annu. Rev. Ecol. Syst. 16 15 38 CrossRef Google Scholar Proctor, M., Yeo, P., Lack, A. 1996The Natural History of Pollination Timber Press Portland 479 Google Scholar Radford, A. E., Ahles, H. E., Bell, C. R. 1968Manual of the Vascular Flora of the Carolinas The University of North Carolina Press Chapel Hill Google Scholar Raguso, R. A. 2003 Olfactory landscapes and deceptive pollination: Signal, noise and convergent evolution in floral scent Blomquist, G. J. Vogt, R. eds. Insect Pheromone Biochemistry and Molecular Biology Academic Press New York 631 650 Google Scholar Raguso, R. A., Levin, R. A., Foose, S. E., Holmberg, M. W., McDade, L. A. 2003 Fragrance chemistry, nocturnal rhythms and pollination “syndromes” in Nicotiana Phytochemistry 63 265 284 CrossRef PubMed Google Scholar Schiestl, F. P., 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 CrossRef Google Scholar Sokal, R. S., Rohlf, F. J. 1995Biometry3 W. H. Freeman and Co. New York Google Scholar Strauss, S. Y. 1997 Floral characters link herbivores, pollinators, and plant fitness Ecology 78 1640 1645 Google Scholar
Theis, N. 2003. Targeting pollinators and evading herbivores: Floral scent emission in two species of
. Ph.D. dissertation, State University of New York at Stony Brook.
Google Scholar Tollsten, L. 1993 A multivariate approach to post-pollination changes in the floral scent of Platanthera bifolia (Orchidaceae) Nord. J. Bot. 13 495 499 Google Scholar Tollsten, L., Bergström, J. 1989 Variation and post-pollination changes in floral odors released by Platanthera bifolia (Orchidaceae) Nord. J. Bot. 9 359 362 Google Scholar Tollsten, L., Ovstedal, D. O. 1994 Differentiation in floral scent chemistry among populations of Conopodium majus (Apiaceae) Nord. J. Bot. 14 361 367 Google Scholar Doorn, W. G. 1997 Effects of pollination on floral attraction and longevity J. Exp. Bot. 48 1615 1622 CrossRef Google Scholar Staden, J., Cook, E., Noodén, L. D. 1988 Cytokinins and senescence Noodén, L. D. Leopold, A. C. eds. Senescence and Aging in Plants Academic Press San Diego 281 328 Google Scholar Wheiss, M. R. 1995 Floral color-change—a widespread functional convergence Am. J. Bot. 82 167 185 Google Scholar WHeiss, M. R. 1997 Innate colour preferences and flexible colour learning in the pipevine swallowtail Anim. Behav. 53 1043 1052 CrossRef Google Scholar WHeiss, M. R. 2001 Vision and learning in some neglected pollinators: Beetles, flies, moths, and butterflies Chittka, L. Thomson, J. D. eds. Cognitive Ecology of Pollination Cambridge University Press Cambridge 171 190 Google Scholar Copyright information
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