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.
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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
Buchmann SL, Cane JH (1989) Bees assess pollen returns while sonicating Solanum flowers. Oecologia 81:289–294
Burd M (1994) Bateman’s Principle and plant reproduction: the role of pollen limitation in fruit and seed set. Bot Rev 60:83–139
Charnov EL (1976) Optimal foraging, the marginal value theorem. Theor Pop Biol 9:129–136
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
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
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
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
Harder LD (1990a) Pollen removal by bumble bees and its implications for pollen dispersal. Ecology 71:1110–1125
Harder LD (1990b) Behavioral responses by bumble bees to variation in pollen availability. Oecologia 85:41–47
Harder LD, Barclay RMR (1994) The functional significance of poricidal anthers and buzz pollination: controlled pollen removal from Dodecatheon. Funct Ecol 8:509–517
Harder LD, Barrett SCH (1995) Mating cost of large floral displays in hermaphrodite plants. Nature 373:512–515
Harder LD, Thomson JD (1989) Evolutionary options for maximizing pollen dispersal of animal-pollinated plants. Am Nat 133:323–344
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
Ishii HS (2004) Increase of male reproductive components with size in an animal-pollinated hermaphrodite, Narthecium asiaticum (Liliaceae). Funct Ecol 18:130–137
Kato M (1988) Bumblebee visits to Impatiens spp.: pattern and efficiency. Oecologia 76:364–370
King MJ, Buchmann SL (1996) Sonication dispensing of pollen from Solanum laciniatum flowers. Funct Ecol 10:449–456
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
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
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
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
Larson BMH, Barrett SCH (1999a) The ecology of pollen limitation in buzz-pollinated Rhexia virginica (Melastomataceae). J Ecol 87:371–381
Larson BMH, Barrett SCH (1999b) The pollination ecology of buzz-pollinated Rhexia virginica (Melastomataceae). Am J Bot 87:371–381
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
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
Macior LW (1986) Pollination ecology and endemic adaptation of Pedicularis howellii Gray (Scrophulariaceae). Pl Sp Biol 1:163–172
Macior LW (1988) A preliminary study of the pollination ecology of Pedicularis (Scrophulariaceae) in Japan. Pl Sp Biol 3:61–66
Macior LW (1990) Pollination ecology of Pedicularis punctata Decne. (Scrophulariaceae) in the Kashmir Himalaya. Pl Sp Biol 5:215–223
Macior LW (1993) Pollination ecology of Pedicularis palustris L. (Scrophulariaceae) in North America. Pl Sp Biol 8:35–44
Macior LW (1995a) Pollination ecology of Pedicularis in the Teton Mountain Region. Pl Sp Biol 10:77–82
Macior LW (1995b) Pollination ecology of Pedicularis parryi ssp. purpurea (Parry) Carr (Scrophulariaceae). Pl Sp Biol 10:163–168
Macior LW (1996) Pollination ecology of Pedicularis bracteosa in the montane-subalpine ecotone. Pl Sp Biol 11:165–171
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
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
Nilsson LA (1992) Orchid pollinator biology. Trends Ecol Evo 7:255–259
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
Pellmyr O (1988) Bumble bees (Hymenoptera: Apidae) assess pollen availability in Anemonopsis macrophylla (Ranunculaceae) through floral shape. Ann Ent Soc Am 81:792–797
Pyke GH (1981) Honeyeater foraging: a test of optimal foraging theory. Anim Behav 29:878–888
Ramsey M (1995) Ovule pre-emption and pollen limitation in a self-fertile perennial herb (Blandfordia grandiflora, Liliaceae). Oecologia 103:101–108
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
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
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
Wolfe LM, Barrett SCH (1987) Pollinator foraging behavior and pollen collection on the floral Pontederia cordata L. Oecologia 74:347–351
Young HJ, Stanton ML (1990) Influences of floral variation on pollen removal and seed production in wild radish. Ecology 71: 536–547
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).
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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
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DOI: https://doi.org/10.1007/s11284-008-0500-6