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Journal of Plant Research

, Volume 132, Issue 2, pp 251–261 | Cite as

Dynamics of secondary pollen presentation in Campanula medium (Campanulaceae)

  • Marco D’AntraccoliEmail author
  • Francesco Roma-Marzio
  • Giovanni Benelli
  • Angelo Canale
  • Lorenzo Peruzzi
Regular Paper

Abstract

After several decades of research, dynamics and patterns of mating system in floral evolution remain incompletely understood, especially with regards to strategies that combine both outcrossing and selfing, as frequently recorded in the genus Campanula. Data about temporal and spatial dynamics of secondary pollen presentation are still scarce in literature: we investigated them using Campanula medium (Campanulaceae) as case study. Experimental pollinations were conducted under natural conditions, to characterise the breeding system of this species. Effects on stigma opening and stigma receptivity of stylar pollen presence were investigated in manipulated flowers. The temporal dynamics and fitness of male and female functional phases were estimated. Flower visitors and their interactions with sexual parts of the flower were also annotated. C. medium is xenogamous and self-incompatible, with a clear temporal separation between sexual functional phases. Floral lifespan is shortened by experimental outcrossing. Removal of pollen from the style shortened the time span of male function. Pollen viability was highest at the beginning of the anthesis, decreasing during the flowering period, whereas stigmatic receptivity shows an opposite trend. We found a severe pollen limitation in the studied population. Bees were the most frequent floral visitors. In some of these insects we observed stereotyped interactions with the reproductive structures of the flower, in particular with the pollen, exposed along the upper and median portion of the style. Sexual phases in C. medium are inversely correlated and finely spatially and temporally coordinated, since stigma maturation is scalar along its length and depends on pollen presence on the style. Overall, our findings push forward the knowledge on reproductive strategies in Campanula.

Keywords

Breeding systems Flower longevity Plant–insect interactions Protandry Pollen limitation 

Notes

Acknowledgements

This study is dedicated to the memory of Maria Ansaldi (1959–2013). The Botanical Garden of Apuan Alps “Pellegrini-Ansaldi” is gratefully acknowledged for the logistic support in carrying out experimental activities. We thank Francesca Angeli, Junior Lacerda, Nico Menchini, Andrea Ribolini, and Romario Tabosa for their help in field activities. —deceased.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10265_2019_1090_MOESM1_ESM.doc (510 kb)
Supplementary material 1 (DOC 511 KB)

References

  1. Ashman TL, Schoen DJ (1996) Floral longevity: fitness consequences and resource costs. In: Lloyd DG, Barrett SCH (eds) Floral biology. Chapman and Hall, New YorkGoogle Scholar
  2. Ashman TL, Knight TM, Steets JA, Amarasekare P, Burd M, Burd M, Campbell DR, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421CrossRefGoogle Scholar
  3. Astuti G, Roma-Marzio F, D’Antraccoli M, Bedini G, Carta A, Sebastiani F, Bruschi P, Peruzzi L (2017) Conservation biology of the last Italian population of Cistus laurifolius (Cistaceae): demographic structure, genetics and reproductive success. Nat Conserv 22:169–190CrossRefGoogle Scholar
  4. Astuti G, Bedini G, Carta A, Roma-Marzio F, Trinco A, Peruzzi L (2018) Comparative assessment of reproductive traits across different habitats in the endangered Webb’s hyacinth (Bellevalia webbiana Parl.). Nat Conserv 24:81–92CrossRefGoogle Scholar
  5. Barrett SCH (2002) The evolution of plant sexual diversity. Nat Rev Genet 3:274–284CrossRefGoogle Scholar
  6. Barrett SCH (2003) Mating strategies in flowering plants: the outcrossing–selfing paradigm and beyond. Philos Trans R Soc Lond Ser B 358:991–1004CrossRefGoogle Scholar
  7. Bartolucci F, Peruzzi L, Galasso G, Albano A, Alessandrini A, Ardenghi NMG, Astuti G, Bacchetta G, Ballelli S, Banfi E, Barberis G, Bernardo L, Bouvet D, Bovio M, Cecchi L, Di Pietro R, Domina G, Fascetti S, Fenu G, Festi F, Foggi B, Gallo L, Gubellini L, Gottschlich G, Iamonico D, Iberite M, Jinénez-Mejías P, Lattanzi E, Martinetto E, Masin RR, Medagli P, Passalacqua NG, Peccenini S, Pennesi R, Pierini B, Poldini L, Prosser F, Raimondo FM, Marchetti D, Roma-Marzio F, Rosati L, Santangelo A, Scoppola A, Scortegagna S, Selvaggi A, Selvi F, Soldano A, Stinca A, Wagensommer RP, Wilhalm T, Conti F (2018) An updated checklist of the vascular flora native to Italy. Plant Biosyst 152:179–303CrossRefGoogle Scholar
  8. Bertin RI, Sullivan M (1988) Pollen interference and cryptic self-fertility in Campsis radicans. Am J Bot 75:1140–1147CrossRefGoogle Scholar
  9. Bielawska H (1964) Self fertilization in Campanula rotundifolia L. s.1. group. Acta Soc Bot Pol 42:253–264CrossRefGoogle Scholar
  10. Bingham RA, Orthner AR (1998) Efficient pollination of plants. Nature 391:238–239CrossRefGoogle Scholar
  11. Blionis GJ, Vokou D (2001) Pollination ecology of Campanula species on Mt Olympos. Greece Ecography 24:287–297CrossRefGoogle Scholar
  12. Bosma T, Dole JM (2002) Postharvest handling of cut Campanula medium flowers. Hort Sci 37:954–958Google Scholar
  13. Broyles SB, Wyatt R (1993) The consequences of self-pollination in Ascelpias exaltata, a self-incompatible milkweed. Am J Bot 80:41–44CrossRefGoogle Scholar
  14. Burd M (1994) Bateman’s principle and plant reproduction- the role of pollen limitation in fruit and seed set. Bot Rev 60:83–139CrossRefGoogle Scholar
  15. Carrió E, Güemes J (2013) The role of a mixed mating system in the reproduction of a Mediterranean subshrub (Fumana hispidula, Cistaceae). J Plant Res 126:33–40CrossRefGoogle Scholar
  16. Castro S, Silveira P, Navarro L (2008) How flower biology and breeding system affect the reproductive success of the narrow endemic Polygala vayredae Costa (Polygalaceae). Bot J Linn Soc 157:67–81CrossRefGoogle Scholar
  17. Cavins TJ, Dole JM (2001) Photoperiod, juvenility, and high intensity lighting affect flowering and cut stem quality of Campanula and Lupinus. Hort Sci 36:1192–1196Google Scholar
  18. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Evol Syst 18:237–268CrossRefGoogle Scholar
  19. Dafni A, Motte Maués M (1998) A rapid and simple procedure to determine stigma receptivity. Sex Plant Reprod 11:177–180CrossRefGoogle Scholar
  20. Dafni A, Kevan PG, Husband BC (2005) Practical pollination biology. Enviroquest, OntarioGoogle Scholar
  21. Endress PK (1994) Diversity and evolutionary biology of tropical flowers. Cambridge University Press, CambridgeGoogle Scholar
  22. Evanhoe L, Galloway LF (2002) Floral longevity in Campanula americana (Campanulaceae): a comparison of morphological and functional gender phases. Am J Bot 89:587–591CrossRefGoogle Scholar
  23. Faegri K, van der Pijl L (1979) The principles of pollination ecology. Pergamon Press, OxfordGoogle Scholar
  24. Fan YL, Kress WJ, Li QJ (2015) A new secondary pollen presentation mechanism from a wild ginger (Zingiber densissimum) and its functional roles in pollination process. PLoS One 10:e0143812CrossRefGoogle Scholar
  25. Galen C, Gregory T, Galloway LF (1989) Costs of self-pollination in a self-incompatible plant, Polemonium viscosum. Am J Bot 76:1675–1680CrossRefGoogle Scholar
  26. Galloway LF, Cirigliano T, Gremski K (2002) The contribution of display size and dichogamy to potential geitonogamy in Campanula americana. Int J Plant Sci 163:133–139CrossRefGoogle Scholar
  27. Goodwillie C, Kalisz S, Eckert CG (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Ann Rev Ecol Evol Syst 36:47–79CrossRefGoogle Scholar
  28. Guitián J, Navarro L (1996) Allocation of reproductive resources within inflorescences of Petrocoptis grandiflora (Caryophyllaceae). Can J Bot 74:1482–1486CrossRefGoogle Scholar
  29. Gullan PJ, Cranston PS (2009) The insects: an outline of entomology. Wiley, LondonGoogle Scholar
  30. Harder LD, Johnson SD (2005) Adaptive plasticity of floral display size in animal-pollinated plants. Proc R Soc Lond B Biol Sci 272:2251–2265CrossRefGoogle Scholar
  31. Harder LD, Wilson WG (1994) Floral evolution and male reproductive success: optimal dispensing schedules for pollen dispersal by animal-pollinated plants. Evol Ecol 8:542–559CrossRefGoogle Scholar
  32. Harder LD, Wilson WG (1998) A clarification of pollen discounting and its joint effects with inbreeding depression on mating system evolution. Am Nat 152:684–695CrossRefGoogle Scholar
  33. Hargreaves AL, Harder LD, Johnson SD (2009) Consumptive emasculation: the ecological and evolutionary consequences of pollen theft. Biol Rev Camb Philos Soc 84:259–276CrossRefGoogle Scholar
  34. Hill L, Hill N (2003) The flower gardener’s Bible: time-tested techniques, creative designs, and perfect plants for colorful gardens. Storey Publishing, North AdamsGoogle Scholar
  35. Hojsgaard D, Klatt S, Baier R, Carman JG, Hörandl E (2014) Taxonomy and biogeography of apomixis in angiosperms and associated biodiversity characteristics. CRC Crit Rev Plant Sci 33:414–427CrossRefGoogle Scholar
  36. Howell GJ, Slater AT, Knox RB (1993) Secondary pollen presentation in angiosperms and its biological significance. Aust J Bot 41:417–438CrossRefGoogle Scholar
  37. Inoue K (1990) Dichogamy, sex allocation, and mating system of Campanula microdonta and C. punctata. Plant Spec Biol 5:197–203CrossRefGoogle Scholar
  38. Janzon L (1983) Pollination studies of Campanula persicifolia (Campanulaceae) in Sweden. Grana 22:153–165CrossRefGoogle Scholar
  39. Kalisz S, Vogler D, Fails B, Finer M, Shepard E, Herman T, Gonzales R (1999) The mechanism of delayed selfing in Collinsia verna (Scrophulariaceae). Am J Bot 86:1239–1247CrossRefGoogle Scholar
  40. Kalinganire A, Harwood CE, Slee MU, Simons AJ (2000) Floral structure, stigma receptivity and pollen viability in relation to protandry and self-incompatibility in silky oak (Grevillea robusta A. Cunn.). Ann Bot 86:133–148CrossRefGoogle Scholar
  41. Kato M, Shimizu H, Onozaki T, Tanikawa N, Ikeda H, Hisamatsu T, Ichimura K (2002) Role of ethylene in senescence of pollinated and unpollinated Campanula medium flowers. Hort J 71:385–387Google Scholar
  42. Khatun S, Flowers TJ (1995) The estimation of pollen viability in rice. J Exp Bot 46:151–154CrossRefGoogle Scholar
  43. Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DF, Dudash MR, Johnston MO, Mitchell RJ, Ashman TL (2005) Pollen limitation of plant reproduction: pattern and process. Ann Rev Ecol Evol 36:467–497CrossRefGoogle Scholar
  44. Koski MH, Kuo L, Niedermaier KM, Galloway LF (2018a) Timing is everything: dichogamy and pollen germinability underlie variation in autonomous selfing among populations. Am J Bot 105:241–248CrossRefGoogle Scholar
  45. Koski MH, Ison JL, Padilla A, Pham AQ, Galloway LF (2018b) Linking pollinator efficiency to patterns of pollen limitation: small bees exploit the plant–pollinator mutualism. Proc R Soc B 285:20180635CrossRefGoogle Scholar
  46. Ladd PG (1994) Pollen presenters in the flowering plants - form and function. Bot J Linn Soc 115:165–195Google Scholar
  47. Lankinen Å, Armbruster WS, Antonsen L (2007) Delayed stigma receptivity in Collinsia heterophylla (Plantaginaceae): genetic variation and adaptive significance in relation to pollen competition, delayed self-pollination, and mating-system evolution. Am J Bot 94:1183–1192CrossRefGoogle Scholar
  48. Larson BMH, Barrett SCH (2000) A comparative analysis of pollen limitation in flowering plants. Biol J Linn Soc 69:503–520CrossRefGoogle Scholar
  49. Leins P, Erbar C (1990) On the mechanisms of secondary pollen presentation in the Campanulales–Asterales-complex. Bot Acta 103:87–92CrossRefGoogle Scholar
  50. Lin H, Fan X, Zhou X, Gao J (2012) Self-interference is reduced in a secondary pollen presentation species Duperrea pavettifolia (Rubiaceae). Flora 207:895–902CrossRefGoogle Scholar
  51. Lloyd DG (1965) Evolution of self-compatibility and racial differentiation in Leavenworthia (Cruciferae). Contr Gray Herb 195:3–134Google Scholar
  52. Lloyd DG, Schoen DJ (1992) Self-fertilization and cross-fertilization in plants. I. Functional dimensions. Int J Plant Sci 153:358–369CrossRefGoogle Scholar
  53. Lloyd DG, Webb CJ (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms I. Dichogamy. N Z J Bot 24:135–162CrossRefGoogle Scholar
  54. Moore JC, Pannell JR (2011) Sexual selection in plants. Curr Biol 21:R176–R182CrossRefGoogle Scholar
  55. Nyman Y (1991) Crossing experiments within the Campanula dichotoma group (Campanulaceae). Plant Syst Evol 117:185–192CrossRefGoogle Scholar
  56. Nyman Y (1992a) Pollination mechanisms in six Campanula species (Campanulaceae). Plant Syst Evol 188:97–108CrossRefGoogle Scholar
  57. Nyman Y (1992b) Reproduction in Campanula afra: mating system and the role of the pollen collecting hairs. Plant Syst Evol 183:33–41CrossRefGoogle Scholar
  58. Nyman Y (1993a) The pollen-collecting hairs of Campanula (Campanulaceae). II. Function and adaptive significance in relation to pollination. Am J Bot 80:1437–1443CrossRefGoogle Scholar
  59. Nyman Y (1993b) The pollen-collecting hairs of Campanula (Campanulaceae). I. Morphological variation and the retractive mechanism. Am J Bot 80:1427–1436CrossRefGoogle Scholar
  60. Ockendon DJ, Currah L (1977) Self pollen reduces the number of cross-pollen tubes in the styles of Brassica oleracea L. New Phytol 78:675–680CrossRefGoogle Scholar
  61. Ooi M, Auld T, Whelan R (2005) Comparison of the cut and tetrazolium tests for assessing seed viability: a study using Australian native Leucopogon species. Ecol Manag Restor 5:141–143CrossRefGoogle Scholar
  62. Pignatti S (1982) Flora d’Italia. Ed. Agricole, BolognaGoogle Scholar
  63. Primack RB (1985) Longevity of individual flowers. Annu Rev Ecol Evol Syst 16:15–35CrossRefGoogle Scholar
  64. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
  65. Raduski AR, Haney EB, Igic B (2011) The expression of self-incompatibility in angiosperms is bimodal. Evolution 66:1275–1283CrossRefGoogle Scholar
  66. Rathcke BJ (2003) Floral longevity and reproductive assurance: seasonal patterns and an experimental test with Kalmia latifolia (Ericaceae). Am J Bot 90:1328–1332CrossRefGoogle Scholar
  67. Richardson TE, Stephenson AG (1989) Pollen removal and pollen deposition affect the duration of the staminate and pistillate phases in Campanula rapunculoides. Am J Bot 76:532–538CrossRefGoogle Scholar
  68. Rodriguez-Riano T, Dafni A (2000) A new procedure to assess pollen viability. Sex Plant Reprod 12:241–244CrossRefGoogle Scholar
  69. Roquet C, Sáez L, Aldasoro JJ, Susanna A, Alarcón ML, Garcia-Jacas N (2008) Natural delineation, molecular phylogeny and floral evolution in Campanula. Syst Bot 33:203–217CrossRefGoogle Scholar
  70. Ruan CJ, Li H, Mopper S (2009) Kosteletzkya virginica displays mixed mating in response to the pollinator environment despite strong inbreeding depression. Plant Ecol 203:183–193CrossRefGoogle Scholar
  71. Ruiz-Zapata TR, Kalin-Arroyo MTK (1978) Plant reproductive ecology of a secondary deciduous tropical forest in Venezuela. Biotropica 10:221–230CrossRefGoogle Scholar
  72. Schlindwein C, Wittmann D, Martins CF, Hamm A, Siqueira JA, Schiffler D, Machado IC (2005) Pollination of Campanula rapunculus L. (Campanulaceae): how much pollen flows into pollination and into reproduction of oligolectic pollinators? Plant Syst Evol 250:147–156CrossRefGoogle Scholar
  73. Schoen DJ, Ashman TL (1995) The evolution of floral longevity: resource allocation to maintenance vs. construction of repeated parts in modular organisms. Evolution 49:131–139CrossRefGoogle Scholar
  74. Shetler SG (1979) Pollen-collecting hairs of Campanula (Campanulaceae), I: Historical review. Taxon 28:205–221CrossRefGoogle Scholar
  75. Shivanna KR (2003) Pollen–pistil interaction and fertilization. In: Pollen biology and biotechnology. Science Publisher Inc., EnfieldGoogle Scholar
  76. Song JS, Bang CS, Chang YD, Jang HT, Lee JS (2003) Forcing of Campanula medium champion cultivars. Acta Hortic 620:259–265CrossRefGoogle Scholar
  77. Sprengel CK (1793) Das entdeckte Geheimnis der Naturim Bau und in der Befruchtung der Blumen. Friedrich Vieweg, BerlinGoogle Scholar
  78. Sutherland BL, Quarles BM, Galloway LF (2018) Intercontinental dispersal and whole-genome duplication contribute to loss of self-incompatibility in a polyploid complex. Am J Bot 105:249–256CrossRefGoogle Scholar
  79. Tangmitcharoen S, Owens JN (1997) Floral biology, pollination, pistil receptivity, and pollen tube growth of teak (Tectona grandis Linn f.). Ann Bot 79:227–241CrossRefGoogle Scholar
  80. Vranken S, Brys R, Hoffmann M, Jacquemyn H (2014) Secondary pollen presentation and the temporal dynamics of stylar hair retraction and style elongation in Campanula trachelium (Campanulaceae). Plant Biol 16:669–676CrossRefGoogle Scholar
  81. Waser NM, Price MV (1991) Reproductive costs of self-pollination in Ipomopsis aggregata (Polemoniaceae). Am J Bot 78:1036–1043CrossRefGoogle Scholar
  82. Webb CJ, Lloyd DG (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms. II. Herkogamy. N Z J Bot 24:163–178CrossRefGoogle Scholar
  83. Wesselingh RA (2007) Pollen limitation meets resource allocation: towards a comprehensive methodology. New Phytol 174:26–37CrossRefGoogle Scholar
  84. Westerkamp C, Weber A (1997) Secondary and tertiary pollen presentation in Polygala myrtifolia and allies (Polygalaceae, South Africa). South Afr J Bot 63:254–258CrossRefGoogle Scholar
  85. Wilcock C, Neiland R (2002) Pollination failure in plants: why it happens and when it matters. Trends Plant Sci 7:270–277CrossRefGoogle Scholar
  86. Wright SI, Kalisz S, Slotte T (2013) Evolutionary consequences of self-fertilization in plants. Proc R Soc Lond B Biol Sci 280:20130133CrossRefGoogle Scholar
  87. Yang JQ, Fan YL, Jiang XF, Li QJ, Zhu XF (2018) Correlation between the timing of autonomous selfing and floral traits: a comparative study from three selfing Gentianopsis species (Gentianaceae). Sci Rep 8:3634CrossRefGoogle Scholar
  88. Young HJ, Gravitz L (2002) The effects of stigma age on receptivity in Silene alba (Caryophyllaceae). Am J Bot 89:1237–1241CrossRefGoogle Scholar

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© The Botanical Society of Japan and Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biology, Unit of BotanyUniversity of PisaPisaItaly
  2. 2.Department of Agriculture, Food and EnvironmentUniversity of PisaPisaItaly

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