Oecologia

, Volume 160, Issue 4, pp 667–674 | Cite as

Flower orientation enhances pollen transfer in bilaterally symmetrical flowers

  • Atushi Ushimaru
  • Ikumi Dohzono
  • Yasuoki Takami
  • Fujio Hyodo
Plant-Animal Interactions - Original Paper

Abstract

Zygomorphic flowers are usually more complex than actinomorphic flowers and are more likely to be visited by specialized pollinators. Complex zygomorphic flowers tend to be oriented horizontally. It is hypothesized that a horizontal flower orientation ensures effective pollen transfer by facilitating pollinator recognition (the recognition-facilitation hypothesis) and/or pollinator landing (the landing-control hypothesis). To examine these two hypotheses, we altered the angle of Commelina communis flowers and examined the efficiency of pollen transfer, as well as the behavior of their visitors. We exposed unmanipulated (horizontal-), upward-, and downward-facing flowers to syrphid flies (mostly Episyrphus balteatus), which are natural visitors to C. communis. The frequency of pollinator approaches and landings, as well as the amount of pollen deposited by E. balteatus, decreased for the downward-facing flowers, supporting both hypotheses. The upward-facing flowers received the same numbers of approaches and landings as the unmanipulated flowers, but experienced more illegitimate landings. In addition, the visitors failed to touch the stigmas or anthers on the upward-facing flowers, leading to reduced pollen export and receipt, and supporting the landing-control hypothesis. Collectively, our data suggested that the horizontal orientation of zygomorphic flowers enhances pollen transfer by both facilitating pollinator recognition and controlling pollinator landing position. These findings suggest that zygomorphic flowers which deviate from a horizontal orientation may have lower fitness because of decreased pollen transfer.

Keywords

Commelina communis Pollinator specialization Horizontal Flower orientation Zygomorphic flower 

References

  1. Cruden RW (1977) Pollen–ovule ratio: a conservative indicator of breeding system in flowering plants. Evolution 31:32–46CrossRefGoogle Scholar
  2. Darwin C (1862) On the various contrivances by which British and foreign orchids are fertilized. Murray, LondonGoogle Scholar
  3. Faden RB (1992) Floral attraction and floral hairs in the Commelinaceae. Ann Mo Bot Gard 79:46–52CrossRefGoogle Scholar
  4. Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 35:375–403CrossRefGoogle Scholar
  5. Fulton M, Hodges SA (1999) Floral isolation between Aquilegia formosa and A. pubescens. Proc R Soc Lond B 266:2247–2252CrossRefGoogle Scholar
  6. Grant V, Grant KA (1965) Flower pollination in the Phlox family. Columbia University Press, New YorkGoogle Scholar
  7. Harder LD, Barrett SCH (1993) Pollen removal from tristylous Pontederia cordata: effects of anther position and pollinator specialization. Ecology 74:1059–1072CrossRefGoogle Scholar
  8. Harder LD, Wilson WG (1994) Floral evolution and male reproductive success: optimal dispensing schedules for pollen dispersal by animal-pollinated plants. Evol Ecol 8:542–559CrossRefGoogle Scholar
  9. Harder LD, Wilson WG (1998) Theoretical consequence of heterogeneous transport conditions for pollen dispersal by animals. Ecology 79:2789–2807CrossRefGoogle Scholar
  10. Hrycan WC, Davis AR (2005) Comparative structure and pollen production of the stamens and pollinator-deceptive staminodes of Commelina coelestis and C. dianthifolia (Commelinaceae). Ann Bot 95:1113–1130CrossRefGoogle Scholar
  11. Huang S-Q, Takahashi Y, Dafni A (2002) Why does the flower stalk of Pulsatilla cernua (Ranunculaceae) bend during anthesis? Am J Bot 89:1599–1603CrossRefGoogle Scholar
  12. Ishii HS (2004) Increase of male reproductive components with size in an animal-pollinated hermaphrodite, Narthecium asiaticum (Liliaceae). Funct Ecol 18:130–137CrossRefGoogle Scholar
  13. Ishii HS, Sakai S (2002) Temporal variation in floral display size and individual floral sex allocation in racemes of Narthecium asiaticum (Liliaceae). Am J Bot 89:441–446CrossRefGoogle Scholar
  14. Johnson SD, Steiner KE (1995) Long-proboscid fly pollination of two orchids in the Cape Drankensberg mountains, South Arica. Plant Syst Evol 195:169–175CrossRefGoogle Scholar
  15. Johnson SD, Steiner KE (2000) Generalization and specialization in plant pollination systems. Trends Ecol Evol 15:140–143PubMedCrossRefGoogle Scholar
  16. Kevan PG (1975) Sun-trucking solar furnaces in high arctic flowers: significance for pollination and insects. Science 189:723–726PubMedCrossRefGoogle Scholar
  17. Kudo G (1995) Ecological significance of flower heliotropism in the spring ephemeral Adonis ramosa (Ranunculaceae). Oikos 72:14–20CrossRefGoogle Scholar
  18. Morita T, Nigorikawa T (1999) Phenotypic plasticity of floral sex. In: Ohara M (ed) Natural history of flowers. Hokkaido University Press, Sapporo, pp 227–242 (in Japanese)Google Scholar
  19. Neal PR, Dafni A, Giurfa M (1998) Floral symmetry and its role in plant-pollinator systems: terminology, distribution, and hypotheses. Annu Rev Ecol Evol Syst 29:345–373CrossRefGoogle Scholar
  20. Nilsson LA (1988) The evolution of flowers with deep corolla tubes. Nature 334:147–149CrossRefGoogle Scholar
  21. Patino S, Jeffree C, Grace J (2002) The ecological role of orientation in tropical convolvulaceous flowers. Oecologia 130:373–379CrossRefGoogle Scholar
  22. Robertson C (1928) Flowers and insects. Lists of visitors of four hundred and fifty-three flowers. Charles Robertson, CarlinvilleGoogle Scholar
  23. Sargent RD (2004) Floral symmetry affects speciation rates in angiosperms. Proc R Soc Lond B 271:603–608 CrossRefGoogle Scholar
  24. Stebbins GL (1970) Adaptive radiation of reproductive characteristics in angiosperms. Annu Rev Ecol Evol Syst 1:307–326Google Scholar
  25. Tadey M, Aizen MA (2001) Why do flowers of a hummingbird-pollinated mistletoe face down? Funct Ecol 15:782–790CrossRefGoogle Scholar
  26. R Development Core Team (2005) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org
  27. Ushimaru A, Hyodo F (2005) Why do bilateral symmetrical flowers orient vertically? Flower orientation influences pollinator landing behavior. Evol Ecol Res 7:151–160Google Scholar
  28. Ushimaru A, Nakata K (2001) Evolution of flower allometry and its significance on pollination success in the deceptive orchid, Pogonia japonica. Int J Plant Sci 162:1307–1311CrossRefGoogle Scholar
  29. Ushimaru A, Itagaki T, Ishii HS (2003a) Variation in floral organ size depends on function: a test with Commelina communis, an andromonoecious species. Evol Ecol Res 5:615–622Google Scholar
  30. Ushimaru A, Itagaki T, Ishii HS (2003b) Floral correlations in an andromonoecious species, Commelina communis (Commelinaceae). Plant Species Biol 18:103–106CrossRefGoogle Scholar
  31. Ushimaru A, Kawase D, Imamura A (2006) Flowers adaptively face down-slope in ten forest-floor herbs. Funct Ecol 20:585–591CrossRefGoogle Scholar
  32. Ushimaru A, Watanabe T, Nakata K (2007) Colored floral organs influence pollinator behavior and pollen transfer in Commelina communis. Am J Bot 94:249–258CrossRefGoogle Scholar
  33. Vogel S (1978) Evolutionary shifts from reward to deception in pollen flowers. In: Richards AJ (ed) The pollination of flowers by insects. Academic Press, New York, pp 89–96Google Scholar
  34. West EL, Laverty TM (1998) Effects of floral symmetry on flower choice and foraging behavior of bumble bees. Can J Zool 76:730–739CrossRefGoogle Scholar
  35. Wilson P (1995) Selection for pollination success and the mechanical fit of Impatiens flowers around bumble bee bodies. Biol J Linn Soc 55:355–383Google Scholar
  36. Wolfe LM, Krstolic JL (1999) Floral symmetry and Its Influence on variance in flower size. Am Nat 154:484–488 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Atushi Ushimaru
    • 1
    • 4
  • Ikumi Dohzono
    • 2
  • Yasuoki Takami
    • 3
    • 4
  • Fujio Hyodo
    • 1
  1. 1.Research Institute for Humanity and NatureKyotoJapan
  2. 2.Makino Herbarium, Graduate School of ScienceTokyo Metropolitan UniversityHachioji-shiJapan
  3. 3.Laboratory of Animal Ecology, Graduate School of ScienceKyoto UniversityKyotoJapan
  4. 4.Graduate School of Human Development and EnvironmentKobe UniversityKobeJapan

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