Relative impact of mate versus pollinator availability on pollen limitation and outcrossing rates in a mass-flowering species

Plant Biology

Volumn 17, Issue 1, 2015, Pages 209-218

  Delmas, C E L ^a,b,f   Escaravage, N ^a,b   Cheptou, P O ^c   Charrier, O ^a,b   Ruzafa, S ^d   Winterton, P ^e   Pornon, A ^a,b  

^a Laboratoire Evolution et Diversité Biologique   (France)

^b CNRS   (France)

^c CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^d CEMAGREF   (France)

^e UNIVERSITÉ PAUL SABATIER   (France)

^f BORDEAUX SCIENCES AGRO   (France)

Author keywords

Floral display; Insect visits; Mass flowering; Outcrossing rate; Pollen limitation; Reproductive traits; Rhododendron ferrugineum; Self incompatibility

Indexed keywords

HEXAPODA; RHODODENDRON FERRUGINEUM;

ANIMAL; CROSS BREEDING; FLOWER; GENETICS; INSECT; MULTIVARIATE ANALYSIS; PHENOTYPE; PHYSIOLOGY; PLANT SEED; POLLEN; POLLINATION; REPRODUCTION; RHODODENDRON;

ANIMALS; CROSSES, GENETIC; FLOWERS; INSECTS; MULTIVARIATE ANALYSIS; PHENOTYPE; POLLEN; POLLINATION; REPRODUCTION; RHODODENDRON; SEEDS;

EID: 84923231000     PISSN: 14358603     EISSN: 14388677     Source Type: Journal    
DOI: 10.1111/plb.12200     Document Type: Article

References (89)

1. Aizen M.A., Feinsinger P. (1994) Habitat fragmentation, native insect pollinators, and feral honey bees in Argentine "Chaco Serrado". Ecological Applications, 4, 378-392.
2. Aizen M.A., Harder L.D. (2007) Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology, 88, 271-281.
3. Ashman T.L., Knight T.M., Steets J.A., Amarasekare P., Burd M., Campbell D.R., Dudash M.R., Mazer S.J., Johnston M., Mitchell R.J., Morgan M.T., Wilson W.G. (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology, 85, 2408-2421.
4. Baker H.G. (1955) Self-compatibility and establishment after 'long distance' dispersal. Evolution, 9, 347-349.
5. Barrett S.C.H., Case A.L. (2006) The ecology and evolution of gender strategies in plants: the example of Australian Wurmbea (Colchicaceae). Australian Journal of Botany, 54, 417-433.
6. Biesmeijer J.C., Roberts S.P.M., Reemer M., Ohlemuller R., Edwards M., Peeters T., Schaffers A.P., Potts S.G., Kleukers R., Thomas C.D., Settele J., Kunin W.E. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science, 313, 351-354.
7. Brys R., Jacquemyn H., Endels P., van Rossum F., Hermy M., Triest L., De Bruyn L., Blust G.D.E. (2004) Reduced reproductive success in small populations of the self-incompatible Primula vulgaris. Journal of Ecology, 92, 5-14.
8. Buchmann S.L. (1983) Buzz pollination in angiosperms. In: Jones C.E., Little J.R. (Eds), Handbook of experimental pollination biology. Van Nostrand Reinhold, New York, USA, pp 73-113.
9. Burnham K.P., Anderson D.R. (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociological Methods & Research, 33, 261-304.
10. Campbell L.G., Husband B.C. (2007) Small populations are mate-poor but pollinator-rich in a rare, self-incompatible plant, Hymenoxys herbacea (Asteraceae). New Phytologist, 174, 915-925.
11. Cheptou P.O. (2012) Clarifying Baker's law. Annals of Botany, 109, 633-641.
12. Cheptou P.O., Avendano L.G. (2006) Pollination processes and the Allee effect in highly fragmented populations: consequences for the mating system in urban environments. New Phytologist, 172, 774-783.
13. Cheptou P.O., Imbert E., Lepart J., Escarre J. (2000) Effects of competition on lifetime estimates of inbreeding depression in the outcrossing plant Crepis sancta (Asteraceae). Journal of Evolutionary Biology, 13, 522-531.
14. Dauber J., Biesmeijer J.C., Gabriel D., Kunin W.E., Lamborn E., Meyer B., Nielsen A., Potts S.G., Roberts S.P.M., Sõber V., Settele J., Steffan-Dewenter I., Stout J.C., Teder T., Tscheulin T., Vivarelli D., Petanidou T. (2010) Effects of patch size and density on flower visitation and seed set of wild plants: a pan-European approach. Journal of Ecology, 98, 188-196.
15. Delmas C.E.L., Escaravage N., Pornon A. (2014) Massive floral display affects insect visits but not pollinator-mediated pollen transfer in Rhododendron ferrugineum. Plant Biology, 16, 234-243.
16. Delmas C.E.L., Lhuiller E., Pornon A., Escaravage N. (2011) Isolation and characterization of microsatellite loci in Rhododendron ferrugineum (Ericaceae) using pyrosequencing technology. American Journal of Botany, 98, e120-e122.
17. Dendauw J., De Riek J., Arens P., Van Bockstaele E., Vosman B., De Loose M. (2001) Development of sequenced tagged microsatellite site (STMS) markers in azaleae. Acta Horticulturae, 546, 193-197.
18. Dudash M.R., Ritland K. (1991) Multiple paternity and self-fertilization in relation to floral age in Mimulus guttatus (Scrophulariaceae). American Journal of Botany, 78, 1746-1753.
19. Duncan D.H., Nicotra A.B., Wood J.T., Cunningham S.A. (2004) Plant isolation reduces outcross pollen receipt in a partially self-compatible herb. Journal of Ecology, 92, 977-985.
20. Eckert C.G. (2000) Contributions of autogamy and geitonogamy to self-fertilization in a mass-flowering, clonal plant. Ecology, 81, 532-542.
21. Eckert C.G., Kalisz S., Geber M.A., Sargent R., Elle E., Cheptou P.O., Goodwillie C., Johnston M.O., Kelly J.K., Moeller D.A., Porcher E., Ree R.H., Vallejo-Marin M., Winn A.A. (2010) Plant mating systems in a changing world. Trends in Ecology & Evolution, 25, 35-43.
22. Eckert C.G., Samis K.E., Dart S. (2006) Reproductive assurance and the evolution of uniparental reproduction in flowering plants. In: Harder L.D., Barrett S.C.H. (Eds), Ecology and evolution of flowers. Oxford University Press, Oxford, UK, pp 183-203.
23. Elle E., Hare J.D. (2002) Environmentally induced variation in floral traits affects the mating system in Datura wrightii. Functional Ecology, 16, 79-88.
24. Eriksson O. (1989) Seedling dynamics and life histories in clonal plants. Oikos, 55, 231-238.
25. Escaravage N. (1997) Système de reproduction et stratégie de colonisation de Rhododendron ferrugineum L. (Ericaceae) (étage subalpin; Alpes du Nord). PhD Thesis, University of Grenoble, France.
26. Escaravage N., Flubacker E., Pornon A., Doche B., Till-Bottraud I. (2001) Stamen dimorphism in Rhododendron ferrugineum (Ericaceae): development and function. American Journal of Botany, 88, 68-75.
27. Escaravage N., Pornon A., Doche B., Till-Bottraud I. (1997) Breeding system in an alpine species: Rhododendron ferrugineum L (Ericaceae) in the French northern Alps. Canadian Journal of Botany, 75, 736-743.
28. Escaravage N., Questiau S., Pornon A., Doche B., Taberlet P. (1998) Clonal diversity in a Rhododendron ferrugineum L. (Ericaceae) population inferred from AFLP markers. Molecular Ecology, 7, 975-982.
29. Escaravage N., Wagner J. (2004) Pollination effectiveness and pollen dispersal in a Rhododendron ferrugineum (Ericaceae) population. Plant Biology, 6, 606-615.
30. Fernández J.D., Bosch J., Nieto-Ariza B., Gómez J.M. (2012) Pollen limitation in a narrow endemic plant: geographical variation and driving factors. Oecologia, 170, 421-431.
31. Franceschinelli E.V., Bawa K.S. (2000) The effect of ecological factors on the mating system of a South American shrub species (Helicteres brevispira). Heredity, 84, 116-123.
32. García-Ramos G., Kirkpatrick M. (1997) Genetic models of adaptation and gene flow in peripheral populations. Evolution, 51, 21-28.
33. Garibaldi L.A., Steffan-Dewenter I., Winfree R., Aizen M.A., Bommarco R., Cunningham S.A., Kremen C., Carvalheiro L.G., Harder L.D., Afik O., Bartomeus I., Benjamin F., Boreux V., Cariveau D., Chacoff N.P., Dudenhöffer J.H., Freitas B.M., Ghazoul J., Greenleaf S., Hipólito J., Holzschuh A., Howlett B., Isaacs R., Javorek S.K., Kennedy C.M., Krewenka K.M., Krishnan S., Mandelik Y., Mayfield M.M., Motzke I., Munyuli T., Nault B.A., Otieno M., Petersen J., Pisanty G., Potts S.G., Rader R., Ricketts T.H., Rundlöf M., Seymour C.L., Schüepp C., Szentgyörgyi H., Taki H., Tscharntke T., Vergara C.V., Viana B.F., Wanger T.C., Westphal C., Williams N., Klein A.M. (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science, 339, 1608-1611.
34. González-Varo J.P., Arroyo J., Aparicio A. (2009) Effects of fragmentation on pollinator assemblage, pollen limitation and seed production of Mediterranean myrtle (Myrtus communis). Biological Conservation, 142, 1058-1065.
35. Goodwillie C., Kalisz S., Eckert C.G. (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annual Review of Ecology, Evolution and Systematics, 36, 47-79.
36. Groom M.J. (1998) Allee effects limit population viability of an annual plant. The American Naturalist, 151, 487-496.
37. Harder L.D., Aizen M.A. (2010) Floral adaptation and diversification under pollen limitation. Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 529-543.
38. Harder L.D., Barrett S.C.H. (1996) Pollen dispersal and mating patterns in animal-pollinated plants. In: Lloyd D.G., Barrett S.C.H. (Eds), Floral biology: studies on floral evolution in animal pollinated plants. Chapman & Hall, New York, USA, pp 140-190.
39. Herlihy C.R., Eckert C.G. (2007) Evolutionary analysis of a key floral trait in Aquilegia canadensis (Ranunculaceae): genetic variation in herkogamy and its effect on the mating system. Evolution, 61, 1661-1674.
40. Heywood J.S. (1991) Spatial analysis of genetic variation in plant populations. Annual Review of Ecology and Systematics, 22, 335-355.
41. Holsinger K.E. (1991) Mass-action models of plant mating systems: the evolutionary stability of mixed mating systems. The American Naturalist, 138, 606-622.
42. Jakobsson A., Lazaro A., Totland O. (2009) Relationships between the floral neighborhood and individual pollen limitation in two self-incompatible herbs. Oecologia, 160, 707-719.
43. Jennersten O. (1988) Pollination in Dianthus deltoides (Caryophyllaceae): effects of habitat fragmentation on visitation and seed set. Conservation Biology, 2, 359-366.
44. Johnson S.D., Hollens H., Kuhlmann M. (2012) Competition versus facilitation: conspecific effects on pollinator visitation and seed set in the iris Lapeirousia oreogena. Oikos, 121, 545-550.
45. Karron J.D., Jackson R.T., Thumser N.N., Schlicht S.L. (1997) Outcrossing rates of individual Mimulus ringens genets are correlated with anther-stigma separation. Heredity, 79, 365-370.
46. Karron J.D., Mitchell R.J., Bell J.M. (2006) Multiple pollinator visits to Mimulus ringens (Phrymaceae) flowers increase mate number and seed set within fruits. American Journal of Botany, 93, 1306-1312.
47. Karron J.D., Mitchell R.J., Holmquist K.G., Bell J.M., Funk B. (2004) The influence of floral display size on selfing rates in Mimulus ringens. Heredity, 92, 242-248.
48. Karron J.D., Thumser N.N., Tucker R., Hessenauer A.J. (1995) The influence of population-density on outcrossing rates in Mimulus ringens. Heredity, 75, 175-180.
49. Knight T.M. (2003) Floral density, pollen limitation, and reproductive success in Trillium grandiflorum. Oecologia, 137, 557-563.
50. Knight T.M., Steets J.A., Vamosi J.C., Mazer S.J., Burd M., Campbell D.R., Dudash M.R., Johnston M.O., Mitchell R.J., Ashman T.L. (2005) Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology, Evolution and Systematics, 36, 467-497.
51. Kramer C.Y. (1956) Extension of multiple range tests to group means with unequal numbers of replications. Biometrics, 12, 307-310.
52. Kunin W.E. (1997) Population size and density effects in pollination: pollinator foraging and plant reproductive success in experimental arrays of Brassica kaber. Journal of Ecology, 85, 225-234.
53. Larson B.M.H., Barrett S.C.H. (1999) The ecology of pollen limitation in buzz-pollinated Rhexia virginica (Melastomataceae). Journal of Ecology, 87, 371-381.
54. Larson B.M.H., Barrett S.C.H. (2000) A comparative analysis of pollen limitation in flowering plants. Biological Journal of the Linnean Society, 69, 503-520.
55. Levin D.A. (1988) Local differentiation and the breeding structure of plant populations. In: Gottlieb L.D., Jain S.K. (Eds), Plant evolutionary biology. Chapman & Hall, New York, USA, pp 305-329.
56. Lloyd D.G., Schoen D.J. (1992) Self- and cross-fertilization in plants. I. Functional dimensions. International Journal of Plant Sciences, 153, 358-369.
57. Lloyd D.G., Webb C.J. (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms I. Dichogamy. New Zealand Journal of Botany, 24, 135-162.
58. Mimura M., Barbour R.C., Potts B.M., Vaillancourt R.E., Watanabe K.N. (2009) Comparison of contemporary mating patterns in continuous and fragmented Eucalyptus globulus native forests. Molecular Ecology, 18, 4180-4192.
59. Morgan M.T., Schoen D.J., Bataillon T.M. (1997) The evolution of self-fertilization in perennials. The American Naturalist, 150, 618-638.
60. Naito K., Isagi Y., Nakagoshi N. (1998) Isolation and characterization of microsatellites of Rhododendron metternichii Sieb. et Zucc. var. hondoense Nakai. Molecular Ecology, 7, 927-928.
61. Ozenda P. (1985) La végétation de la chaine alpine dans l'espace montagnard européen. Masson, Paris, France, pp 344.
62. Porcher E., Lande R. (2005) The evolution of self-fertilization and inbreeding depression under pollen discounting and pollen limitation. Journal of Evolutionary Biology, 18, 497-508.
63. Pornon A., Escaravage N., Thomas P., Taberlet P. (2000) Dynamics of genotypic structure in clonal Rhododendron ferrugineum (Ericaceae) populations. Molecular Ecology, 9, 1099-1111.
64. Potts S.G., Biesmeijer J.C., Kremen C., Neumann P., Schweiger O., Kunin W.E. (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution, 25, 345-353.
65. Rathcke B.J. (1983) Competition and facilitation among plants for pollination. In: Real L. (Ed), Pollination biology. Academic Press, New York USA, pp 305-329.
66. Ritland K. (1986) Joint maximum likelihood estimation of genetic and mating structure using open-pollinated progenies. Biometrics, 42, 25-43.
67. Ritland K. (1989) Correlated matings in the partial selfer Mimulus guttatus. Evolution, 43, 848-859.
68. Ritland K. (2002) Extensions of models for the estimation of mating systems using n independent loci. Heredity, 88, 221-228.
69. Ritland K., Jain S. (1981) A model for the estimation of outcrossing rate and gene frequencies using n independent loci. Heredity, 47, 35-52.
70. Routley M.B., Mavraganis K., Eckert C.G. (1999) Effect of population size on the mating system in a self-compatible, autogamous plant, Aquilegia canadensis (Ranunculaceae). Heredity, 82, 518-528.
71. Sakomoto Y., Ishiguo M., Kitagawa G. (1986) Akaike information criterion statistics. K.T.K. Scientific, Tokyo, Japan.
72. Schmid-Hempel P., Speiser B. (1988) Effects of inflorescence size on pollination in Epilobium angustifolium. Oikos, 53, 98-104.
73. Schmitt J. (1983) Density-dependent pollinator foraging, flowering phenology, and temporal pollen dispersal patterns in Linanthus bicolor. Evolution, 37, 1247-1257.
74. Smouse R.E., Sork V.L. (2004) Measuring pollen flow in forest trees: an exposition of alternative approaches. Forest Ecology and Management, 197, 21-38.
75. Snow A.A., Spira T.P., Simpson R., Klips R.A. (1996) The ecology of geitonogamous pollination. In: Lloyd D.G., Barrett S.C.H. (Eds), Floral biology: studies on floral evolution in animal-pollinated plants. Chapman & Hall New York, USA, pp 191-216.
76. Spigler R.B., Chang S.M. (2009) Pollen limitation and reproduction varies with population size in experimental populations of Sabatia angularis (Gentianaceae). Botany, 87, 330-338.
77. Sun M., Ritland K. (1998) Mating system of yellow starthistle (Centaurea solstitialis), a successful colonizer in North America. Heredity, 80, 225-232.
78. Takebayashi N., Wolf D.E., Delph L.F. (2006) Effect of variation in herkogamy on outcrossing within a population of Gilia achilleifolia. Heredity, 96, 159-165.
79. van Oosterhout C., Hutchinson W.F., Wills D.P.M., Shipley P. (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535-538.
80. Vaughton G., Ramsey M. (2010) Pollinator-mediated selfing erodes the flexibility of the best-of-both-worlds mating strategy in Bulbine vagans. Functional Ecology, 24, 374-382.
81. Vaughton G., Ramsey M., Simpson I. (2008) Does selfing provide reproductive assurance in the perennial herb Bulbine vagans (Asphodelaceae)? Oikos, 117, 390-398.
82. Veddeler D., Klein A.-M., Tscharntke T. (2006) Contrasting responses of bee communities to coffee flowering at different spatial scales. Oikos, 112, 594-601.
83. Waites A.R., Agren J. (2004) Pollinator visitation, stigmatic pollen loads and among-population variation in seed set in Lythrum salicaria. Journal of Ecology, 92, 512-526.
84. Ward M., Johnson S., Zalucki M. (2012) When bigger is not better: intraspecific competition for pollination increases with population size in invasive milkweeds. Oecologia, 171, 1-9.
85. Ward M., Johnson S.D. (2005) Pollen limitation and demographic structure in small fragmented populations of Brunsvigia radulosa (Amaryllidaceae). Oikos, 108, 253-262.
86. Webb C.J., Lloyd D.G. (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms II. Herkogamy. New Zealand Journal of Botany, 24, 163-178.
87. Winfree R., Bartomeus I., Cariveau D.P. (2011) Native pollinators in anthropogenic habitats. Annual Review of Ecology, Evolution, and Systematics, 42, 1.
88. Young H.J., Young T.P. (1992) Alternative outcomes of natural and experimental high pollen loads. Ecology, 73, 639-647.
89. Zimmerman M. (1980) Reproduction in Polemonium: competition for pollinators. Ecology, 61, 497-501.