Skip to main content
Log in

Effectiveness of buzz pollination in Pedicularis chamissonis: significance of multiple visits by bumblebees

  • Original Article
  • Published:
Ecological Research

Abstract

Pollination success of plants is highly susceptible to the frequency of visits and foraging behavior of pollinators. Pollination of the nectarless flowers of Pedicularis species depends on bumblebee workers collecting pollen by vibrating the anthers (buzz pollination). However, little is known about the efficiency of the pollination system. Foraging behavior, pollen removal from anthers and pollen deposition on stigmas of P. chamissonis were studied to assess the effectiveness of buzz pollination in an alpine snowbed population of northern Japan. Although bumblebees tended to visit most of the flowers open at a given time within inflorescences during a single visit, pollen removal rate at the first visit was about 20%, and buzzing period decreased with increasing number of previous visits, resulting in a decreasing proportion of pollen removed per visit as the number of visits increased. These trends enable plants to provide pollen for more pollinators. The number of pollen grains deposited on stigmas was not saturated during the first visit and increased with additional visits. Irrespective of weak self-compatibility, evidence of interference between self and outcross pollen was lacking for seed production. Therefore, buzz pollination in P. chamissonis acts as a mechanism that improves the chance of cross-pollination upon multiple visits if pollinator visitation is frequent.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1a–b
Fig. 2a–b
Fig. 3

Similar content being viewed by others

References

  • Buchmann SL (1983) Buzz pollination in angiosperms. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Nortrand Reinhold, New York, pp 73–113

    Google Scholar 

  • Buchmann SL, Cane JH (1989) Bees assess pollen returns while sonicating Solanum flowers. Oecologia 81:289–294

    Article  Google Scholar 

  • Burd M (1994) Bateman’s Principle and plant reproduction: the role of pollen limitation in fruit and seed set. Bot Rev 60:83–139

    Article  Google Scholar 

  • Charnov EL (1976) Optimal foraging, the marginal value theorem. Theor Pop Biol 9:129–136

    Article  CAS  Google Scholar 

  • Duncan DH, Nicotra AB, Cunningham SA (2004) High self-pollen transfer and low fruit set in buzz-pollinated Dianella revolute (Phormiaceae). Aus J Bot 52:185–193

    Article  Google Scholar 

  • Galen C, Plowright RC (1985) Contrasting movement patterns of nectar-collecting and pollen-collecting bumble bees (Bombus terricola) on fireweed (Chamaenerion augustifolium) inflorescences. Ecol Ent 10:9–17

    Article  Google Scholar 

  • Grindeland JM, Sletvold N, Ims RA (2005) Effects of floral display size and plant density on pollinator visitation rate in a natural population of Digitalis purpurea. Funct Ecol 19:383–390

    Article  Google Scholar 

  • Gross CL, Bartier FV, Mulligan DR (2003) Floral structure, breeding system and fruit-set in the threatened sub-shrub Tetratheca juncea Smith (Tremandraceae). Ann Bot 92:771–777

    Article  PubMed  CAS  Google Scholar 

  • Harder LD (1990a) Pollen removal by bumble bees and its implications for pollen dispersal. Ecology 71:1110–1125

    Article  Google Scholar 

  • Harder LD (1990b) Behavioral responses by bumble bees to variation in pollen availability. Oecologia 85:41–47

    Article  Google Scholar 

  • Harder LD, Barclay RMR (1994) The functional significance of poricidal anthers and buzz pollination: controlled pollen removal from Dodecatheon. Funct Ecol 8:509–517

    Article  Google Scholar 

  • Harder LD, Barrett SCH (1995) Mating cost of large floral displays in hermaphrodite plants. Nature 373:512–515

    Article  CAS  Google Scholar 

  • Harder LD, Thomson JD (1989) Evolutionary options for maximizing pollen dispersal of animal-pollinated plants. Am Nat 133:323–344

    Article  Google Scholar 

  • Hirao AS, Kameyama Y, Ohara M, Isagi Y, Kudo G (2006) Seasonal changes in pollinator activity influence pollen dispersal and seed production of the alpine shrub Rhododendron aureum (Ericaceae). Mol Ecol 15:1165–1173

    Article  PubMed  CAS  Google Scholar 

  • Ishii HS (2004) Increase of male reproductive components with size in an animal-pollinated hermaphrodite, Narthecium asiaticum (Liliaceae). Funct Ecol 18:130–137

    Article  Google Scholar 

  • Kato M (1988) Bumblebee visits to Impatiens spp.: pattern and efficiency. Oecologia 76:364–370

    Google Scholar 

  • King MJ, Buchmann SL (1996) Sonication dispensing of pollen from Solanum laciniatum flowers. Funct Ecol 10:449–456

    Article  Google Scholar 

  • Klinkhamer PG, de Jong TJ (1990) Effects of plant size, plant density and sex differential nectar reward on pollinator visitation in the protandrous Echium vulgare (Boraginaceae). Oikos 57:399–405

    Article  Google Scholar 

  • Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DR, Dudash MR, Johnston MO, Mitchell RJ, Ashman T-L (2005) Pollen limitation of plant reproduction: pattern and process. Ann Rev Ecol Evo Syst 36:467–497

    Article  Google Scholar 

  • Kudo G (1993) Relationship between flowering time and fruit set of the entomophilous alpine shrub, Rhododendron aureum (Ericaceae), inhabiting snow patches. Am J Bot 80:1300–1304

    Article  Google Scholar 

  • Kudo G, Harder LD (2005) Effectiveness of floral and inflorescence traits on pollen removal and seed production of six legume species. Funct Ecol 19:245–254

    Article  Google Scholar 

  • Larson BMH, Barrett SCH (1999a) The ecology of pollen limitation in buzz-pollinated Rhexia virginica (Melastomataceae). J Ecol 87:371–381

    Article  Google Scholar 

  • Larson BMH, Barrett SCH (1999b) The pollination ecology of buzz-pollinated Rhexia virginica (Melastomataceae). Am J Bot 87:371–381

    Google Scholar 

  • Liu H, Koptur S (2003) Breeding system and pollination of a narrowly endemic herb of the Lower Florida Keys: Impacts of the urban-wildland interface. Am J Bot 90:1180–1187

    Article  Google Scholar 

  • Lloyd DG, Yates JMA (1982) Intrasexual selection and the segregation of pollen and stigmas in hermaphrodite plants, exemplified by Wahlenbergia albomarginata (Campanulaceae). Evolution 36:903–913

    Article  Google Scholar 

  • Macior LW (1986) Pollination ecology and endemic adaptation of Pedicularis howellii Gray (Scrophulariaceae). Pl Sp Biol 1:163–172

    Article  Google Scholar 

  • Macior LW (1988) A preliminary study of the pollination ecology of Pedicularis (Scrophulariaceae) in Japan. Pl Sp Biol 3:61–66

    Article  Google Scholar 

  • Macior LW (1990) Pollination ecology of Pedicularis punctata Decne. (Scrophulariaceae) in the Kashmir Himalaya. Pl Sp Biol 5:215–223

    Article  Google Scholar 

  • Macior LW (1993) Pollination ecology of Pedicularis palustris L. (Scrophulariaceae) in North America. Pl Sp Biol 8:35–44

    Article  Google Scholar 

  • Macior LW (1995a) Pollination ecology of Pedicularis in the Teton Mountain Region. Pl Sp Biol 10:77–82

    Article  Google Scholar 

  • Macior LW (1995b) Pollination ecology of Pedicularis parryi ssp. purpurea (Parry) Carr (Scrophulariaceae). Pl Sp Biol 10:163–168

    Article  Google Scholar 

  • Macior LW (1996) Pollination ecology of Pedicularis bracteosa in the montane-subalpine ecotone. Pl Sp Biol 11:165–171

    Article  Google Scholar 

  • Mitchell RJ, Karron JD, Holmquist KG, Bell JM (2004) The influence of Mimulus ringens floral display size on pollinator visitation patterns. Funct Ecol 18:116–124

    Article  Google Scholar 

  • Mustajärvi K, Siikamäki P, Rytkönen S, Lammi A (2001) Consequences of plant population size and density for plant–pollinator interactions and plant performance. J Ecol 89:80–87

    Article  Google Scholar 

  • Nilsson LA (1992) Orchid pollinator biology. Trends Ecol Evo 7:255–259

    Article  Google Scholar 

  • Ohashi K, Yahara T (2001) Behavioral responses of pollinators to variation in floral display size and their influences on the evolution of floral traits. In: Chittka L, Thomson JD (eds) Cognitive ecology of pollination. Cambridge University Press, New York, pp 274–296

    Google Scholar 

  • Pellmyr O (1988) Bumble bees (Hymenoptera: Apidae) assess pollen availability in Anemonopsis macrophylla (Ranunculaceae) through floral shape. Ann Ent Soc Am 81:792–797

    Google Scholar 

  • Pyke GH (1981) Honeyeater foraging: a test of optimal foraging theory. Anim Behav 29:878–888

    Article  Google Scholar 

  • Ramsey M (1995) Ovule pre-emption and pollen limitation in a self-fertile perennial herb (Blandfordia grandiflora, Liliaceae). Oecologia 103:101–108

    Article  Google Scholar 

  • R Development Core Team (2005) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org

  • Ree RH (2005) Phylogeny and the evolution of floral diversity in Pedicularis (Orobanchaceae). Int J Plant Sci 166:595–613

    Article  CAS  Google Scholar 

  • Snow AA, Spira TP, Simpson R, Klips RA (1996) The ecology of geitonogamous pollination. In: Lloyd DG, Barrett SCH (eds) Floral biology: studies on floral evolution in animal-pollinated plants. Chapman & Hall, New York, pp 191–216

    Google Scholar 

  • Thomson JD, Thomson BA (1992) Pollen presentation and viability schedules in animal-pollinated plants: consequences for reproductive success. In: Wyatt R (ed) Ecology and evolution of plant reproduction. Chapman & Hall, New York, pp 1–24

    Google Scholar 

  • Wolfe LM, Barrett SCH (1987) Pollinator foraging behavior and pollen collection on the floral Pontederia cordata L. Oecologia 74:347–351

    Article  Google Scholar 

  • Young HJ, Stanton ML (1990) Influences of floral variation on pollen removal and seed production in wild radish. Ecology 71: 536–547

    Article  Google Scholar 

Download references

Acknowledgments

We greatly thank two anonymous reviewers for helping to improve an earlier version of the manuscript. We also thank Y. Kameyama for field assistance, T. Kubo for assistance in data analysis, T. Kohyama and T. Takada for their suggestions, and T.Y. Ida for laboratory technical advice. This study was supported by grants from the Ministry of Education, Science and Culture, Japan (no. 16370007) and by a grant-in-aid from the Ministry of Environment for the Global Environment Research Fund (F-052).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yuka Kawai.

About this article

Cite this article

Kawai, Y., Kudo, G. Effectiveness of buzz pollination in Pedicularis chamissonis: significance of multiple visits by bumblebees. Ecol Res 24, 215–223 (2009). https://doi.org/10.1007/s11284-008-0500-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11284-008-0500-6

Keywords

Navigation