Abstract
Darwin pointed out that plants with vertical inflorescences are likely to be outcrossed if the inflorescence is acropetalous (flowers from the bottom up), the flowers are protandrous (pollen is dispersed before stigmas are receptive), and pollinators move upward on the inflorescence. This syndrome is common in species pollinated by bees and flies, and very few exceptions are known. We investigated flowering phenology and pollinator behavior in Besseya bullii (Scrophulariaceae) and found that it did not fit Darwin's syndrome. The vertical inflorescence was acropetalous but the flowers were distinctly protogynous, so flowers with newly receptive stigmas appeared on the inflorescence above those with dehiscing anthers. A number of small insects visited B. bullii; bees in the family Halictidae (Augochlorella striata and Dialictus spp.) were most common. When insects moved between gender phases within inflorescences, they moved up more often than down (61% versus 39% of observations, respectively) but this difference was only marginally significant. Most visits were to male-phase flowers only, and this preference was more pronounced for pollen-foraging insects than for nectar-foraging insects. B. bullii was self-compatible, so its flowering characteristics potentially could result in considerable self-pollination. However, an average of 38% of the lowermost flowers opened before any pollen was available on the same inflorescence; these “solo females” had a high probability of outcrossing (though fruit set was relatively low in the bottom portion of the inflorescence). Upper flowers may also be outcrossed because downward insect movement was not uncommon. Therefore protogyny in B. bullii may not necessarily lead to more selfing than would protandry.
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References
Bawa KS, Beach JH (1981) Evolution of sexual systems in flowering plants. Ann Mo Bot Gard 68: 254–274
Bertin RI (1993) Incidence of monoecy and dichogamy in relation to self-fertilization in angiosperms. Am J Bot 80: 557–560
Bertin RI, Newman CM (1993) Dichogamy in angiosperms. Bot Rev 59: 112–152
Best LS, Bierzychudek P (1982) Pollimator foraging on foxglove (Digitalis purpurea): a test of a new model. Evolution 36: 70–79
Coffin B, Pfannmuller L (1988) Minnesota's endangered flora and fauna. University of Minnesota Press, Minneapolis, Minn
Corbet SA, Cuthill I, Fallows M, Harrison T, Hartley G (1981) Why do nectar-foraging bees and wasps work upwards on inflorescences? Oecologia 51: 79–83
Curtis JT (1959) The vegetation of Wisconsin. University of Wisconsin Press, Madison, Wis
Darwin C (1877) The various contrivances by which orchids are fertilised by insects, reprint of 2nd edn. University of Chicago Press, Chicago, Ill
Delph LF, Lively CM (1992) Pollinator visitation, floral display, and nectar production of the sexual morphs of a gynodioecious shrub. Oikos 63: 161–170
Faegri K, Pijl L van der (1979) The principles of pollination ecology, 3rd edn. Pergamon Press, Oxford
Ginsberg HS (1985) Foraging movements of Halictus ligatus (Hymenoptera: Halictidae) and Ceratina calcarata (Hymenoptera: Anthophoridae) on Chrysanthemum leucanthemum and Erigeron annuus (Asteraceae). J Kans Entomol Soc 58: 19–26
Harder LD (1990) Pollen removal by bumble bees and its implication for pollen dispersal. Ecology 71: 1110–1125
Haynes JM, Mesler M (1984) Pollen foraging by bumblebees: foraging patterns and efficiency on Lupinus polyphyllus. Oecologia 61: 249–253
Holmgren NH (1986) Scrophulariaceae. In: Great Plains Flora Association, Flora of the Great Plains. University Press of Kansas, Lawrence, Kan, pp 751–797
Hong D-Y (1984) Taxonomy and evolution of the Veroniceae (Scrophulariaceae) with special reference to palynology. Opera Bot 75: 1–60
Hufford L (1992) Floral structure of Besseya and Synthyris (Scrophulariaceae). Int J Plant Sci 153: 217–229
Hufford L (1993) A phylogenetic analysis of Besseya (Scrophulariaceae). Int J Plant Sci 154: 350–360
Lloyd DG, Webb CJ (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms. I. Dichogamy. NZ J Bot 24: 135–162
Lloyd DG, Yates JMA (1982) Intrasexual selection and the segregation of pollen and stigmas in hermaphroditic plants, exemplified by Wahlenbergia albomarginata (Campanulaceae). Evolution 903–913
Mitchell TB (1960) Bees of the eastern United States, vol I. Tech Bull Agric Exp Stn (NC) 141
Moure JS, Hurd PD Jr. (1987) An annotated catalog of the halictid bees of the Western Hemisphere (Hymeoptera: Halictidae). Smithsonian Institution Press, Washington, DC
Pellmyr O (1985) Pollination ecology of Cimicifugo arizonica (Ranunculaceae). Bot Gaz 146: 404–412
Pyke GH (1978) Optimal foraging in bumblebees and coevolution with their plants. Oecologia 36: 281–293
Pyke GH (1979) Optimal foraging in bumblebees: rule of movement between flowers within inflorescences. Anim Behav 27: 1167–1181
Stanton ML, Ashman T-L, Galloway LF, Young HJ (1992) Estimating male fitness of plants in natural populations. In: Wyatt R (ed) Ecology and evolution of plant reproduction. Chapman and Hall, New York, pp 62–90
Waddington KD, Heinrich B (1979) The foraging movements of bumblebees on vertical “inflorescences”: an experimental analysis. J Comp Physiol [A] 134: 113–117
Williams JB, Batzli GO (1982) Pollination and dispersion of five species of lousewort (Pedicularis) near Atkasook, Alaska U.S.A. Arct Alp Res 14: 59–74
Wilson P, Thomson JD (1991) Heterogeneity among floral visitors leads to discordance between removal and deposition of pollen. Ecology 72: 1503–1507
Wyatt R (1983) Pollinator-plant interactions and the evolution of breeding systems. In: Real L (ed) Pollination biology. Academic Press, Orlando, Fla, pp 51–95
Young HJ, Stanton ML (1990) Influences of floral variation on pollen removal and seed production in wild radish. Ecology 71: 536–547
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McKone, M.J., Ostertag, R., Rauscher, J.T. et al. An exception to Darwin's syndrome: floral position, protogyny, and insect visitation in Besseya bullii (Scrophulariaceae). Oecologia 101, 68–74 (1995). https://doi.org/10.1007/BF00328902
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DOI: https://doi.org/10.1007/BF00328902