Evolutionary Ecology

, Volume 24, Issue 4, pp 671–684 | Cite as

Modification of bumblebee behavior by floral color change and implications for pollen transfer in Weigela middendorffiana

Original Paper


Flowers of Weigela middendorffiana change the color from yellow to red. The previous study revealed that red-phase flowers no longer have sexual function and nectar, and bumblebees selectively visit yellow-phase flowers. The present study examined how retaining color-changed flowers can regulate the foraging behavior of bumblebees and pollen transport among flowers within (geitonogamous pollination) and between (outcrossing pollination) plants and how the behavior is influenced by display size (i.e., number of functional flowers) and visitation frequency. The visitation frequencies of bumblebees to plants and successive flower probes within plants were observed in the field using plants whose flower number and composition of the two color-phase flowers had been manipulated. To evaluate pollination efficiency over multiple pollinator visits, a pollen transport model was constructed based on the observed bumblebee behavior. In the simulation, three flowering patterns associated with display size and existence of color-changed flowers were postulated as follows: Type 1, large display (100 functional flowers) and no retention of color-changed flowers; Type 2, small display (50 functional flowers) and retention of color-changed flowers (50 old flowers), and; Type 3, large display (100 functional flowers) and retention of color-changed flowers (100 old flowers). Color-changed flowers did not contribute to increasing bumblebee attraction at a distance but reduced the number of successive flower probes within plants. Comparisons of pollen transfer between Types 1 and 3 revealed that the retention of color-changed flowers did not influence the total amount of pollen exported when pollinator visits were abundant (>100 visits) but decreased geitonogamous pollination. Comparisons between Types 2 and 3 revealed that the discouragement effect of floral color change on successive probes accelerated in plants with a large display size. Overall, the floral color change strategy contributed to reduce geitonogamous pollination, but its effectiveness was highly sensitive to display size and pollinator frequency.


Floral color change Geitonogmous pollination Outcrossing pollination Pollen discounting Pollen dynamics Weigela middendorffiana 



We are grateful to Yoshiaki Kameyama for discussing this study to Asuka Koyama for help in the field survey, and to the two anonymous reviewers for their critical comments on the earlier version of the manuscript. This work was partly supported by JSPS Research Fellowships from the Japan Society for the Promotion of Science for Young Scientists.


  1. Aizen MA, Harder LD (2007) Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88:271–281CrossRefPubMedGoogle Scholar
  2. Barrett SCH (2002) Sexual interference of the floral kind. Heredity 88:154–159CrossRefPubMedGoogle Scholar
  3. Barrett SCH, Harder LD, Cole WW (1994) Effects of flower number and position on self-fertilization in experimental populations of Eichhornia paniculata (Pontederiaceae). Funct Ecol 8:526–535CrossRefGoogle Scholar
  4. Broyles SB, Wyatt R (1993) The consequences of self-pollination in Asclepias exaltata, a self-incompatible milkweed. Am J Bot 80:41–44CrossRefGoogle Scholar
  5. Casper BB, Lapine TR (1984) Changes in corolla color and other floral characteristics in Cryptantha humilis (Boraginaceae): cues to discourage pollinators. Evolution Int J org Evolution 38:128–141Google Scholar
  6. Chittka L, Dyer AG, Bock F, Dornhaus A (2003) Bees trade off foraging speed for accuracy. Nature 424:388CrossRefPubMedGoogle Scholar
  7. Cozzolino S, Widmer A (2005) Orchid diversity: an evolutionary consequence of deception? Trends Ecol Evol 20:487–494CrossRefPubMedGoogle Scholar
  8. Cruzan MB, Neal PR, Willson MF (1988) Floral display in Phyla incisa: consequences for male and female reproductive success. Evolution Int J org Evolution 42:505–515Google Scholar
  9. Dafni A, Lehrer M, Kevan PG (1997) Spatial flower parameters and insect spatial vision. Biol Rev 72:239–282CrossRefGoogle Scholar
  10. De Jong TJ, Klinkhamer PGL, Vanstaalduinen MJ (1992) The consequences of pollination biology for selection of mass or extended blooming. Funct Ecol 6:606–615CrossRefGoogle Scholar
  11. De Jong TJ, Waser NM, Klinkhamer PGL (1993) Geitonogamy: the neglected side of selfing. Trends Ecol Evol 8:321–325CrossRefGoogle Scholar
  12. Driessen G, Bernstein C (1999) Patch departure mechanisms and optimal host exploitation in an insect parasitoid. J Anim Ecol 68:445–459CrossRefGoogle Scholar
  13. Driessen G, Bernstein C, Vanalphen JJM, Kacelnik A (1995) A count-down mechanism for host search in the parasitoid Venturia canescens. J Anim Ecol 64:117–125CrossRefGoogle Scholar
  14. Dyer AG, Chittka L (2004) Bumblebees (Bombus terrestris) sacrifice foraging speed to solve difficult colour discrimination tasks. J Comp Physiol A 190:759–763Google Scholar
  15. Dyer AG, Spaethe J, Prack S (2008) Comparative psychophysics of bumblebee and honeybee colour discrimination and object detection. J Comp Physiol A 194:617–627CrossRefGoogle Scholar
  16. Engel EC, Irwin RE (2003) Linking pollinator visitation rate and pollen receipt. Am J Bot 90:1612–1618CrossRefGoogle Scholar
  17. Galen C, Stanton ML (1989) Bumble bee pollination and floral morphology: factors influencing pollen dispersal in the alpine sky pilot, Polemonium viscosum (Polemoniaceae). Am J Bot 76:419–426CrossRefGoogle Scholar
  18. Gori DF (1983) Post-pollination phenomena and adaptive floral changes. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Nostrand Reinhold, New York, NY, pp 31–49Google Scholar
  19. Gori DF (1989) Floral color-change in Lupinus argenteus (Fabaceae): why should plants advertise the location of unrewarding flowers to pollinators. Evolution Int J org Evolution 43:870–881Google Scholar
  20. Harder LD, Barrett SCH (1995) Mating cost of large floral displays in hermaphrodite plants. Nature 373:512–515CrossRefGoogle Scholar
  21. Harder LD, Barrett SCH (1996) Pollen dispersal and mating patterns in animal-pollinated plants. In: Lloyd DG, Barrett SCH (eds) Floral biology: studies on floral evolution in animal-pollinated plants. Chapman and Hall, New York, NY, pp 140–190Google Scholar
  22. Harder LD, Thomson JD (1989) Evolutionary options for maximizing pollen dispersal of animal-pollinated plants. Am Nat 133(3):323–344CrossRefGoogle Scholar
  23. Harder LD, Wilson WG (1998) Theoretical consequences of heterogeneous transport conditions for pollen dispersal by animals. Ecology 79:2789–2807CrossRefGoogle Scholar
  24. Herlihy CR, Eckert CG (2002) Genetic cost of reproductive assurance in a self-fertilizing plant. Nature 416:320–323CrossRefPubMedGoogle Scholar
  25. Ida TY, Kudo G (2003) Floral color change in Weigela middendorffiana (Caprifoliaceae): reduction of geitonogamous pollination by bumble bees. Am J Bot 90:1751–1757CrossRefGoogle Scholar
  26. Jones CE, Cruzan MB (1999) Floral morphological changes and reproductive success in deer weed (Lotus scoparius, Fabaceae). Am J Bot 86:273–277CrossRefGoogle Scholar
  27. Jones KN, Reithel JS (2001) Pollinator-mediated selection on a flower color polymorphism in experimental populations of Antirrhinum (Scrophulariaceae). Am J Bot 88:447–454CrossRefGoogle Scholar
  28. Kadmon R, Shmida A (1992) Departure rules used by bees foraging for nectar: a field-test. Evol Ecol 6:142–151CrossRefGoogle Scholar
  29. Kessler D, Gase K, Baldwin IT (2008) Field experiments with transformed plants reveal the sense of floral scents. Science 321:1200–1202CrossRefPubMedGoogle Scholar
  30. Kudo G, Ishii HS, Hirabayashi Y, Ida TY (2007) A test of the effect of floral color change on pollination effectiveness using artificial inflorescences visited by bumblebees. Oecologia 154:119–128CrossRefPubMedGoogle Scholar
  31. Lefebvre D, Pierre J, Outreman Y, Pierre JS (2007) Patch departure rules in Bumblebees: evidence of a decremental motivational mechanism. Behav Ecol Sociobiol 61:1707–1715CrossRefGoogle Scholar
  32. Nilsson LA (1992) Orchid pollination biology. Trends Ecol Evol 7:255–259CrossRefGoogle Scholar
  33. Oberrath R, Böhning-Gaese K (1999) Floral color change and the attraction of insect pollinators in lungwort (Pulmonaria collina). Oecologia 121:383–391CrossRefGoogle Scholar
  34. Rademaker MCJ, De Jong TJ, Klinkhamer PGL (1997) Pollen dynamics of bumble-bee visitation on Echium vulgare. Funct Ecol 11:554–563CrossRefGoogle Scholar
  35. Raguso RA (2008) The “Invisible hand” of floral chemistry. Science 321:1163–1164CrossRefPubMedGoogle Scholar
  36. Waage JK (1979) Foraging for patchily distributed hosts by the parasitoid, Nemeritis canescens. J Anim Ecol 48:353–371CrossRefGoogle Scholar
  37. Waser NM, Price MV (1991) Reproductive costs of self-pollination in Ipomopsis aggregata (Polemoniaceae). Am J Bot 78:1036–1043CrossRefGoogle Scholar
  38. Weiss MR (1991) Floral color change as cues for pollinators. Nature 354:227–229CrossRefGoogle Scholar
  39. Weiss MR (1995) Floral color-change: a widespread functional convergence. Am J Bot 82:167–185CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Graduate School of Environmental ScienceHokkaido UniversitySapporoJapan

Personalised recommendations