Consequences of multiple inflorescences and clonality for pollinator behavior and plant mating

American Naturalist

Volumn 184, Issue 5, 2014, Pages 580-592

  Liao, Wan Jin ^a   Harder, Lawrence D ^b  

^a BEIJING NORMAL UNIVERSITY   (China)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Bumble bee foraging; Clonality; Geitonogamy; Inflorescence; Plant architecture; Plant mating

Indexed keywords

ANGIOSPERM; BEE; CLONAL ORGANISM; DISPERSAL; FLOWER; FORAGING BEHAVIOR; PLANT ARCHITECTURE; SEX ROLE;

BOMBUS (GENUS);

NECTAR;

ANATOMY AND HISTOLOGY; ANGIOSPERM; ANIMAL; BEE; FLOWER; GENETICS; INFLORESCENCE; NECTAR; PHYSIOLOGY; POLLINATION; REPRODUCTION;

ANGIOSPERMS; ANIMALS; BEES; FLOWERS; INFLORESCENCE; PLANT NECTAR; POLLINATION; REPRODUCTION;

EID: 84908005920     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/678117     Document Type: Article

References (75)

1. Aizen, M. A. 2001. Flower sex ratio, pollinator abundance, and the seasonal pollination dynamics of a protandrous plant. Ecology 82: 127-144.
2. Albert, M. J., J. M. Iriondo, A. Escudero, and E. Torres. 2008. Dissecting components of flowering pattern: size effects on female fitness. Botanical Journal of the Linnean Society 156:227-236.
3. Albert, T., O. Raspé, and A.-L. Jacquemart. 2008. Influence of clonal growth on selfing rate in Vaccinium myrtillus L. Plant Biology 10: 643-649.
4. Araki, K., and M. Ohara. 2008. Reproductive demography of ramets and genets in a rhizomatous clonal plant Convallaria keiskei. Journal of Plant Research 121:147-154.
5. Bernhardt, C. E., R. J. Mitchell, and H. J. Michaels. 2008. Effects of population size and density on pollinator visitation, pollinator behavior, and pollen tube abundance in Lupinus perennis. International Journal of Plant Sciences 169:944-953.
6. Bertin, R. I., and C. M. Newman. 1993. Dichogamy in angiosperms. Botanical Review 59:112-152.
7. Biernaskie, J. M., R. V. Cartar, and T. A. Hurly. 2002. Risk-averse inflorescence departure in hummingbirds and bumble bees: could plants benefit from variable nectar volumes? Oikos 98:98-104.
8. Biernaskie, J. M., and R. J. Gegear. 2007. Habitat assessment ability of bumble-bees implies frequency-dependent selection on floral rewards and display size. Proceedings of the Royal Society B: Biological Sciences 274:2595-2601.
9. Charpentier, A. 2002. Consequences of clonal growth for plant mating. Evolutionary Ecology 15:521-530.
10. Conner, J. K., R. Davis, and S. Rush. 1995. The effect of wild radish floral morphology on pollination efficiency by four taxa of pollinators. Oecologia (Berlin) 104:234-245.
11. Cresswell, J. E. 1990. How and why do nectar-foraging bumblebees initiate movements between inflorescences of wild Monarda fistulosa (Lamiaceae)? Oecologia (Berlin) 82:450-460.
12. de Waal, C., S. C. H. Barrett, and B. Anderson. 2012. The effect of mammalian herbivory on inflorescence architecture in ornithophilous Babiana (Iridaceae): implications for the evolution of a bird perch. American Journal of Botany 99:1096-1103.
13. Dorken, M. E., and W. E. Van Drunen. 2010. Sex allocation in clonal plants: might clonal expansion enhance fitness gains through male function? Evolutionary Ecology 24:1463-1474.
14. Dreisig, H. 1989. Nectar distribution assessment by bumblebees foraging at vertical inflorescences. Oikos 55:239-249.
15. Dreisig, H. 2012. How long to stay on a plant: the response of bumblebees to encountered nectar levels. Arthropod-Plant Interactions 6:315-325.
16. Eckert, C. G. 2000. Contributions of autogamy and geitonogamy to self-fertilization in a mass-flowering, clonal plant. Ecology 81:532-542.
17. Fishbein, M., and D. L. Venable. 1996. Evolution of inflorescence design: theory and data. Evolution 50:2165-2177.
18. Fitzmaurice, G. M., N. M. Laird, and J. H. Ware. 2004. Applied longitudinal analysis. Wiley-Interscience, Hoboken, NJ.
19. Galen, C., and R. C. Plowright. 1985. Contrasting movement patterns of nectar-collecting and pollen-collecting bumble bees (Bombus terricola) on fireweed (Chamaenerion angustifolium) inflorescences. Ecological Entomology 10:9-17.
20. Gonzalez, A., C. L. Rowe, P. J. Weeks, D. Whittle, F. S. Gilbert, and C. J. Barnard. 1995. Flower choice by honey bees (Apis mellifera L.): sex-phase of flowers and preferences among nectar and pollen foragers. Oecologia (Berlin) 101:258-264.
21. Goulson, D., J. C. Stout, J. Langley, and W. O. H. Hughes. 2000. Identity and function of scent marks deposited by foraging bumblebees. Journal of Chemical Ecology 26:2897-2911.
22. Hao, Y.-Q., X.-Q. Zhao, D.-Y. She, B. Xu, D.-Y. Zhang, and W.-J. Liao. 2012. The role of late-acting self-incompatibility and earlyacting inbreeding depression in governing female fertility in monkshood, Aconitum kusnezoffii. PLoS ONE 7:e47034.
23. Harder, L. D. 1990a. Behavioral responses by bumble bees to variation in pollen availability. Oecologia (Berlin) 85:41-47.
24. Harder, L. D. 1990b. Pollen removal by bumble bees and its implications for pollen dispersal. Ecology 71:1110-1125.
25. Harder, L. D., and S. C. H. Barrett. 1995. Mating cost of large floral displays in hermaphrodite plants. Nature 373:512-515.
26. Harder L. D., S. C. H. Barrett, and W. W. Cole. 2000. The mating consequences of sexual segregation within inflorescences of flowering plants. Proceedings of the Royal Society B: Biological Sciences 267:315-320.
27. Harder, L. D., and S. D. Johnson. 2005. Adaptive plasticity of floral display size in animal-pollinated plants. Proceedings of the Royal Society B: Biological Sciences 272:2651-2657.
28. Harder, L. D., C. Y. Jordan, W. E. Gross, and M. B. Routley. 2004. Beyond floricentrism: the pollination function of inflorescences. Plant Species Biology 19:137-148.
29. Harder, L. D., and P. Prusinkiewicz. 2013. The interplay between inflorescence development and function as the crucible of architectural diversity. Annals of Botany 112:1477-1493.
30. Hirabayashi, Y., H. S. Ishii, and G. Kudo. 2006. Significance of nectar distribution for bumblebee behaviour within inflorescences, with reference to inflorescence architecture and display size. Éconscience 13:351-359.
31. Hodges, C. M. 1985 Bumble bee foraging: the threshold departure rule. Ecology 66:179-187.
32. Huang, S. Q., S. G. Sun, Y. Takahashi, and Y. H. Guo. 2002. Gender variation of sequential inflorescences in a monoecious plant Sagittaria trifolia (Alismataceae). Annals of Botany 90:613-622.
33. Hurlbert, A. H., S. A. Hosoi, E. J. Temeles, and P. W. Ewald. 1996. Mobility of Impatiens capensis flowers: effect on pollen deposition and hummingbird foraging. Oecologia (Berlin) 105:243-246.
34. Husband, B. C., and D. W. Schemske. 1996. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50:54-70.
35. Ishii, H. S., Y. Hirabayashi, and G. Kudo G. 2008. Combined effects of inflorescence architecture, display size, plant density and empty flowers on bumble bee behaviour: experimental study with artificial inflorescences. Oecologia (Berlin) 156:341-350.
36. Jensen, J. L. W. V. 1906. Sur les fonctions convexes et les inégalités entre les valeurs moyennes. Acta Mathematica 30:175-193.
37. Jersáková, J., and S. D. Johnson. 2006. Lack of floral nectar reduces self-pollination in a fly-pollinated orchid. Oecologia (Berlin) 147: 60-68.
38. Jersáková, J., and S. D. Johnson. 2007. Protandry promotes male pollination success in a moth-pollinated orchid. Functional Ecology 21:496-504.
39. Johnson, S. D., C. I. Peter, and J. Ågren. 2004. The effects of nectar addition on pollen removal and geitonogamy in the non-rewarding orchid Anacamptis morio. Proceedings of the Royal Society B: Biological Sciences 271:803-809.
40. Jordan, C. Y., and L. D. Harder. 2006. Manipulation of bee behavior by inflorescence architecture and its consequences for plant mating. American Naturalist 167:496-509.
41. Kadmon, R., and A. Shmida. 1992. Departure rules used by bees foraging for nectar: a field test. Evolutionary Ecology 6:142-151.
42. Karron, J. D., and R. J. Mitchell. 2012. Effects of floral display size on male and female reproductive success in Mimulus ringens. Annals of Botany 109:563-570.
43. Karron, J. D., R. J. Mitchell, K. G. Holmquist, J. M. Bell, and B. Funk. 2004. The influence of floral display size on selfing rates in Mimulus ringens. Heredity 92:242-248.
44. Kenward, M. G., and J. H. Roger. 2009. An improved approximation to the precision of fixed effects from restricted maximum likelihood. Computational Statistics and Data Analysis 53:2583-2595.
45. Kevan, P. G. 1990. How large bees, Bombus and Xylocopa (Apoidea Hymenoptera) forage on trees: optimality and patterns of movement in temperate and tropical climates. Ethology, Ecology and Evolution 2:233-242.
46. Lau, J. A., R. E. Miller, and M. D. Rausher. 2008. Selection through male function favors smaller floral display size in the common morning glory Ipomoea purpurea (Convolvulaceae). American Naturalist 172:63-74.
47. Liao, W.-J., and L. D. Harder. 2014. Data from: Consequences of multiple inflorescences and clonality for pollinator behavior and plant mating. American Naturalist, Dryad Digital Repository, http://dx.doi.org/10.5061/dryad.5s63b.
48. Liao, W.-J., Y. Hu, B.-R. Zhu, X.-Q. Zhao, Y.-F. Zeng, and D.-Y. Zhang. 2009. Female reproductive success decreases with display size in monkshood, Aconitum kusnezoffii (Ranunculaceae). Annals of Botany 104:1405-1412.
49. Lloyd, D. G. 1987. Selection of offspring size at independence and other size-versus-number strategies. American Naturalist 129:800-817.
50. Maad, J., and L. G. Reinhammar. 2004. Incidence of geitonogamy differs between two populations in the hawkmoth-pollinated Platanthera bifolia (Orchidaceae). Canadian Journal of Botany 82: 1586-1893.
51. Meagher, T. R., and L. F. Delph. 2001. Individual flower demography, floral phenology and floral display size in Silene latifolia. Evolutionary Ecology Research 3:845-860.
52. Mitchell, R. J., J. D. Karron, K. G. Holmquist, and J. M. Bell. 2004. The influence of Mimulus ringens floral display size on pollinator visitation patterns. Functional Ecology 18:116-124.
53. Miyake, Y. C., and S. Sakai. 2005. Effects of number of flowers per raceme and number of racemes per plant on bumblebee visits and female reproductive success in Salvia nipponica (Labiatae). Ecological Research 20:395-403.
54. Murcia, C. 1990. Effect of floral morphology and temperature on pollen receipt and removal in Ipomoea trichocarpa. Ecology 71: 1098-1109.
55. Mustajärvi, K., P. Siikamäki, S. Rytkönen, and A. Lammi. 2001. Consequences of plant population size and density for plant-pollinator interactions and plant performance. Journal of Ecology 89:80-87.
56. Ohashi, K., and T. Yahara. 2002. Visit larger displays but probe proportionally fewer flowers: counterintuitive behaviour of nectarcollecting bumble bees achieves an ideal free distribution. Functional Ecology 16:492-503.
57. Richards, S. A., N. M. Williams, and L. D. Harder. 2009. Variation in pollination: causes and consequences for plant reproduction. American Naturalist 174:382-398.
58. Routley, M. B., P. Kron, and B. C. Husband. 2004. The consequences of clone size for paternal and maternal success in domestic apple (Malus # domestica). American Journal of Botany 91:1326-1332.
59. Sage, T. L., F. Strumas, W. M. Cole, and S. C. H. Barrett. 1999. Differential ovule development following self- and cross-pollination: the basis of self-sterility in Narcissus triandrus (Amaryllidaceae). American Journal of Botany 86:855-870.
60. Saleh, N., K. Ohashi, J. D. Thomson, and L. Chittka. 2006. Facultative use of the repellent scent mark in foraging bumblebees: complex versus simple flowers. Animal Behaviour 71:847-854.
61. SAS Institute. 2011. SAS OnlineDoc 9.3. SAS Institute, Cary, NC.
62. Schoen, D. J., and M. Dubuc. 1990. The evolution of inflorescence size and number: a gamete-packaging strategy in plants. American Naturalist 135:841-857.
63. Smith, C. C., and S. D. Fretwell. 1974. The optimal balance between size and number of offspring. American Naturalist 108:499-506.
64. Stout, J. C., and D. Goulson. 2002. The influence of nectar secretion rates on the responses of bumblebees (Bombus spp.) to previously visited flowers. Behavioral Ecology and Sociobiology 52:239-246.
65. Thomson, J. D. 1988. Effects of variation in inflorescence size and floral rewards on the visitation rates of traplining pollinators of Aralia hispida. Evolutionary Ecology 2:65-76.
66. Valladares, F., and Ü. Niinemets. 2007. The architecture of plant crowns. Pages 101-150 in F. Valladares and F. I. Pugnaire, eds. Functional plant ecology. 2nd ed. CRC, Boca Raton, FL.
67. Vallejo-Marín, M., M. E. Dorken, and S. C. H. Barrett. 2010. The ecological and evolutionary consequences of clonality for plant mating. Annual Reviews of Ecology, Evolution and Systematics 41: 193-213.
68. Vallejo-Marín, M., and H. E. O’Brien. 2007. Correlated evolution of self-incompatibility and clonal reproduction in Solanum (Solanaceae). New Phytologist 173:415-421.
69. Van Drunen, W. E., and M. E. Dorken. 2012. Trade-offs between clonal and sexual reproduction in Sagittaria latifolia (Alismataceae) scale up to affect the fitness of entire clones. New Phytologist 196: 606-616.
70. van Groenendael, J. M., L. Klimeš, J. Klimešová, and R. J. J. Hendriks. 1996. Comparative ecology of clonal plants. Philosophical Transactions of the Royal Society B: Biological Sciences 351:1331-1339.
71. Vaughton, G., and M. Ramsey. 2010. Pollinator-mediated selfing erodes the flexibility of the best-of-both-worlds mating strategy in Bulbine vagans. Functional Ecology 24:374-382.
72. Williams, C. F. 2007. Effects of floral display size and biparental inbreeding on outcrossing rates in Delphinium barbeyi (Ranunculaceae). American Journal of Botany 94:1696-1705.
73. Williams, C. F., J. Ruvinsky, P. E. Scott, and D. K. Hews. 2001. Pollination, breeding systems, and genetic structure in two sympatric Delphinium (Ranunculaceae) species. American Journal of Botany 88:1623-1633.
74. Wilson, A. S. G., B. J. van der Kamp, and C. Ritland. 2005. Opportunities for geitonogamy in the clonal herb Maianthemum dilatatum. Canadian Journal of Botany 83:1082-1087.
75. Wolf, L. L., and F. R. Hainsworth. 1986. Information and hummingbird foraging at individual inflorescences of Ipomopsis aggregata. Oikos 46:15-22.