Should food-deceptive species flower before or after rewarding species? An experimental test of pollinator visitation behaviour under contrasting phenologies

Journal of Evolutionary Biology

Volumn 21, Issue 5, 2008, Pages 1358-1365

  Internicola, A I ^a   Bernasconi, G ^a,b   Gigord, L D B ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b UNIVERSITY OF NEUCHÂTEL   (Switzerland)

Author keywords

Artificial inflorescences; Bombus terrestris; Corolla colour similarity; Deceptive pollination; Flowering phenology; Pollinator behaviour; Pollinator learning

Indexed keywords

ADAPTATION; COLOR MORPH; COMPARATIVE STUDY; EXPERIMENTAL STUDY; FLOWER VISITING; FLOWERING; HERB; PHENOLOGY; POLLINATION; REPRODUCTIVE SUCCESS;

ANIMAL; ARTICLE; BEE; COLOR; FEEDING BEHAVIOR; FLOWER; ORCHIDACEAE; PHYSIOLOGY; POLLINATION; REWARD;

ANIMALS; BEES; COLOR; FEEDING BEHAVIOR; FLOWERS; ORCHIDACEAE; POLLINATION; REWARD;

BOMBUS TERRESTRIS; ORCHIDACEAE;

EID: 49549093129     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2008.01565.x     Document Type: Article

References (45)

1. Ackerman, J.D. 1981. Pollination biology of Calypso bulbosa var. occidentalis (Orchidaceae): a food-deception system. Madroño 28 : 101 110.
2. Ackerman, J.D. 1986. Mechanisms and evolution of food-deceptive pollination systems in orchids. Lindleyana 1 : 108 113.
3. Aizen, M.A. 2003. Influences of animal pollination and seed dispersal on winter flowering in a temperate mistletoe. Ecology 84 : 2613 2627.
4. Antonovics, J. 2006. Evolution in closely adjacent plant populations: long-term persistence of prereproductive isolation at a mine boundary. Heredity 97 : 33 37.
5. Chittka, L. 1992. The colour hexagon: a chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. J. Comp. Physiol. A 170 : 533 543.
6. Darwin, C. 1877. The Various Contivances by Which Orchids are Fertilized by Insects. Chicago University Press, Chicago, IL.
7. Dukas, R. Real, L.A. 1993. Learning constraints and floral choice behaviour in bumble bees. Anim. Behav. 46 : 637 644.
8. Dyer, A.G. 2006. Bee discrimination of flower colours in natural settings. Entomol. Gener. 28 : 257 268.
9. Dyer, A.G. Chittka, L. 2004a. Biological significance of distinguishing between similar colours in spectrally variable illumination: bumblebees (Bombus terrestris) as a case study. J. Comp. Physiol. A 190 : 105 114.
10. Dyer, A.G. Chittka, L. 2004b. Fine colour discrimination requires differential conditioning in bumblebees. Naturwissenschaften 91 : 224 227.
11. Elzinga, J.A., Atlan, A., Biere, A., Gigord, L.D.B., Weis, A. Bernasconi, G. 2007. Time after time: flowering phenology and biotic interactions. TREE 22 : 432 439.
12. Franks, S.J., Sim, S. Weis, A.E. 2007. Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proc. Natl Acad. Sci. U. S. A. 104 : 1278 1282.
13. Gigord, L.D.B., Macnair, M.R., Stritesky, M. Smithson, A. 2002. Experimental evidence for floral mimicry in a rewardless orchid. Proc. R. Soc. Lond. B Biol. Sci. 269 : 1389 1395.
14. Gill, D.E. 1989. Fruiting failure, pollinator inefficiency and speciation in orchids. In : Speciation and its Consequences (D. Otte J.A. Endler, eds pp. 458 481. Sinauer, Sunderland, MA.
15. Gillespie, J.H. 1977. Natural selection for variance in offspring numbers: a new evolutionary principle. Am. Nat. 111 : 1010 1014.
16. Gumbert, A. 2000. Colour choices by bumble bees (Bombus terrestris): innate preferences and generalization after learning. Behav. Ecol. Sociobiol. 48 : 36 43.
17. Heinrich, B. 1975. Bee flowers: a hypothesis on flower variety and blooming times. Evolution 29 : 325 334.
18. Heinrich, B. 1976. The foraging specializations of individual bumblebees. Ecol. Monogr. 46 : 105 128.
19. Heinrich, B., Mudge, P.R. Deringis, P.G. 1977. Laboratory analysis of flower constancy in foraging bumblebees: Bombus ternarius and B. terricola. Behav. Ecol. Sociobiol. 2 : 247 265.
20. Internicola, A.I., Juillet, N., Smithson, A. Gigord, L.D.B. 2006. Experimental investigation of the effect of spatial aggregation on reproductive success in a rewardless orchid. Oecologia 150 : 435 441.
21. Internicola, A.I., Page, P., Bernasconi, G. Gigord, L.D.B. 2007. Competition for pollinator visitation between deceptive and rewarding artificial inflorescences: an experimental test of the effects of floral colour similarity and spatial mingling. Func. Ecol. 21 : 864 872.
22. Johnson, S.D. Nilsson, L.A. 1999. Pollen carryover, geitonogamy, and the evolution of deceptive pollination systems in orchids. Ecology 80 : 2607 2619.
23. Johnson, S.D., Peter, C.I., Nilsson, L.A. Ågren, J. 2003. Pollination success in a deceptive orchid is enhanced by co-occurring rewarding magnet plants. Ecology 84 : 2919 2927.
24. Keasar, T., Motro, U., Shur, U. Shmida, A. 1996. Overnight memory retention of foraging skills by bumblebees is imperfect. Anim. Behav. 52 : 95 104.
25. Kindlmann, P. Balounová, Z. 2001. Irregular flowering patterns in terrestrial orchids: theories vs empirical data. Web Ecol. 2 : 75 82.
26. Manly, B.F.J. 1997. Randomization, Bootstrap and Monte Carlo Methods in Biology. Chapman & Hall, London.
27. Menzel, R. Shmida, A. 1993. The ecology of flower colours and the natural colour vision of insect pollinators: the Israeli flora as a study case. Biol. Rev. 68 : 81 120.
28. Neiland, M.R. Wilcock, C.C. 1998. Fruit set, nectar reward, and rarity in the Orchidaceae. Am. J. Bot. 85 : 1657 1671.
29. Nilsson, L.A. 1980. The pollination ecology of Dactylorhiza sambucina (Orchidaceae). Bot. Notiser. 133 : 367 385.
30. Nilsson, L.A. 1983. Anthecology of Orchis mascula (Orchidaceae). Nord. J. Bot. 3 : 157 179.
31. Nilsson, L.A. 1984. Anthecology of Orchis morio (Orchidaceae) as its outpost in the north. Nov. Act. Reg. Soc. Sci. Uppsal. 3 : 167 179.
32. Ollason, J.G. Ren, N. 2002. Taking the rough with the smooth: foraging for particulate food in continuous time. Theor. Popul. Biol. 62 : 313 327.
33. Ollerton, J. Lack, A.J. 1992. Flowering phenology - an exemple of relaxation of natural selection? TREE 7 : 274 276.
34. Peitsch, D., Fietz, A., Hertel, H., de Souza, J., Ventura, D.F. Menzel, R. 1992. The spectral input system of hymenopteran insects and their receptor based colour vision. J. Comp. Physiol. A 170 : 23 40.
35. Pilson, D. 2000. Herbivory and natural selection on flowering phenology in wild sunflower, Helianthus annuus. Oecologia 122 : 72 82.
36. Quinn, J.A. Wetherington, J.D. 2002. Genetic variability and phenotypic plasticity in flowering phenology in populations of two grasses. J. Torrey Bot. Soc. 129 : 96 106.
37. R development Core Team 2007. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-00-3. Available at: http://www.R-project.org.
38. Rathcke, B. 1983. Competition and facilitation among plants for pollination. In : Pollination Biology (L. Real, ed. pp. 309 329. Academic Press, New York.
39. Rathcke, B. Lacey, E.P. 1985. Phenological patterns of terrestrial plants. Annu. Rev. Ecol. Syst. 16 : 179 214.
40. Smithson, A. Gigord, L.D.B. 2001. Are there fitness advantages in being a rewardless orchid? Reward supplementation experiments with Barlia robertiana Proc. R. Soc. Lond. B Biol. Sci. 268 : 1 7.
41. Smithson, A. Gigord, L.D.B. 2003. The evolution of empty flowers revisited. Am. Nat. 161 : 537 552.
42. Tremblay, R.L., Ackerman, J.D., Zimmerman, J.K. Calvo, R.N. 2005. Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification. Biol. J. Linn. Soc. 84 : 1 54.
43. Van der Pijl, L. Dodson, C.H. 1966. Orchid Flowers: Their Pollination and Evolution. University of Miami Press, Coral Gables.
44. Wolfe, L.M., Elzinga, J.A. Biere, A. 2004. Increased susceptibility to enemies following introduction in the invasive plant Silene latifolia. Ecol. Lett. 7 : 813 820.
45. Zimmerman, J.K., Roubik, D.W. Ackerman, J.D. 1989. Asynchronous phenologies of a neotropical orchid and its euglossine bee pollinators. Ecology 70 : 1192 1195.