'Anti-bee' and 'pro-bird' changes during the evolution of hummingbird pollination in Penstemon flowers

Journal of Evolutionary Biology

Volumn 17, Issue 4, 2004, Pages 876-885

  Castellanos, M C ^a,b   Wilson, P ^c   Thomson, J D ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b ROCKY MOUNTAIN BIOLOGICAL LABORATORY   (United States)

^c CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

Bumblebee; Experimental flower modification; Floral evolution; Hummingbird; Penstemon; Pollen transfer; Pollinator shift

Indexed keywords

EVOLUTION; FLOWER VISITING; PHENOTYPE; POLLINATION; SELECTION;

ADAPTATION; ANIMAL; ARTICLE; BEE; BIRD; COMPARATIVE STUDY; EVOLUTION; FLOWER; GENETIC SELECTION; HISTOLOGY; NONPARAMETRIC TEST; PENSTEMON; PHYSIOLOGY; POLLEN;

ADAPTATION, BIOLOGICAL; ANIMALS; BEES; BIRDS; EVOLUTION; FLOWERS; PENSTEMON; POLLEN; SELECTION (GENETICS); STATISTICS, NONPARAMETRIC;

ANIMALIA; APOIDEA; AVES; COROLLA; PENSTEMON; PENSTEMON BARBATUS; PENSTEMON STRICTUS; TROCHILIDAE;

EID: 3042698840     PISSN: 1010061X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2004.00729.x     Document Type: Article

References (56)

1. Aigner, P. 2001. Optimality modeling of fitness trade-offs: when should plants become pollinator specialists? Oikos 95: 177-184.
2. Armbruster, W.S. 1991. Multilevel analysis of morphometric data from natural plant populations: insights into ontogenetic, genetic, and selective correlations in Dalechampia scandens. Evolution 45: 1229-1244.
3. Beattie, A.J. 1971. A technique for the study of insect-born pollen. Pan-Pac. Entomol. 47: 82.
4. Brink, D.E. 1980. Reproduction and variation in Aconitum columbianum (Ranunculaceae) with emphasis on California populations. Am. J. Bot. 67: 263-273.
5. Brody, A.K. 1992. Oviposition choices by a predispersal seed predator (Hylemya sp.).1. Correspondence with hummingbird pollinators, and the role of plant size, density and floral morphology. Oecologia 91: 56-62.
6. Brown, J.H. & Kodric-Brown, A. 1979. Convergence, competition, and mimicry in a temperate community of humming-bird-pollinated flowers. Ecology 60: 1022-1035.
7. Campbell, D.R., Waser, N.M., Price, M.V., Lynch, E.A. & Mitchell, R.J. 1991. Components of phenotypic selection: pollen export and flower corolla width in Ipomopsis aggregata. Evolution 45: 1458-1467.
8. Campbell, D.R., Waser, N.M. & Price, M.V. 1994. Indirect selection of stigma position in Ipomopsis aggregata via a genetically correlated trait. Evolution 48: 55-68.
9. Campbell, D.R., Waser, N.M. & Price, M.V. 1996. Mechanisms of hummingbird-mediated selection for flower width in Ipomopsis aggregata. Ecology 77: 1463-1472.
10. Castellanos, M., Wilson, P. & Thomson, J. 2002. Dynamic nectar replenishment in flowers of Penstemon (Scrophulariaceae). Am. J. Bot. 89: 111-118.
11. Castellanos, M.C., Wilson, P. & Thomson, J.D. 2003. Pollen transfer by hummingbirds and bumblebees, and the divergence in pollination modes in Penstemon. Evolution 57: 2742-2752.
12. Clements, F.E. & Long, F.L. 1923. Experimental Pollination: An Outline of the Ecology of Flowers and Insects. Carnegie Institution, Washington.
13. Conner, J.K., Davis, R. & Rush, S. 1995. The effect of wild radish floral morphology on pollination efficiency by 4 taxa of pollinators. Oecologia 104: 234-245.
14. Crosswhite, F.S. 1967. Revision of Penstemon section Habroanthus (Scrophulariaceae) Conspectus. Am. Midl. Nat. 77: 1-11.
15. Crosswhite, F.S. & Crosswhite, C.D. 1981. Hummingbirds as pollinators of flowers in the red-yellow segment of the color spectrum, with special reference to Penstemon and the 'open habitat'. Desert Plants 3: 156-170.
16. Fægri, K. & van der Pijl, L. 1979. The Principles of Pollination Ecology. Pergamon Press, Oxford, UK.
17. Fenster, C.B., Armbruster, W.S., Dudash, M.R., Wilson, P. & Thomson, J.D. 2004. Pollination syndromes and floral specialization. Annu. Rev. Ecol. Syst. 35: (in press).
18. Fetscher, A.E., Rupert, S.M. & Kohn, J.R. 2002. Hummingbird foraging position is altered by the touch-sensitive stigma of bush monkeyflower. Oecologia 133: 551-558.
19. Fulton, M. & Hodges, S.A. 1999. Floral isolation between Aquilegia formosa and Aquilegia pubescens. Proc. R. Soc. Land. B. 266: 2247-2252.
20. Galen, C. & Cuba, J. 2001. Down the tube: pollinators, predators, and the evolution of flower shape in the Alpine Skypilot, Polemonium viscusum. Evolution 55: 1963-1971.
21. Grant, K.A. & Grant, V. 1968. Hummingbirds and their Flowers. Columbia University Press, New York.
22. Grant, V. & Temeles, E.J. 1992. Foraging ability of Rufous Hummingbirds on hummingbird flowers and hawkmoth flowers. Proc. Natl. Acad. Sci. USA 89: 9400-9404.
23. Harder, L.D. & Barrett, S.C.H. 1993. Pollen removal from tristylus Pentederia cordata: effects of anther position and pollinator specialization. Ecology 74: 1059-1072.
24. Herrera, C.M. 1993. Selection on floral morphology and environmental determinants of fecundity in a hawk moth-pollinated violet. Ecol. Monogr. 63: 251-275.
25. Herrera, C.M. 2001. Deconstructing floral phenotype: do pollinators select for corolla integration in Lavandula latifolia? J. Evol. Biol. 14: 574-584.
26. Hodges, S.A., Whittall, J.B., Fulton, M. & Yang, J.Y. 2002. Genetics of floral traits influencing reproductive isolation between Aquilegia formosa and Aquilegia pubescens. Am. Nat. 159: S51-S60.
27. Hurlbert, A.H., Hosoi, S.A., Temeles, E.J. & Ewald, P.W. 1996. Mobility of Impatiens capensis flowers: effect on pollen deposition and hummingbird foraging. Oecologia 105: 243-246.
28. Jadwiszczak, P. 2003. Rundom Projects: an application for randomization and bootstrap testing, version 1.1. Computer program available from. http://pjadw.tripod.com.
29. Kunin, W. & Iwasa, Y. 1996. Pollinator foraging strategies in mixed floral arrays: density effects and floral constancy. Theor. Pop. Biol. 49: 232-263.
30. Mayfleld, M.M., Waser, N.M. & Price, M.V. 2001. Exploring the 'most effective pollinator principle' with complex flowers: bumblebees and Ipomopsis aggregata. Ann. Bot. 88: 591-596.
31. Meléndez-Ackerman, E., Campbell, D.R. & Waser, N.M. 1997. Hummingbird behavior and mechanisms of selection flower color in Ipomopsis. Ecology 78: 2532-2541.
32. Murcia, C. 1990. Effect of floral morphology and temperature on pollen receipt and removal in Ipomoea trichocarpa. Ecology 71: 1098-1109.
33. Ohashi, K. 2002. Consequences of floral complexity for bumblebee-mediated geitonogamous self-pollination in Salvia nipponica Miq. (Labiatae). Evolution 56: 2414-2423.
34. Pellmyr, O. 2002. Pollination by animals. In: Plant-animal Interactions. An Evolutionary Approach (C. M. Herrera & O. Pellmyr, eds), pp. 157-184. Blackwell Science, Oxford, UK.
35. Pyke, G.H. 1991. What does it cost a plant to produce nectar? Nature 350: 58-59.
36. Raven, P.H. 1972. Why are bird-visited flowers predominantly red? Evolution 26: 674.
37. Schemske, D.W. & Bradshaw, H.D. 1999. Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proc. Natl. Acad. Sci. USA 96: 11910-11915.
38. Smith, C.E., Stevens, J.T., Temeles, E.J., Ewald, P.W., Hebert, R.J. & Bonkovsky, R.L. 1996. Effect of floral orifice width and shape on hummingbird-flower interactions. Oecologia 106: 482-492.
39. Stiles, F.G. 1976. Taste preferences, color preferences, and flower choice in hummingbirds. Condor 78: 10-26.
40. Stout, J.C., Allen, J.A. & Goulson, D. 1998. The influence of relative plant density and floral morphological complexity on the behaviour of bumblebees. Oecologia 117: 543-550.
41. Strauss, S.Y. 1997. Floral characters link herbivores, pollinators, and plant fitness. Ecology 78: 1640-1645.
42. Straw, R.M. 1956. Adaptive morphology of the Penstemon flower. Phytomorphology 6: 112-119.
43. Sutherland, S.D. & Vickery, R.K. 1993. On the relative importance of floral color, shape, and nectar rewards in attracting pollinators to Mimulus. Great Basin Naturalist 53: 107-117.
44. Tadey, M. & Aizen, M.A. 2001. Why do flowers of a humming-bird-pollinated mistletoe face down? Funct. Ecol. 15: 782-790.
45. Temeles, E.J. 1996. A new dimension to hummingbird-flower relationships. Oecologia 105: 517-523.
46. Temeles, E.J. & Rankin, A.G. 2000. Effect of the lower lip of Monarda didyma on pollen removal by hummingbirds. Can. J. Bot. 78: 1164-1168.
47. Thomson, J.D. 1988. Effects of variation in inflorescence size and floral rewards on the visitation rates of traplining pollinators of Aralia hispida. Evol. Ecol. 2: 65-76.
48. Thomson, J.D. 2003. When is it mutualism? Am. Nat. 162: S1-S9.
49. Thomson, J.D. & Thomson, B. 1992. Pollen presentation and viability schedules in animal-pollinated plants: consequences for reproductive success. In: Ecology and Evolution of Plant Reproduction (R. Wyatt, ed.), pp. 1-24. Chapman & Hall, New York.
50. Thomson, J.D., Wilson, P., Valenzuela, M. & Malzone, M. 2000. Pollen presentation and pollination syndromes, with special reference to Penstemon. Plant Species Biol. 15: 11-29.
51. Waser, N.M. & Price, M.V. 1985. The effect of nectar guides on pollinator preference: experimental studies with a montane herb. Oecologia 67: 121-126.
52. Williams, N.M. & Thomson, J.D. 1998. Trapline foraging by bumble bees: III. Temporal patterns of visitation and foraging success at single plants. Behav. Ecol. 9: 612-621.
53. Wilson, P. 1995. Selection for pollination success and the mechanical fit of Impatiens flowers around bumblebee bodies. Biol. J. Lin. Soc. 55: 355-383.
54. Wilson, P., Castellanos, M.C., Wolf, A. & Thomson, J.D. In press. Shifts between bee- and bird-pollination among penstemons. In: Specialization and Generalization in Pollination Systems (N. M. Waser & J. Ollerton, eds) University of Chicago Press, Chicago, USA.
55. Wilson, P., Thomson, J.D., Stanton, M.L. & Rigney, L.P. 1994. Beyond floral Batemania - Gender biases in selection for pollination success. Am. Nat. 143: 283-296.
56. Wilson, P., Castellanos, M.C., Hogue, J.N., Thomson, J.D. & Armbruster, W. S. 2004. A multivariate search for pollination syndromes among penstemons. Oikos 104: 345-361.