Skip to main content
Springer Nature Link
Log in

Stigma–anther reciprocity, pollinators, and pollen transfer efficiency in populations of heterostylous species of Lithodora and Glandora (Boraginaceae)

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

According to Darwin, the reciprocal position of sexual whorls in heterostylous plants enhances disassortative pollen transfer between different floral morphs. It is believed that greater reciprocity between morphs will promote more efficient transfer of pollen. Additionally, efficient pollination will act as a selective force in achieving greater reciprocity between floral morphs. In this study we test whether variation in reciprocity of sexual organs between morphs is related to the efficiency of pollinators in transferring pollen between them. To do this, we first describe the pollinator’s array in several populations of species of the genus formerly known as Lithodora, which have different types of stylar polymorphism and degrees of reciprocity, and determine their abundance, plant visitation rate, number of flowers visited per plant and handling time in the population. We estimate the efficiency of the pollinator arrays by use of an approximation based on qualitative (location of pollen loads on different areas of insect bodies) and quantitative (plant visitation rate) measurements. Our results show a correlation between the degree of reciprocity and the efficiency of pollinators associated with the populations. These observations suggest that pollinators are a possible selective force driving the evolution of heterostyly.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Adler LS, Irwin RE (2006) Comparison of pollen transfer dynamics by multiple floral visitors: experiments with pollen and fluorescent dye. Ann Bot 97:141–150

    Article  PubMed  Google Scholar 

  • Aigner PA (2001) Optimality modeling and fitness trade-offs: when should plants become pollinator specialists? Oikos 95:177–184

    Article  Google Scholar 

  • Arroyo J, Dafni A (1995) Variations in habitat, season, flower traits and pollinators in dimorphic Narzissus tazetta L. (Amaryllidaceae) in Israel. New Phytol 129:135–145

    Article  Google Scholar 

  • Arroyo J, Barrett SCH, Hidalgo R, Cole WC (2002) Evolutionary maintenance of stigma-height dimorphism in Narcissus papyraceus (Amaryllidaceae). Am J Bot 89:1242–1249

    Article  Google Scholar 

  • Barrett SCH, Lloyd DG, Arroyo J (1996) Stylar polymorphisms and the evolution of heterostyly in Narcissus (Amaryllidaceae). In: Lloyd DG, Barrett SCH (eds) Floral biology. Studies on floral evolution in animal-pollinated plants. Chapman and Hall, New York, pp 339–376

    Google Scholar 

  • Brys R, Jacquemyn H, Hermy M, Beeckman T (2008) Pollen deposition and the functioning of distyly in the perennial Pulmonaria officinalis (Boraginaceae). Pl Syst Evol 273:1–12

    Article  Google Scholar 

  • Castellanos C, Wilson P, Thompson JD (2003) Pollen transfer by hummingbirds and bumblebees, and the divergence of pollination modes in Penstemon. Evolution 57:2742–2752

    PubMed  Google Scholar 

  • Castro S, Silveira P, Navarro L (2008) How does secondary pollen presentation affect the fitness of Polygala vayredae (Polygalaceae)? Am J Bot 95:706–712

    Article  Google Scholar 

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

    Google Scholar 

  • Ferrero V (2009) The ecology and evolution of floral polymorphism in Lithodora. PhD dissertation, Department of Plant Biology and Soil Sciences, University of Vigo, Pontevedra, Spain

  • Ferrero V, Arroyo J, Vargas P, Thompson JD, Navarro L (2009) Evolutionary transitions of style polymorphisms in Lithodora (Boraginaceae). Perspect Plant Ecol Evol Syst 11:111–125

    Article  Google Scholar 

  • Ferrero V, Chapela I, Arroyo J, Navarro L (2011) Reciprocal style polymorphisms are not so easily categorized: the case of heterostyly in Lithodora and Glandora (Boraginaceae). Plant Biol doi:10.1111/j.1438-8677.2009.00307.x

  • Ganders FR (1976) Pollen flow in distylous populations of Amsinckia (Boraginaceae). Can J Bot 54:2530–2535

    Article  Google Scholar 

  • Harder LD (1982) Measurement and estimation of functional proboscis length in bumblebees (Hymenoptera: Apidae). Can J Zool 60:1073–1079

    Article  Google Scholar 

  • Harder LD, Barrett SCH (1993) Pollen removal from tristylous Pontederia cordata: effects of anther position and pollinator specialization. Ecology 74:1059–1072

    Article  Google Scholar 

  • Herrera CM (1987) Components of pollinator “quality”: comparative analysis of a diverse insect assemblage. Oikos 50:79–90

    Article  Google Scholar 

  • Herrera CM (1989) Pollinator abundance, morphology, and flower visitation rate: analysis of the “quantity” component in a plant-pollinator system. Oecologia 80:241–248

    Google Scholar 

  • Inouye DW, Gill DE, Dudash MR, Fenster CB (1994) A model and lexicon for pollen fate. Am J Bot 81:1517–1530

    Article  Google Scholar 

  • Kingsolver JG, Daniel TL (1983) Mechanical determinants of nectar feeding strategy in hummingbirds: energetics, tongue morphology, and licking behavior. Oecologia 60:214–226

    Article  Google Scholar 

  • Lau P, Bosque C (2003) Pollen flow in the distylous Palicourea fendleri (Rubiaceae): an experimental test of the disassortative pollen flow hypothesis. Oecologia 135:593–600

    PubMed  Google Scholar 

  • Lloyd DG, Webb CJ (1992) The evolution of heterostyly. In: Barrett SCH (ed) Evolution and function of heterostyly. Springer-Verlag, Berlin, pp 151–178

    Google Scholar 

  • McArdle BR, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297

    Article  Google Scholar 

  • Nicholls MS (1985) Pollen flow, population composition, and the adaptive significance of distyly in Linum tenuifolium L. (Linaceae). Biol J Linn Soc 25:235–242

    Article  Google Scholar 

  • Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson GL, Solymos P, Stevens MHH, Wagner H (2008) vegan: Community Ecology Package. R package version 1.15-1. http://cran.r-project.org/, http://vegan.r-forge.r-project.org/

  • Ornduff R (1975) Heterostyly and pollen flow in Hypericum aegypticum (Guttiferae). Bot J Linn Soc 71:51–57

    Article  Google Scholar 

  • Ornduff R (1978) Features of pollen flow in dimorphic species of Lythrum section Euhyssopifolia. Am J Bot 65:1077–1083

    Article  Google Scholar 

  • Ornelas F, Jiménez L, González C, Hernández A (2004) Reproductive ecology of distylous Palicourea padifolia (Rubiaceae) in a tropical montane cloud forest. I. Hummingbirds’ effectiveness as pollen vectors. Am J Bot 91:1052–1060

    Article  Google Scholar 

  • Pailler T, Maurice S, Thompson JD (2002) Pollen transfer patterns in a distylous plant with overlapping pollen-size distributions. Oikos 99:308–316

    Article  Google Scholar 

  • Pérez-Barrales R, Vargas P, Arroyo J (2006) New evidence for the Darwinian hypothesis of heterostyly: breeding systems and pollinators in Narcissus sect. Apodanthi. New Phytol 171:553–567

    Article  PubMed  Google Scholar 

  • Pérez-Barrales R, Arroyo J, Armbruster W (2007) Differences in pollinator faunas may generate geographic differences in floral morphology and integration in Narcissus papyraceus (Amaryllidaceae). Oikos 116:1904–1918

    Article  Google Scholar 

  • Rademaker MCJ, De Jong TJ, Klinkhamer PJL (1997) Pollen dynamics of bumblebee visitation on Echium vulgare. Funct Ecol 11:554–563

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Schemske DW, Horvitz CC (1984) Variation among floral visitors in pollination ability: a precondition for mutualism specialization. Science 225:519–521

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org

  • Thomas DC, Weigend M, Hilger HH (2008) Phylogeny and systematic of Lithodora (Boraginaceae-Lithospermeae) and its affinities to the monotypic genera Mairetis, Halacsya and Paramoltkia based on ITS1 and trnLUAA–sequence data and morphology. Taxon 57:79–97

    Google Scholar 

  • Weller SG (1980) Pollen flow and fecundity in the population of Lithospermum carolinense. Am J Bot 67:1334–1341

    Article  Google Scholar 

  • Wolfe LM, Barrett SCH (1989) Patterns of pollen removal and deposition in tristylous Pontederia cordata L. (Pontederiaceae). Biol J Linn Soc 36:317–329

    Article  Google Scholar 

  • Young HJ (1988) Differential importance of beetle species pollinating Dieffenbachia longispatha (Araceae). Ecology 69:832–844

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank I. Stanescu, G. Carvallo, B. Negrea, I. Chapela, B. Molinos, A. Vale, and D. Rojas for their help in collecting field data, D. Rojas, A. Vale, J.M. Gómez, and J. Fernández for their comments and help with the statistical analysis, F. Torres and J. Bosh for their help with insect identification, and J. Arroyo for his revision and useful comments. This research was supported by the Spanish Dirección General de Investigación, Ciencia y Técnología (DGICYT) through Projects CGL2006-13847-CO2-02 and CGL2009-10466, the Agencia Española de Cooperación Internacional (AECI) through Projects A/6962/06 and A/017570/08, and the Xunta de Galicia through Project PGIDT04PXIC31003PN. The Ministerio de Educación y Ciencia (MEC) financed the work of V. Ferrero through a PhD scholarship (AP-2004-6394) together with the Fundación Ramón Areces; and the Portuguese Foundation for Science and Technology financed the work of S. Castro (BPD/41200/2007).

Author information

Authors and Affiliations

  1. Centre for Functional Ecology and Department of Life Sciences, Faculty of Sciences and Technology, University of Coimbra, Calçada Martins de Freitas, PO Box 3046, 3001-401, Coimbra, Portugal

    Victoria Ferrero & Sílvia Castro

  2. Department of Plant Biology and Soil Sciences, Faculty of Biology, University of Vigo, As Lagoas-Marcosende, 36310, Vigo, Spain

    Victoria Ferrero, José M. Sánchez & Luis Navarro

Authors
  1. Victoria Ferrero
    View author publications

    Search author on:PubMed Google Scholar

  2. Sílvia Castro
    View author publications

    Search author on:PubMed Google Scholar

  3. José M. Sánchez
    View author publications

    Search author on:PubMed Google Scholar

  4. Luis Navarro
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Victoria Ferrero.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ferrero, V., Castro, S., Sánchez, J.M. et al. Stigma–anther reciprocity, pollinators, and pollen transfer efficiency in populations of heterostylous species of Lithodora and Glandora (Boraginaceae). Plant Syst Evol 291, 267–276 (2011). https://doi.org/10.1007/s00606-010-0387-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-010-0387-x

Keywords

Profiles

  1. Sílvia Castro View author profile
  2. Luis Navarro View author profile