Skip to main content
SpringerLink
Log in

Temporal stability of pollinator preference in an alpine plant community and its implications for the evolution of floral traits

  • Plant-Animal interactions - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

A traditional view of diverse floral traits is that they reflect differences in foraging preferences of pollinators. The role of pollinators in the evolution of floral traits has been questioned recently by broad community surveys, especially studies concerning variation in pollinator assemblages and visitation frequency, which suggest a diminished role of pollinators in floral evolution. Here, we investigate the relationships between six categories of floral traits of 29 species and 10 pollinator functional groups in an alpine meadow in the Hengduan Mountains of China, over three consecutive years. Simpson’s diversity index was used to estimate the level of pollinator generalization of each plant species by considering both pollinator groups and their relative visitation frequencies. Multivariate analyses indicated that eight of the ten pollinator groups showed constant preferences for at least two floral traits, leading to a relatively stable level of ecological generalization for most floral traits (two out of three categories), despite the fact that the level of generalization of the entire community varied across years. Shape preferences of butterflies, honeybees and beeflies varied such that open flowers exhibited a lower level of ecological generalization in 2007 than closed flowers, in contrast with the other 2 years. These results suggest that temporally stabilized preferences of diverse pollinators may contribute to the evolution of specialized versus generalized floral traits; however, their role may be moderated by variation in community structure, including both the composition and abundance of plants and pollinators.

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

Similar content being viewed by others

References

  • Alarcón R, Waser NM, Ollerton J (2008) Year-to-year variation in the topology of a plant–pollinator interaction network. Oikos 117:1796–1807

    Article  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Anderson MJ (2003) XMATRIX: a FORTRAN computer program for calculating design matrices for terms in ANOVA designs in a linear model. Department of Statistics, University of Auckland, New Zealand

  • Anderson MJ (2004) DISTLM v.5: a FORTRAN computer program to calculate a distance-based multivariate analysis for a linear model. Department of Statistics, University of Auckland, New Zealand

  • Armbruster WS, Fenster CB, Dudash MR (2000) Pollination “principles” revisited: specialization, pollination syndromes, and the evolution of flowers. Det Nor Vidensk Acad I Mat Natur Kl Skr Ny Ser 39:179–200

    Google Scholar 

  • Arnold SEJ, Savolainen V, Chittka L (2009) Flower colours along an alpine altitude gradient, seen through the eyes of fly and bee pollinators. Arthropod Plant Interact 3:27–43

    Article  Google Scholar 

  • Bosch J, Retana J, Cerdá X (1997) Flowering phenology, floral traits and pollinator composition in an herbaceous Mediterranean plant community. Oecologia 109:583–591

    Article  Google Scholar 

  • Dicks LV, Corbet SA, Pywell RF (2002) Compartmentalization in plant–insect flower visitor webs. J Anim Ecol 71:32–43

    Article  Google Scholar 

  • Dupont YL, Padrón B, Olesen JM, Petanidou T (2009) Spatio-temporal variation in the structure of pollination networks. Oikos 118:1261–1269

    Article  Google Scholar 

  • Eckhart VM (1992) Spatio-temporal variation in abundance and variation in foraging behavior of the pollinators of gynodioecious Phacelia linearis (Hydrophyllaceae). Oikos 64:573–586

    Article  Google Scholar 

  • Endress PK (2001) Evolution of floral symmetry. Curr Opin Plant Biol 4:86–91

    Article  PubMed  CAS  Google Scholar 

  • Faegri K, van der Pijl L (1979) The principles of pollination ecology, 3rd edn. Pergamon, Oxford

    Google Scholar 

  • Fenster CB, Dudash MR (2001) Spatiotemporal variation in the role of hummingbirds as pollinators of Silene virginica. Ecology 82:844–851

    Google Scholar 

  • Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 35:375–403

    Article  Google Scholar 

  • Gong Y-B, Huang S-Q (2009) Floral symmetry: pollinator-mediated stabilizing selection on flower size in bilateral species. Proc R Soc Lond B 276:4013–4020

    Article  Google Scholar 

  • Harder LD, Thomson JD (1989) Evolutionary options for maximizing pollen dispersal of animal pollinated plants. Am Nat 133:323–344

    Article  Google Scholar 

  • Herrera CM (1988a) Variation in mutualisms: the spatiotemporal mosaic of a pollinator assemblage. Biol J Linn Soc 35:95–125

    Article  Google Scholar 

  • Herrera J (1988b) Pollination relationships in southern Spanish Mediterranean shrublands. J Ecol 76:274–287

    Article  Google Scholar 

  • Herrera CM (1995) Microclimate and individual variation in pollinator: flowering plants are more than their flower. Ecology 76:1516–1524

    Article  Google Scholar 

  • Herrera CM (2005) Plant generalization on pollinators: species property or local phenomenon? Am J Bot 92:13–20

    Article  Google Scholar 

  • Hingston AB, McQuillan PB (2000) Are pollination syndromes useful predictors of floral visitors in Tasmania? Austral Ecol 25:600–609

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Lázaro A, Hegland SJ, Totland Ø (2008) The relationships between floral traits and specificity of pollination systems in three Scandinavian plant communities. Oecologia 157:249–257

    Article  PubMed  Google Scholar 

  • Lázaro A, Rebekka L, Totland Ø (2009) Co-flowering neighbors influence the diversity and identity of pollinator groups visiting plant species. Oikos 118:691–702

    Article  Google Scholar 

  • Lloyd DG, Yates JMA (1982) Intrasexual selection and the segregation of pollen and stigmas in hermaphroditic plants, exemplified by Wahlenbergia albomarginata (Campanulaceae). Evolution 36:903–913

    Article  Google Scholar 

  • McCall C, Primack RB (1992) Influence of flower characteristics, weather, time of day, and season on insect visitation rates in three plant communities. Am J Bot 79:434–442

    Article  Google Scholar 

  • McDonald JH (2008) Handbook of biological statistics. Sparky House, Maryland

    Google Scholar 

  • Momose K, Yumoto T, Nagamitsu T, Kato M, Nagamasu H, Sakai S, Harrison RD, Itioka T, Hamid AA, Inoue T (1998) Pollination biology of a lowland dipterocarp forest. I. Characteristics of the plant–pollinator community in a lowland dipterocarp forest. Am J Bot 85:1477–1501

    Article  Google Scholar 

  • Nakano C, Washitani I (2003) Variability and specialization of plant–pollinator systems in a northern maritime grassland. Ecol Res 18:221–246

    Article  Google Scholar 

  • Ne’eman G, Jürgens A, Newstrom-Lloyd L, Potts SG, Dafni A (2010) A framework for comparing pollinator performance: effectiveness and efficiency. Biol Rev 85:435–451

    PubMed  Google Scholar 

  • Olesen JM, Bascompte J, Elberling H, Jordano P (2008) Temporal dynamics in a pollination network. Ecology 89:1573–1582

    Article  PubMed  Google Scholar 

  • Ollerton J, Watts S (2000) Phenotype space and floral typology: towards an objective assessment of pollination syndromes. Det Nor Vidensk Acad I Mat Natur Kl Skr Ny Ser 39:149–159

    Google Scholar 

  • Ollerton J, Killick A, Lamborn E, Watts S, Whiston M (2007) Multiple meanings and modes: on the many ways to a generalist flower. Taxonomy 56:717–728

    Article  Google Scholar 

  • Ollerton J, Alarcón R, Waser NM, Price MV, Watts S, Cranmer L, Hingston A, Peter CI, Rotenberry J (2009) A global test of the pollination syndrome hypothesis. Ann Bot 103:1471–1480

    Article  PubMed  Google Scholar 

  • Pauw A, Stofberg J, Waterman RJ (2009) Flies and flowers in Darwin’s race. Evolution 63:268–279

    Article  PubMed  Google Scholar 

  • Pellmyr O (2002) Pollination by animals. In: Herrera CM, Pellmyr O (eds) Plant–animal interactions: an evolutionary approach. Blackwell, Oxford, pp 157–184

    Google Scholar 

  • Petanidou T, Kallimanis AS, Tzanopoulos J, Sgardelis SP, Pantis JD (2008) Long-term observation of a pollination network: fluctuation in species and interactions, relative invariance of network structure and implications for estimates of specialization. Ecol Lett 11:564–575

    Article  PubMed  Google Scholar 

  • Pettersson MW (1991) Pollination by a guild of fluctuating moth populations: option for unspecialization in Silene vulgaris. J Ecol 79:594–604

    Google Scholar 

  • Reynolds RJ, Fenster CB (2008) Point and interval estimation of pollinator importance: a study using pollination data of Silene caroliniana. Oecologia 156:325–332

    Article  PubMed  Google Scholar 

  • Reynolds RJ, Westbrook MJ, Rhode AS, Cridland JM, Fenster CB, Dudash MR (2009) Pollinator specialization and pollination syndromes of three related North American Silene. Ecology 90:2077–2087

    Article  PubMed  Google Scholar 

  • Reynolds RJ, Dudash MR, Fenster CB (2010) Multiyear study of multivariate linear and nonlinear phenotypic selection on floral traits of hummingbird-pollinated Silene virginica. Evolution 64:358–369

    Article  PubMed  Google Scholar 

  • Sahli HF, Conner JK (2006) Characterizing ecological generalization in plant–pollination systems. Oecologia 148:365–372

    Article  PubMed  Google Scholar 

  • Schemske DW, Bradshaw HD (1999) Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proc Natl Acad Sci USA 96:11910–11915

    Article  PubMed  CAS  Google Scholar 

  • Schemske DW, Horvitz CC (1989) Temporal variation in selection on a floral character. Evolution 43:461–465

    Article  Google Scholar 

  • Simpson EH (1949) Measurement of diversity. Nature 163:688

    Article  Google Scholar 

  • Strauss SY, Whittall JB (2006) Non-pollinator agents of selection on floral traits. In: Harder LD, Barrett SCH (eds) Ecology and evolution of flowers. Oxford University Press, Oxford, pp 120–138

    Google Scholar 

  • Sun J-F, Gong Y-B, Renner SS, Huang S-Q (2008) Multifunctional bracts in the dove tree Davidia involucrata (Nyssaceae: Cornales): rain protection and pollinator attraction. Am Nat 171:119–124

    Article  PubMed  Google Scholar 

  • Ter Braak CJF (1994) Canonical community ordination. Part I. Basic theory and linear methods. Ecoscience 1:127–140

    Google Scholar 

  • Ter Braak CJF, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca

    Google Scholar 

  • Waser NM (2006) Specialization and generalization in plant–pollinator interaction: a historical perspective. In: Waser NM, Ollerton J (eds) Plant–pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago, pp 3–17

    Google Scholar 

  • Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060

    Article  Google Scholar 

  • Wilson P, Thomson JD (1991) Heterogeneity among floral visitors leads to discordance between removal and deposition of pollen. Ecology 72:1503–1507

    Article  Google Scholar 

  • Wolfe LM, Sowell DR (2006) Do pollination syndromes partition the pollinator community? A test using four sympatric morning glory species. Int J Plant Sci 167:1169–1175

    Article  Google Scholar 

Download references

Acknowledgments

We thank laboratory members Ji-Fan Sun, Xiao-Xin Tang, Yang Lu, Yun-Yun Mao, Chang-Qiu Liu, Qiang Fang, Cai Wei, and Huan-Le Liu for their help in the field study, Zhen-Dong Fang, Qin Xu, Zong-Ling Ma and Zi-Quan Pu from Shangri-La Alpine Botanical Garden for their logistical support, Lawrence D. Harder and Charles B. Fenster for comments on experimental design, Marti J. Anderson and Zhi-Gang Zhao for help in data analysis, and Sarah Corbet, Deren Eaton, Jeffrey Karron and three anonymous reviewers providing valuable comments on the manuscript. The experiments comply with the current laws and policy of biodiversity conservation in China. Grants from National Science Foundation of China (30770135 and 31030016) to S.Q.H. supported this work.

Author information

Authors and Affiliations

  1. College of Life Sciences, Wuhan University, Wuhan, 430072, China

    Yan-Bing Gong & Shuang-Quan Huang

Authors
  1. Yan-Bing Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shuang-Quan Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shuang-Quan Huang.

Additional information

Communicated by Jeff Karron.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 294 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gong, YB., Huang, SQ. Temporal stability of pollinator preference in an alpine plant community and its implications for the evolution of floral traits. Oecologia 166, 671–680 (2011). https://doi.org/10.1007/s00442-011-1910-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-011-1910-7

Keywords

Search

Navigation