Skip to main content

Advertisement

SpringerLink
Log in

Pollination ecology in the narrow endemic winter-flowering Primula allionii (Primulaceae)

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Reduction of pollen flow can affect plant abundance and population viability and cause selection on plant mating system and floral traits. Little is known on the effect of this phenomenon in species naturally restricted to small and isolated habitats, that may have developed strategies to cope with long-term isolation and small population size. We investigated the pollination ecology of the endemic distylous winter-flowering P. allionii to verify the possible limitation of female fitness due to reduced pollinator visits. We recorded a higher production of pollen grains in long-styled morph, and a higher seed set in short-styled morph. The high intra-morph variability of sexual organ position may explain the hybridization phenomena allowing and easier intra-morph pollination. The fruit set is constant, although its winter-flowering period might decrease pollen transfer. Nevertheless, the lower competition for pollinators with neighbouring plants and the long-lasting anthesis may offset its reproductive success. Even if our results show no evidence of imminent threats, changes in plant–pollinator interactions might increase inbreeding, resulting in an increased extinction risk.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ågren J (1996) Population size, pollinator limitation, and seed set in the self-incompatible herb Lythrum salicaria. Ecology 77:1779–1790

    Article  Google Scholar 

  • Aronne G, Buonanno M, De Micco V, Giovanetti M, Arena C (2011) Effect of environmental factors on morpho-functional traits of Primula palinuri Petagna (Primulaceae). Bollettino dei Musei ed Istituti Biologici dell’Università di Genova 73:174

  • Barbi S (2008) Studi di biologia riproduttiva per la conservazione di alcune specie vegetali dell’ambiente mediterraneo e per la valorizzazione di produzioni eco-compatibili. PhD Thesis. University of Naples. XXI cycle

  • Barbi S, Aronne G, De Micco V (2007) Successo riproduttivo, germinazione dei semi e strategie di attecchimento delle plantule di Primula palinuri Petagna (Primulaceae) 102° Congresso S.B.I. (Palermo, 26–29 settembre 2007), p 255

  • Barrett SCH (2002) The evolution of plant sexual diversity. Nature 3:274–284

    CAS  Google Scholar 

  • Barrett SCH, Jesson LK, Baker AM (2000) The evolution and function of stylar polymorphisms in flowering plants. Ann Bot Lond 85 (Suppl A):253–265

    Google Scholar 

  • Becker T, Voss N, Durka W (2011) Pollen limitation and inbreeding depression in an ‘old rare’ bumblebee-pollinated grassland herb. Plant Biol 13:857–864

    Article  CAS  PubMed  Google Scholar 

  • Bernhardt CE, Mitchell RJ, Michaelsy HJ (2008) Effects of population size and density on pollinator visitation, pollinator behavior, and pollen tube abundance in Lupinus perennis. Int J Plant Sci 169:944–953

    Article  Google Scholar 

  • Boyd M, Silvertown J, Trucker C (1990) Population ecology of heterostyle and homostyle Primula vulgaris, growth, survival and reproduction in field populations. J Ecol 78:799–813

    Article  Google Scholar 

  • Brys R, Jacquemyn H, Endels P, Hermy M, De Blust G (2003) The relationship between reproductive success and demographic structure in remnant populations of Primula veris. Acta Oecol 24:247–253

    Article  Google Scholar 

  • Brys R, Jacquemyn H, De Bruyn L, Hermy M (2007) Pollination success and reproductive output in experimental populations of the self-incompatible Primula vulgaris. Int J Plant Sci 168:571–578

    Article  Google Scholar 

  • Brys R, Jacquemyn H, Beeckman T (2008) Morph-ratio variation, population size and female reproductive success in distylous Pulmonaria officinalis (Boraginaceae). J Evol Biol 21:1281–1289

    Article  CAS  PubMed  Google Scholar 

  • Burnat E. (1897) Notes sur les jardins botaniques alpins. Bulletins des travaux de la Société Murithienne du Valais 26(append):1–16

  • Byers DL (1995) Pollen quantity and quality as explanations for low seed set in small populations exemplified by Eupatorium (Asteraceae). Am J Bot 82:1000–1006

    Article  Google Scholar 

  • Casazza G, Granato L, Minuto L, Conti E (2012) Polyploid evolution and Pleistocene glacial cycles: a case study from the alpine primrose Primula marginata (Primulaceae). BMC Evol Biol 12:56

    Article  PubMed Central  PubMed  Google Scholar 

  • Casazza G, Marsili S, Granato L, Conti E, Noble V, Selvaggi A, Minuto L (2013) Distribution range and ecological niche of Primula marginata Curtis (Primulaceae). Pl Biosyst. doi:10.1080/11263504.2012.760495

    Google Scholar 

  • Chen M (2009) Comparative reproductive biology of Primula merrilliana Schltr. and P. cicutariifolia Pax. Plant Syst Evol 278:23–32

    Article  Google Scholar 

  • Conti F, Manzi A, Pedrotti F (1992) Libro Rosso delle Piante d’Italia. WWF, Roma

    Google Scholar 

  • Conti F, Manzi A, Pedrotti F (1997) Liste Rosse Regionali delle Piante d’Italia. WWF, Camerino

    Google Scholar 

  • Cook BI, Wolkovich EM, Parmesan C (2012) Divergent responses to spring and winter warming drive community level flowering trends. Proc Natl Acad Sci USA 109:9000–9005

    Article  CAS  PubMed  Google Scholar 

  • Cozzolino S, Widmer A (2005) Orchid diversity, an evolutionary consequence of deception? Trends Ecol Evol 20:487–494

    Article  PubMed  Google Scholar 

  • Darwin C (1877) The different forms of flowers on plants of the same species. John Murray, London

    Book  Google Scholar 

  • de Vos JM, Keller B, Isham ST, Kelso S, Conti E (2012) Reproductive implications of herkogamy in homostylous primroses: variation during anthesis and reproductive assurance in alpine environments. Funct Ecol 26:854–865

    Article  Google Scholar 

  • Dodd ME, Silvertown J, Chase MW (1999) Phylogenetic analysis of trait evolution and species diversity variation among angiosperm families. Evolution 53:732–744

    Article  Google Scholar 

  • Eckert CG, Barrett SCH (1994) Post-pollination mechanism and the maintenance of outcrossing in self-compatible, tristylous, Decodon verticillatus (Lythraceae). Heredity 72:396–411

    Article  Google Scholar 

  • Eckert CG, Kalisz S, Geber MA, Sargent R, Elle E, Cheptou P-O, Goodwillie C, Johnston MO, Kelly JK, Moeller DA, Porcher E, Ree RH, Vallejo-Marin M, Winn AA (2010) Plant mating systems in a changing world. Trends Ecol Evol 25:35–43

    Article  PubMed  Google Scholar 

  • Eriksson O, Bremer B (1991) Fruit characteristics, life forms, and species richness in the plant family Rubiaceae. Am Nat 138:751–761

    Article  Google Scholar 

  • Fey L (1929) Untersuchungen zur Phananalyse der Artbastardes Primula variabilis Goupil (P. veris L. em. Hudson × P. vulgaris Hudson), der Eltemarten und von Primula elatior (L.) Schreber. Institut fur Allgemeine Botanik der Universitat Zurich II. Serie No.10

  • Fisogni A, Cristofolini G, Podda L, Galloni M (2011) Reproductive ecology in the endemic Primula apennina Widmer (Primulaceae). Plant Biosyst 145:353–361

    Article  Google Scholar 

  • García-Robledo C, Mora F (2007) Pollination biology and the impact of floral display, pollen donors, and distyly on seed production in Arcytophyllum lavarum (Rubiaceae). Plant Biol 9:453–461

    Article  PubMed  Google Scholar 

  • Gilman RT, Fabina NS, Abbott KC, Rafferty NE (2012) Evolution of plant–pollinator mutualisms in response to climate change. Evol Appl 5:2–16

    Article  PubMed Central  Google Scholar 

  • Giménez-Benavides L, Garcia-Camacho R, Maria Iriondo J, Escudero A (2011) Selection on flowering time in Mediterranean high-mountain plants under global warming. Evol Ecol 25:777–794

    Article  Google Scholar 

  • Gordo O, Sanz JJ (2010) Impact of climate change on plant phenology in Mediterranean ecosystems. Global Change Biol 16:1082–1106

    Article  Google Scholar 

  • Harder LD, Aizen MA (2010) Floral adaptation and diversification under pollen limitation. Phil Trans R Soc B 365:529–543

    Article  PubMed  Google Scholar 

  • Internicola AI, Bernasconi G, Gigord LDB (2008) Should food-deceptive species flower before or after rewarding species? An experimental test of pollinator visitation behaviour under contrasting phenologies. J Evol Biol 21:1358–1365

    Article  CAS  PubMed  Google Scholar 

  • Jennersten O (1988) Pollination in Dianthus deltoides (Caryophyllaceae), effects of habitat fragmentation on visitation and seed set. Conserv Biol 2:359–366

    Article  Google Scholar 

  • Johnson SD, Steiner KE (2000) Generalisation versus specialization in plant pollination systems. Trends Ecol Evol 15:140–143

    Article  PubMed  Google Scholar 

  • Kálmán K, Medvegy A, Pénzes ZS, Mihalik E (2007) Morph-specific variation of floral traits associated with reciprocal herkogamy in natural populations of Primula vulgaris and Primula veris. Plant Syst Evol 268:15–27

    Article  Google Scholar 

  • Kay QON, Daoud HS, Stirton CH (1981) Pigment distribution, light reflection and cell structure in petals. Bot J Linn Soc 83:57–84

    Article  CAS  Google Scholar 

  • Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant–pollinator interactions. Annu Rev Ecol Syst 29:83–112

    Article  Google Scholar 

  • Keller B, de Vos JM, Conti E (2012) Decrease of sexual organ reciprocity between heterostylous primrose species, with possible functional and evolutionary implications. Ann Bot 110:1233–1244

    Article  PubMed  Google Scholar 

  • Kéry M, Matthies D, Schmid B (2003) Demographic stochasticity in population fragments of the declining distylous perennial Primula veris (Primulaceae). Basic Appl Ecol 4:197–206

    Article  Google Scholar 

  • Liu Y, Mu J, Niklas KJ, Li G, Sun S (2012) Global warming reduces plant reproductive output for temperate multi-inflorescence species on the Tibetan plateau. New Phytol 195:427–436

    Article  PubMed  Google Scholar 

  • Martini E (1994) Ricerche geobotaniche su Moehringia lebrunii Merxm. e Primula allionii Loisel. Endemismi ristretti delle Alpi Marittime. Rev Valdôtaine d’Hist Naturelle 48:229–236

    Google Scholar 

  • Matsumura C, Washitani I (2002) Heterostylous morph differences in pollen transfer and deposition patterns in Primula sieboldii on a visitation by a queen bumblebee, measured with a semi-natural experimental system. Plant Species Biol 17:1–12

    Article  Google Scholar 

  • Minuto L, Guerrina M, Roccotiello E, Casazza G (2012a) Demographic structure and reproductive success of Primula allionii, a plant endemic to Maritime Alps. Bollettino dei Musei ed Istituti Biologici dell’Università di Genova 74:38–54

    Google Scholar 

  • Minuto L, Guerrina M, Roccotiello E, Casazza G (2012b) Reproductive efficiency of Primula allionii: is this endemic really threatened? Bollettino dei Musei ed Istituti Biologici dell’Università di Genova 74:87–106

    Google Scholar 

  • Nishihiro J, Washitani I (2011) Post-pollination process in a partially self-compatible distylous plant, Primula sieboldii (Primulaceae). Plant Species Biol 26:213–220

    Article  Google Scholar 

  • Nuttman C, Willmer P (2003) How does insect visitation trigger floral colour change? Ecol Entomol 28:467–474

    Article  Google Scholar 

  • Olivier L, Galland JP, Maurin H (1995) Livre Rouge de la flore menacée de France. Tome I: Espèces prioritaires. Collection Patrimoines Naturels (Série Patrimoine Génétique). n°20. SPN-IEGB/MNHN, DNP/Ministère Environnement, CBN Porquerolles, Paris, 486 pp

  • Pailler T, Thompson JD (1997) Distyly and variation in heteromorphic incompatibility in Gaertnera vaginata (Rubiaceae) endemic to La Reunion Island. Am J Bot 84:315–327

    Article  CAS  PubMed  Google Scholar 

  • Phillips RD, Hopper SD, Dixon KW (2010) Pollination ecology and the possible impacts of environmental change in the Southwest Australian Biodiversity Hotspot. Phil Trans R Soc B 365:517–528

    Article  PubMed  Google Scholar 

  • Piper JG, Charlesworth B (1986) The evolution of distyly in Primula vulgaris. Biol J Linn Soc 29:123–137

    Article  Google Scholar 

  • Proctor M, Yeo P, Lack A (1996) The natural history of pollination. Timber Press, Portland

    Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org

  • Raine NE, Chittka L (2007) The adaptive significance of sensory bias in a foraging context: floral colour preferences in the bumblebee Bombus terrestris. PLoS ONE 2:e556

    Article  PubMed Central  PubMed  Google Scholar 

  • Richards AJ (2003) Primula. Timber Press, New York

    Google Scholar 

  • Sage TL, Strumas F, Cole WW, Barrett SCH (1999) Differential ovule development following self- and cross-pollination, the basis of self-sterility in Narcissus triandrus (Amaryllidaceae). Am J Bot 86:855–870

    Article  CAS  PubMed  Google Scholar 

  • Sanchez JM, Ferrero V, Navarro L (2008) A new approach to the quantification of degree of reciprocity in distylous (sensu lato) plant populations. Ann Bot Lond 102:463–472

    Article  Google Scholar 

  • Schou O (1983) The distyly in Primula elatior (L.) Hill (Primulaceae), with a study of flowering phenology and pollen flow. Bot J Linn Soc 86:261–274

    Article  Google Scholar 

  • Schultze-Motel P, Lamprecht I (1994) Correlation of sound generation and metabolic heat flux in the bumblebee Bombus lapidarius. J Exp Biol 187:315–318

    PubMed  Google Scholar 

  • Shao JW, Zhang XP, Zhang ZX, Zhu GP (2008) Identification of effective pollinators of Primula merrilliana and effects of flower density and population size on pollination efficiency. J Syst Evol 46:537–544

    Google Scholar 

  • StatSoft Inc. (2007) Statistica (data analysis software system) version 8.0. Available from URL. http://www.statsoft.com

  • Stelzer RJ, Chittka L, Carlton M, Ings TC (2010) Winter active bumblebees (Bombus terrestris) achieve high foraging rates in urban Britain. PLoS ONE 5:e9559

    Article  PubMed Central  PubMed  Google Scholar 

  • Thompson JD, Arroyo J (2009) Variations on a Darwinian theme: evolutionary transitions to heterostyly. In: Cristofolini G, Managlia A (eds) Il giardino di Darwin. L’evoluzione delle piante. Umberto Allemandi & C, Torino, pp186–200

  • Van Rossum F, De Sousa SC, Triest L (2006) Morph-specific differences in reproductive success in the distylous Primula veris in a context of habitat fragmentation. Acta Oecol 30:426–433

    Article  Google Scholar 

  • Washitani I (1996) Predicted genetic consequences of strong fertility selection due to pollinator loss in an isolated population of Primula sieboldii. Cons Biol 10:59–64

    Article  Google Scholar 

  • Washitani I, Kato M, Nishihiro J, Suzuki K (1994) Importance of queen bumble bees as pollinators facilitating inter-morph crossing in Primula sieboldii. Plant Species Biol 9:169–176

    Article  Google Scholar 

  • Wiens D, Slaton MR (2011) The mechanism of background extinction. Biol J Linn Soc 105:255–268

    Article  Google Scholar 

  • Wolff D, Liede-Schumann S (2007) Evolution of flower morphology, pollen dimorphism, and nectar composition in Arcytophyllum, a distylous genus of Rubiaceae. Org Div Evol 7:106–123

    Article  Google Scholar 

  • Woodell SRJ (1960) What pollinates Primulas? New Sci 8:568–571

    Google Scholar 

  • Zhang L-B, Comes HP, Kadereit JW (2004) The temporal course of Quaternary diversification in the European high mountain endemic Primula sect. Auricula (Primulaceae). Int J Plant Sci 165:191–207

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to G. Troiano (DISTAV, University of Genoa) for insect identification. Special thanks to R. Poggi (Genoa Natural Science Museum) for providing the insects used for measurements. We thank the anonymous reviewers and editor for their valuable comments.

Author information

Authors and Affiliations

  1. DISTAV, Polo Botanico Hanbury, Università degli Studi di Genova, C.so Dogali 1M, 16136, Genoa, Italy

    Luigi Minuto, Maria Guerrina, Enrica Roccotiello, Nicolò Roccatagliata, Mauro Giorgio Mariotti & Gabriele Casazza

Authors
  1. Luigi Minuto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria Guerrina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Enrica Roccotiello
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nicolò Roccatagliata
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mauro Giorgio Mariotti
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gabriele Casazza
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luigi Minuto.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Minuto, L., Guerrina, M., Roccotiello, E. et al. Pollination ecology in the narrow endemic winter-flowering Primula allionii (Primulaceae). J Plant Res 127, 141–150 (2014). https://doi.org/10.1007/s10265-013-0588-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-013-0588-9

Keywords

Search

Navigation