Floral Scent in Food-Deceptive Orchids: Species Specificity and Sources of Variability

Abstract

One third of all orchid species are deceptive and do not reward their pollinators. Such deceptive orchids are often characterised by unusually high variation in floral signals such as colour and scent. In this study, we investigated the scent composition of two Mediterranean food-deceptive orchids Orchis mascula, Orchis pauciflora, and their hybrid, O. × colemanii. Scent was collected in situ by headspace sorption and was subsequently analysed with gas chromatography and gas chromatography-mass spectrometry. We compared variation of odour compounds within and between populations as well as species. We identified 35 floral scent compounds, mainly monoterpenes, which were shared by both species. Both quantitative and qualitative variability within and among populations was high. Many individuals within species could be classified to different “odour-types”. In spite of high qualitative and quantitative intra- and inter-population variability, the species were clearly differentiated in their scent bouquets, whereas most hybrid individuals emitted an intermediate scent.

Hybridisation - floral odour - Orchis mascula - Orchis pauciflora - pollination - species differentiation - food deception.

References

• 1 Aceto S., Caputo P., Cozzolino S., Gaudio L., Moretti A.. Phylogeny and evolution of Orchis and allied genera based on ITS DNA variation: morphological gaps and molecular continuity.  Molecular Phylogenetics and Evolution. (1999);  13 67-76
• 2 Ackerman J. D.. Mechanisms and evolution of food-deceptive pollination systems in orchids.  Lindleyana. (1986);  1 108-113
• 3 Anderson B., Johnson S. D., Carbutt C.. Exploitation of a specialized mutualism by a deceptive orchid.  American Journal of Botany. (2005);  92 1342-1349
• 4 Andersson S.. Antennal responses to floral scents in the butterflies Inachis io, Aglais urticae (Nymphalidae), and Gonepteryx rhamni (Pieridae).  Chemoecology. (2003);  13 1-11
• 5 Ayasse M., Schiestl F. P., Paulus H. F., Löfstedt C., Hansson B. S., Ibarra F., Francke W.. Evolution of reproductive strategies in the sexually deceptive orchid Ophrys spegodes: how does flower-specific variation of odor signals influence reproductive success?.  Evolution. (2000);  54 1995-2006
• 6 Azuma H., Toyota M., Asakawa Y.. Intraspecific variation of floral scent chemistry in Magnolia kobus DC. (Magnoliaceae).  Journal of Plant Research. (2001);  114 411-422
• 7 Bergström G., Birgersson G., Groth I., Nilsson L. A.. Floral fragrance disparity between three taxa of Ladyslipper Cypripedium calceolus (Orchidaceae).  Phytochemistry. (1992);  31 2315-2319
• 8 Buttery R. G., Kamm J. A., Ling L. C.. Volatile components of red clover leaves, flowers, and seed pods: possible insect attractants.  Journal of Agricultural and Food Chemistry. (1984);  32 254-256
• 9 Campbell D. R.. Natural selection in Ipomopsis hybrid zones: implications for ecological speciation.  New Phytologist. (2004);  161 83-90
• 10 Cozzolino S., Schiestl F. P., Müller A., De Castro O., Nardella A. M., Widmer A.. Evidence for pollinator sharing in Mediterranean nectar-mimic orchids: absence of premating barriers?.  Proceedings of the Royal Society B - Biological Sciences. (2005);  272 1271-1278
• 11 Cozzolino S., Nardella A. M., Impagliazzo S., Widmer A., Lexer C.. Hybridization and conservation of Mediterranean orchids: should we protect the orchid hybrids or the orchid hybrid zones?.  Biological Conservation. (2006);  129 14-23
• 12 Dafni A.. Floral mimicry - mutualism and undirectional exploitation of insects by plants. Juniper, B. and Sothwood, R., eds. Insects and the Plant Surface. London; Edward Arnold (1986): 81-90
• 13 Dafni A., Ivry Y.. Floral mimicry between Orchis israelitica Baumann and Dafni (Orchidaceae) and Bellevalia flexuosa Boiss (Liliaceae).  Oecologia. (1981);  49 229-232
• 14 Delforge P.. Guide des Orchidées d'Europe, d'Afrique du Nord et du Proche-Orient. Lausanne; Delachaux et Niestlé (2001)
• 15 Dobson H. E. M.. Floral volatiles in insect biology. Bernays, E. A., ed. Insect-Plant Interactions. Boca Rato; CRC Press (1994): 47-81
• 16 Dobson H. E. M., Arroyo J., Bergström G., Groth I.. Interspecific variation in floral fragrances within the genus Narcissus (Amaryllidaceae).  Biochemical Systematics and Ecology. (1997);  25 685-706
• 17 Dötterl S., Jürgens A.. Spatial fragrance patterns in flowers of Silene latifolia: lilac compounds as olfactory nectar guides?.  Plant Systematics and Evolution. (2005);  255 99-109
• 18 Dötterl S., Wolfe L. M., Jürgens A.. Qualitative and quantitative analyses of flower scent in Silene latifolia.  Phytochemistry. (2005 a);  66 203-213
• 19 Dötterl S., Füssel U., Jürgens A., Aas G.. 1,4-Dimethoxybenzene, a floral scent compound in willows that attracts an oligolectic bee.  Journal of Chemical Ecology. (2005 b);  31 2993-2998
• 20 Effmert U., Grosse J., Röse U. S. R., Ehrig F., Kägi R., Piechulla B.. Volatile composition, emission pattern, and localization of floral scent emission in Mirabilis jalapa (Nyctaginaceae).  American Journal of Botany. (2005);  92 2-12
• 21 Ferdy J.-B., Gouyon P.-H., Moret J., Godelle B.. Pollinator behavior and deceptive pollination: learning process and floral evolution.  The American Naturalist. (1998);  152 696-705
• 22 Galen C.. Regulation of seed-set in Polemonium viscosum: floral scents, pollination, and resources.  Ecology. (1985);  66 792-797
• 23 Galen C., Kevan P. G.. Scent and color, floral polymorphisms and pollination biology in Polemonium viscosum Nutt.  American Midland Naturalist. (1980);  104 281-289
• 24 Gerlach G., Schill R.. Fragrance analyses, an aid to taxonomic relationships of the genus Coryanthes (Orchidaceae).  Plant Systematics and Evolution. (1989);  168 159-165
• 25 Gigord L. D. B., Macnair M. R., Smithson A.. Negative frequency-dependent selection maintains a dramatic flower color polymorphism in the rewardless orchid Dactylorhiza sambucina (L.) Soò.  Proceedings of the National Academy of Sciences of the USA. (2001);  98 6253-6255
• 26 Granero A. M., Gonzalez F. J. E., Sanz J. M. G., Vidal J. L. M.. Analysis of biogenic volatile organic compounds in zucchini flowers: identification of scent sources.  Journal of Chemical Ecology. (2005);  31 2309-2322
• 27 Gumbert A., Kunze J.. Colour similarity to rewarding model plants affects pollination in a food deceptive orchid, Orchis boryi.  Biological Journal of the Linnean Society. (2001);  72 419-433
• 28 Heinrich B.. Bee flowers: a hypothesis on flower variety and blooming times.  Evolution. (1975);  29 325-334
• 29 Huber F. K., Kaiser R., Sauter W., Schiestl F. P.. Floral scent emission and pollinator attraction in two species of Gymnadenia (Orchidaceae).  Oecologia. (2005);  142 564-575
• 30 Johnson S. D.. Batesian mimicry in the non-rewarding orchid Disa pulchra, and its consequences for pollinator behavior.  Biological Journal of the Linnean Society. (2000);  71 119-132
• 31 Johnson S. D., Peter C. I., Nilsson L. A., Agren J.. Pollination success in a deceptive orchid is enhanced by co-occurring rewarding magnet plants.  Ecology. (2003);  84 2919-2927
• 32 Kaiser R.. The Scent of Orchids. Olfactory and Chemical Investigations. Amsterdam; Elsevier Science Publishers (1993)
• 33 Knudsen J. T., Tollsten L., Bergström G. L.. Floral scents - a checklist of volatile compounds isolated by head-space techniques.  Phytochemistry. (1993);  33 253-280
• 34 Knudsen J. T., Stahl B.. Floral odours in the Theophrastaceae.  Biochemical Systematics and Ecology. (1994);  22 259-268
• 35 Knudsen J. T., Andersson S., Bergman P.. Floral scent attraction in Geonoma macrostachys, an understorey palm of the Amazonian rain forest.  Oikos. (1999);  85 409-418
• 36 Manning A.. Some evolutionary aspects of the flower constancy of bees.  Proceedings of the Royal Physiological Society of Edinburgh. (1957);  25 67-71
• 37 Moya S., Ackerman J. D.. Variation in the floral fragrance of Epidendrum ciliare (Orchidaceae).  Nordic Journal of Botany. (1993);  13 41-47
• 38 Nault J. R.. Site temperatures influence seasonal changes in terpene composition in Douglas-fir vegetative buds and current-year foliage.  Canadian Journal of Forest Research - Revue Canadienne De Recherche Forestière. (2003);  33 2269-2273
• 39 Nilsson L. A.. Anthecology of Orchis mascula (Orchidaceae).  Nordic Journal of Botany. (1983 a);  3 157-179
• 40 Nilsson L. A.. Mimesis of bellflower (Campanula) by the red helleborine orchid Cephalanthera rubra.  Nature. (1983 b);  305 799-800
• 41 Nilsson L. A.. Processes of isolation and introgressive interplay between Platanthera bifolia (L.) Rich and Platanthera chlorantha (Custer) Reichb. (Orchidaceae).  Botanical Journal of the Linnean Society. (1983 c);  87 325-350
• 42 Nilsson L. A.. Orchid pollination biology.  Trends in Ecology and Evolution. (1992);  7 255-259
• 43 Olesen J. M., Knudsen J. T.. Scent profiles of flower color morphs of Corydalis cava (Fumariaceae) in relation to foraging behavior of bumblebee queens (Bombus terrestris).  Biochemical Systematics and Ecology. (1994);  22 231-237
• 44 Ômura H., Honda K.. Priority of color over scent during flower visitation by adult Vanessa indica butterflies.  Oecologia. (2005);  142 588-596
• 45 Raguso R. A.. Olfactory landscapes and deceptive pollination: signal, noise and convergent evolution in floral scent. Blomquist, G. J., ed. Insect Pheromone Biochemistry and Molecular Biology: The Biosynthesis and Detection of Pheromones and Plant Volatiles. Amsterdam; Elsevier Academic Press (2003): 631-650
• 46 Rieseberg L. H., Carney S. E.. Plant hybridization.  New Phytologist. (1998);  140 599-624
• 60 Salzmann C. C., Nardella A. M., Cozzolino S., Schiestl F. P.. Variability in floral scent in rewarding and deceptive orchids: the signature of pollinator-imposed selection?.  Annals of Botany. (2007);  DOI: 10.1093/aob/mcm161
• 47 Schemske D. W., Bradshaw H. D.. Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus).  Proceedings of the National Academy of Sciences of the USA. (1999);  96 11910-11915
• 48 Schiestl F. P., Ayasse M., Paulus H. F., Löfstedt C., Hansson B. S., Ibarra F., Francke W.. Orchid pollination by sexual swindle.  Nature. (1999);  399 421-422
• 49 Schomburg G.. Gas Chromatography. A Practical Course. New York; Wiley-VCH (1990)
• 50 Smithson A., Macnair M. R.. Negative frequency-dependent selection by pollinators on artificial flowers without rewards.  Evolution. (1997);  51 715-723
• 51 Tollsten L., Bergström G.. Variation and post-pollination changes in floral odors released by Platanthera bifolia (Orchidaceae).  Nordic Journal of Botany. (1989);  9 359-362
• 52 Tollsten L., Bergström G.. Fragrance chemotypes of Platanthera (Orchidaceae) - the result of adaptation to pollinating moths.  Nordic Journal of Botany. (1993);  13 607-613
• 53 van der Cingel N. A.. An Atlas of Orchid Pollination. Rotterdam; A. A. Balkema (2001)
• 54 Van der Pijl L., Dodson C. H.. Orchid Flowers. Their Pollination and Evolution. Coral Gables; University of Miami Press (1966)
• 55 Vogel S., Hadacek F.. Contributions to the functional anatomy and biology of Nelumbo nucifera (Nelumbonaceae). III. An ecological reappraisal of floral organs.  Plant Systematics and Evolution. (2004);  249 173-189
• 56 Waller G. D., Loper G. M., Berdel R. L.. Olfactory discrimination by honeybees of terpenes identified from volatiles of alfalfa flowers.  Journal of Apicultural Research. (1974);  13 191-197
• 57 Whitten W. M., Hills H. G., Williams N. H.. Occurence of ipsdienol in floral fragrances.  Phytochemistry. (1988);  27 2759-2760
• 58 Wood D. L.. The role of pheromones, kairomones, and allomones in the host selection and colonization behavior of bark beetles.  Annual Review of Entomology. (1982);  27 411-446
• 59 Wright G. A., Smith. B. H.. Variation in complex olfactory stimuli and its influence on odour recognition.  Proceedings of the Royal Society of London Series B - Biological Sciences. (2004);  271 147-152

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