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Evolution of Reproductive Strategies in the Sexually Deceptive Orchid Ophrys Sphegodes: How Does Flower-Specific Variation of Od

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Evolution of Reproductive Strategies in the Sexually Deceptive Orchid Ophrys Sphegodes: How Does Flower-Specific Variation of Od Evolution, 54(6), 2000, pp. 1995±2006 EVOLUTION OF REPRODUCTIVE STRATEGIES IN THE SEXUALLY DECEPTIVE ORCHID OPHRYS SPHEGODES: HOW DOES FLOWER-SPECIFIC VARIATION OF ODOR SIGNALS INFLUENCE REPRODUCTIVE SUCCESS? MANFRED AYASSE,1,2 FLORIAN P. SCHIESTL,1 HANNES F. PAULUS,1 CHRISTER LOÈ FSTEDT,3 BILL HANSSON,3 FERNANDO IBARRA,4 AND WITTKO FRANCKE4 1Institute of Zoology, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria 2E-mail: [email protected] 3Department of Ecology, Lund University, S-22362 Lund, Sweden 4Institute of Organic Chemistry, D-20146 Hamburg, Germany Abstract. The orchid Ophrys sphegodes Miller is pollinated by sexually excited males of the solitary bee Andrena nigroaenea, which are lured to the ¯owers by visual cues and volatile semiochemicals. In O. sphegodes, visits by pollinators are rare. Because of this low frequency of pollination, one would expect the evolution of strategies that increase the chance that males will visit more than one ¯ower on the same plant; this would increase the number of pollination events on a plant and therefore the number of seeds produced. Using gas chromatography±mass spectrometry (GC-MS) analyses, we identi®ed more than 100 compounds in the odor bouquets of labellum extracts from O. sphegodes; 24 compounds were found to be biologically active in male olfactory receptors based on gas chromatography with electroantennographic detection (GC-EAD). Gas chromatography (GC) analyses of odors from individual ¯owers showed less intraspeci®c variation in the odor bouquets of the biologically active compounds as compared to nonactive compounds. This can be explained by a higher selective pressure on the pollinator-attracting communication signal. Furthermore, we found a characteristic variation in the GC-EAD active esters and aldehydes among ¯owers of different stem positions within an in¯orescence and in the n-alkanes and n-alkenes among plants from different populations. In our behavioral ®eld tests, we showed that male bees learn the odor bouquets of individual ¯owers during mating attempts and recognize them in later encounters. Bees thereby avoid trying to mate with ¯owers they have visited previously, but do not avoid other ¯owers either of a different or the same plant. By varying the relative proportions of saturated esters and aldehydes between ¯owers of different stem positions, we demonstrated that a plant may take advantage of the learning abilities of the pollinators and in¯uence ¯ower visitation behavior. Sixty-seven percent of the males that visited one ¯ower in an in¯orescence returned to visit a second ¯ower of the same in¯orescence. However, geitonogamy is prevented and the likelihood of cross-fertilization is enhanced by the time required for the pollinium deposited on the pollinator to complete its bending movement, which is necessary for pollination to occur. Cross-fertilization is furthermore enhanced by the high degree of odor variation between plants. This variation min- imizes learned avoidance of the ¯owers and increases the likelihood that a given pollinator would visit several to many different plants within a population. Key words. Andrena nigroaenea, chemical communication, learning behavior, Ophrys sphegodes, pollination by sexual deception, reproductive success, scent variation. Received September 14, 1999. Accepted June 4, 2000. Pollination by sexual deceit is exclusive to the Orchidaceae is pollinated by males of usually only one or a few pollinator (Ackerman 1986; Nilsson 1992), and has been documented species (Kullenberg 1961, 1973; Paulus and Gack 1986, in orchids growing in Australia (Peakall 1990), South Amer- 1990, 1994). Because Ophrys orchids are usually interfertile, ica (van der Pijl and Dodson 1966) and Europe (Kullenberg the species-speci®c attraction of pollinators is important for and BergstroÈm 1976; Paulus and Gack 1990). Orchids of the the reproductive isolation of each species. genus Ophrys grow in Europe, especially around the Medi- Ophrys ¯owers tend to produce complex bouquets of vol- terranean, and are pollinated by male insects, mostly bees atiles typically consisting of more than 100 species-speci®c (Andrenidae, Anthophoridae, Colletidae, Megachilidae, and chemical compounds (Borg-Karlson et al. 1985, 1987; Borg- Apidae), but occasionally by predatory (Sphecidae) and par- Karlson 1987, 1990). Behavioral experiments with synthetic asitic wasps (Scoliidae) and in a few cases by beetles (Scar- copies of the compounds produced by Ophrys ¯owers have abaeidae; Kullenberg 1961, 1973; Borg-Karlson 1990; Paulus shown that only certain volatiles are active in stimulating and Gack 1990). Male insects are lured to the orchid by visual mating behavior in the males (Kullenberg and BergstroÈm cues and volatile semiochemicals. At close range, chemical 1976; TengoÈ 1979; Borg-Karlson 1990). Among the com- signals from the ¯owers elicit sexual behavior in males, pounds produced by O. sphegodes, 14 hydrocarbons that were which respond in a manner similar to that shown to sex pher- identi®ed in similar proportions in cuticle extracts of the omones of females, whereby the males try to copulate with pollinators' females elicited copulation attempts in the males the ¯ower labellum. During these so-called pseudocopula- (Schiestl et al. 1999). Therefore, not all of the compounds tions, a male touches the gymnostemium of the ¯ower and may have a function in attracting male pollinators. The role the pollinarium may become attached to the insect's head or of those compounds that do not trigger copulatory behavior in some species to the tip of the abdomen; pollination takes in the males remains unknown. place when the male visits another ¯ower. Because ¯ower visits in non-food-rewarding pollination Numerous behavioral tests have shown that the Ophrys- systems are rare and brief (Peakall and Beattie 1996), food pollinator relationship is highly speci®c: Each Ophrys species and sexual deceptive plant species often show low levels of 1995 q 2000 The Society for the Study of Evolution. All rights reserved. 1996 MANFRED AYASSE ET AL. fruit set compared to food-rewarding species (Hutchings al. 1989) and P. bifolia (Tollsten and BergstroÈm 1989). How- 1987; Gill 1989; Neiland and Wilcock 1995). In six inves- ever, no behavioral tests were performed to show whether tigated species of deceptive orchids, 75±98% of all plants these variations of odor bouquets from various ¯owers of the lacked fruit set (Calvo 1990). In a population of O. sphegodes same or of different plants can be learned by pollinators. near Illmitz (Austria), only 4.9% of 887 plants were visited These important aspects of the behavior of pollinators at by a pollinator, as revealed by either pollinia removal, pol- deceptive ¯owers thus remain to be documented. lination, or both (Ayasse et al. 1997). A high specialization The aim of this study was to determine whether individual in Ophrys orchids to one or a very few pollinators may be ¯ower-speci®c olfactory recognition signals exist in the or- the most important reason for the observed low pollination chid O. sphegodes and if the pollinator males learn and rec- frequency. As an adaptation to this, ¯owers are relatively ognize odors of individual ¯owers. We addressed these goals long-lived and the opportunity for pollination is maximally through: (1) behavioral learning experiments in the ®eld with extended (Dafni and Bernhardt 1990). Furthermore, polli- pollinating male bees of Andrena nigroaenea; (2) quantitative nated ¯owers produce a high number of seeds (van der Cingel chemical analyses of the odors from individual ¯owers; (3) 1995). gas chromatography with electroantennographic detection Such a low pollination frequency should lead to the evo- (GC-EAD) analyses to identify biologically active com- lution of strategies that increase the chance that males visit pounds (compounds perceived by the males); and (4) behav- more than one ¯ower on the same plant, increasing the num- ioral experiments in the ®eld to show how self-pollination is ber of pollination events and therefore the number of seeds avoided when a pollinator visits more than one ¯ower on the produced. However, pollinators successively visiting several same in¯orescence. ¯owers within an in¯orescence may increase the frequency of geitonogamy (pollination of a neighboring ¯ower). Fur- MATERIALS AND METHODS thermore, if they return to an already visited ¯ower, autogamy Study Species (self-pollination) may occur. Although autogamy or geiton- ogamy have an obvious advantage in maintaining a high seed Ophrys sphegodes sphegodes Miller grows on alkaline, dry production even if pollinators are scarce, inbreeding depres- to damp soils in meadows, grassland, and scrubland of the sion may occur. In Orchis morio, self-pollinated ¯owers Mediterranean region and Central Europe (Delforge 1994). showed a delimited fruit formation compared to outcrossed In Austria, O. sphegodes is mostly con®ned to the east and ¯owers (Neiland and Wilcock 1995), and in Caladenia ten- southeast. It ¯owers in April and May. Flower spikes are taculata outcrossing seeds developed more quickly than rarely more than 20 cm tall and one in¯orescence is produced selfed seeds (Peakall and Beatie 1996). Due to these effects per stem. Most plants bear two to ®ve ¯owers that open on ®tness, pollinators should visit several different plants in successively. Flowers are long-lived (14±21 days) if unpol- a population and selection should enhance reproductive suc- linated, fading rapidly after pollination (Schiestl
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