Community-wide integration of floral colour and scent in a Mediterranean scrubland

Abstract

Angiosperm flowers have evolved a dazzling palette of colours and a rich bouquet of scents, principally serving to attract pollinators. Despite recent progress in the ecology of pollination, the sensory floral traits that are important for communication with pollinators (for example, colour and scent) have not been assessed in an unbiased, integrative sense within a community context. Nonetheless, floral sensory stimuli are known key factors that mediate flower visitation, thus affecting community dynamics. Here we show that flowers of the phrygana, a natural Mediterranean scrubland, display integrated patterns of scent composition and colour (as perceived by pollinators). Surprisingly, the data reveal predictive relationships between patterns of volatile composition and flower reflectance spectra. The presence of nectar is related to visual cues and the qualitative composition of floral aromas. Our results reveal a coordinated phenotypic integration consistent with the sensory abilities and perceptual biases of bees, suggesting potential facilitative effects for pollination and highlighting the fundamental importance of bees in Mediterranean-type ecosystems. We offer our unbiased approach as a starting point for more extensive, global investigations of the diversity of floral sensory phenotypes and its role in the community ecology of plant–pollinator interactions.

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Fig. 1: Chemical and visual floral phenotype of the insect-pollinated plants in the study community.
Fig. 2: Loci of the flowers in the study community in the colour spaces of the two visual systems tested.
Fig. 3: The seven modules of the plant–volatilome network and their chemical characterization.
Fig. 4: Floral spectral patterns associated with VOC classes.
Fig. 5: Significant relationships between chemical and colorimetric or spectral properties in the floral phenotypes of the study community.

References

  1. 1.

    Xiong, J., Fischer, W. M., Inoue, K., Nakahara, M. & Bauer, C. E. Molecular evidence for the early evolution of photosynthesis. Science 289, 1724–1730 (2000).

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    Rosenstiel, T. N., Shortlidge, E. E., Melnychenko, A. N., Pankow, J. F. & Eppley, S. M. Sex-specific volatile compounds influence microarthropod-mediated fertilization of moss. Nature 489, 431–433 (2012).

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Smith, S. D. Pleiotropy and the evolution of floral integration. New Phytol. 209, 80–85 (2016).

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Leonard, A. S., Dornhaus, A. & Papaj, D. R. in Evolution of Plant–Pollinator Relationships (ed. Patiny, S.) 279–300 (Cambridge Univ. Press, Cambridge, 2012).

  5. 5.

    Raguso, R. A. Wake up and smell the roses: the ecology and evolution of floral scent. Annu. Rev. Ecol. Evol. S. 39, 549–569 (2008).

    Article  Google Scholar 

  6. 6.

    Srinivasan, M. V., Zhang, S. W. & Zhu, H. Honeybees link sights to smells. Nature 396, 637–638 (1998).

    CAS  Article  Google Scholar 

  7. 7.

    Parachnowitsch, A. L., Raguso, R. A. & Kessler, A. Phenotypic selection to increase floral scent emission, but not flower size or colour in bee-pollinated Penstemon digitalis. New Phytol. 195, 667–675 (2012).

    Article  PubMed  Google Scholar 

  8. 8.

    Hopkins, R. & Rausher, M. D. Pollinator-mediated selection on flower color allele drives reinforcement. Science 335, 1090–1092 (2012).

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Murren, C. J. The integrated phenotype. Integr. Comp. Biol. 52, 64–76 (2012).

    Article  PubMed  Google Scholar 

  10. 10.

    Armbruster, W. S., Pelabon, C., Bolstad, G. H. & Hansen, T. F. Integrated phenotypes: understanding trait covariation in plants and animals. Phil. Trans. R. Soc. B 369, 20130245 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Ben Zvi, M. M. et al. Interlinking showy traits: co-engineering of scent and colour biosynthesis in flowers. Plant Biotechnol. J. 6, 403–415 (2008).

    Article  PubMed  Google Scholar 

  12. 12.

    Armbruster, W. S. Floral specialization and angiosperm diversity: phenotypic divergence, fitness trade-offs and realized pollination accuracy. AoB Plants 6, plu003 (2014).

  13. 13.

    Ordano, M., Fornoni, J., Boege, K. & Dominguez, C. A. The adaptive value of phenotypic floral integration. New Phytol. 179, 1183–1192 (2008).

    Article  PubMed  Google Scholar 

  14. 14.

    Majetic, C. J., Raguso, R. A., Tonsor, S. J. & Ashman, T. L. Flower color–flower scent associations in polymorphic Hesperis matronalis (Brassicaceae). Phytochemistry 68, 865–874 (2007).

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Kemp, D. J. et al. An integrative framework for the appraisal of coloration in nature. Am. Nat. 185, 705–724 (2015).

    Article  PubMed  Google Scholar 

  16. 16.

    Petanidou, T. & Ellis, W. N. Pollinating fauna of a phryganic ecosystem: composition and diversity. Biodivers. Lett. 1, 9–22 (1993).

    Article  Google Scholar 

  17. 17.

    Kantsa, A. Mediterranean Odorscapes: The Role of Plants’ Volatile Organic Compounds in Pollination Networks. PhD thesis, Univ. Aegean (2016).

  18. 18.

    Chittka, L., Shmida, A., Troje, N. & Menzel, R. Ultraviolet as a component of flower reflections, and the colour perception of hymenoptera. Vision Res. 34, 1489–1508 (1994).

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Briscoe, A. D. & Chittka, L. The evolution of color vision in insects. Annu. Rev. Entomol. 46, 471–510 (2001).

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    Dyer, A. G. et al. Parallel evolution of angiosperm colour signals: common evolutionary pressures linked to hymenopteran vision. Proc. R. Soc. B 279, 3606–3615 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Koshitaka, H., Kinoshita, M., Vorobyev, M. & Arikawa, K. Tetrachromacy in a butterfly that has eight varieties of spectral receptors. Proc. R. Soc. B 275, 947–954 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Petanidou, T. & Smets, E. The potential of marginal lands for bees and apiculture: nectar secretion in Mediterranean shrublands. Apidologie 26, 39–52 (1995).

    Article  Google Scholar 

  23. 23.

    Rohde, K., Papiorek, S. & Lunau, K. Bumblebees (Bombus terrestris) and honeybees (Apis mellifera) prefer similar colours of higher spectral purity over trained colours. J. Comp. Physiol. A 199, 197–210 (2013).

    Article  Google Scholar 

  24. 24.

    Poupkou, A. et al. Present climate trend analysis of the etesian winds in the Aegean Sea. Theor. Appl. Climatol. 106, 459–472 (2011).

    Article  Google Scholar 

  25. 25.

    Vereecken, N. J. et al. Pre-adaptations and the evolution of pollination by sexual deception: Cope’s rule of specialization revisited. Proc. R. Soc. B 279, 4786–4794 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Horovitz, A. Edaphic factors and flower colour distribution in the Anemoneae (Ranunculaceae). Plant Syst. Evol. 126, 239–242 (1976).

    Article  Google Scholar 

  27. 27.

    Lunau, K., Papiorek, S., Eltz, T. & Sazima, M. Avoidance of achromatic colours by bees provides a private niche for hummingbirds. J. Exp. Biol. 214, 1607–1612 (2011).

    Article  PubMed  Google Scholar 

  28. 28.

    Slessor, K. N., Winston, M. L. & Le Conte, Y. Pheromone communication in the honeybee (Apis mellifera L.). J. Chem. Ecol. 31, 2731–2745 (2005).

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Schiestl, F. P. & Johnson, S. D. Pollinator-mediated evolution of floral signals. Trends Ecol. Evol. 28, 307–315 (2013).

    Article  PubMed  Google Scholar 

  30. 30.

    Martinez-Harms, J. et al. Evidence of red sensitive photoreceptors in Pygopleurus israelitus (Glaphyridae: Coleoptera) and its implications for beetle pollination in the southeast Mediterranean. J. Comp. Physiol. A 198, 451–463 (2012).

    CAS  Article  Google Scholar 

  31. 31.

    Dafni, A. et al. Red bowl-shaped flowers—convergence for beetle pollination in the Mediterranean region. Israel J. Bot. 39, 81–92 (1990).

    Google Scholar 

  32. 32.

    Kantsa, A., Sotiropoulou, S., Vaitis, M. & Petanidou, T. Plant volatilome in Greece: a review on the properties, prospects, and chemogeography. Chem. Biodivers. 12, 1466–1480 (2015).

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Blight, M. M. et al. Identification of floral volatiles involved in recognition of oilseed rape flowers, Brassica napus by honeybees, Apis mellifera. J. Chem. Ecol. 23, 1715–1727 (1997).

    CAS  Article  Google Scholar 

  34. 34.

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

    Article  PubMed  PubMed Central  Google Scholar 

  35. 35.

    Dudareva, N. & DellaPenna, D. Plant metabolic engineering: future prospects and challenges. Curr. Opin. Biotechnol. 24, 226–228 (2013).

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Andersson, S., Nilsson, L. A., Groth, I. & Bergstrom, G. Floral scents in butterfly-pollinated plants: possible convergence in chemical composition. Bot. J. Linn. Soc. 140, 129–153 (2002).

    Article  Google Scholar 

  37. 37.

    Gershenzon, J. & Dudareva, N. The function of terpene natural products in the natural world. Nat. Chem. Biol. 3, 408–414 (2007).

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Junker, R. R. & Blüthgen, N. Floral scents repel facultative flower visitors, but attract obligate ones. Ann. Bot. 105, 777–782 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Banks, J. A. et al. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332, 960–963 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Hansson, B. S. & Stensmyr, M. C. Evolution of insect olfaction. Neuron 72, 698–711 (2011).

    CAS  Article  PubMed  Google Scholar 

  41. 41.

    Renoult, J. P., Valido, A., Jordano, P. & Schaefer, H. M. Adaptation of flower and fruit colours to multiple, distinct mutualists. New Phytol. 201, 678–686 (2014).

    Article  PubMed  Google Scholar 

  42. 42.

    Sargent, R. D. & Ackerly, D. D. Plant–pollinator interactions and the assembly of plant communities. Trends Ecol. Evol. 23, 123–130 (2008).

    Article  PubMed  Google Scholar 

  43. 43.

    Ashman, T. L. & Arceo-Gomez, G. Toward a predictive understanding of the fitness costs of heterospecific pollen receipt and its importance in co-flowering communities. Am. J. Bot. 100, 1061–1070 (2013).

    Article  PubMed  Google Scholar 

  44. 44.

    Junker, R. R. & Parachnowitsch, A. L. Working towards a holistic view on flower—how floral scents mediate plant–animal interactions in concert with other floral characters. J. Indian I. Sci. 91, 43–67 (2015).

    Google Scholar 

  45. 45.

    Armbruster, W. S. The specialization continuum in pollination systems: diversity of concepts and implications for ecology, evolution and conservation. Funct. Ecol. 31, 88–100 (2017).

    Article  Google Scholar 

  46. 46.

    Waser, N. M., Chittka, L., Price, M. V., Williams, N. M. & Ollerton, J. Generalization in pollination systems, and why it matters. Ecology 77, 1043–1060 (1996).

    Article  Google Scholar 

  47. 47.

    Hubbell, S. P. The Unified Neutral Theory of Biodiversity and Biogeography Vol. 32 (Princeton Univ. Press, Princeton and Oxford, 2001).

  48. 48.

    Kallimanis, A. S., Petanidou, T., Tzanopoulos, J., Pantis, J. D. & Sgardelis, S. P. Do plant–pollinator interaction networks result from stochastic processes? Ecol. Model. 220, 684–693 (2009).

    Article  Google Scholar 

  49. 49.

    Encinas-Viso, F., Revilla, T. A. & Etienne, R. S. Phenology drives mutualistic network structure and diversity. Ecol. Lett. 15, 198–208 (2012).

    Article  PubMed  Google Scholar 

  50. 50.

    Bascompte, J., Jordano, P., Melian, C. J. & Olesen, J. M. The nested assembly of plant–animal mutualistic networks. Proc. Natl Acad. Sci. USA 100, 9383–9387 (2003).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. 51.

    Euro+Med PlantBase - The Information Resource for Euro-Mediterranean Plant Diversity (Euro+Med, Berlin-Dahlem, 2006); http://ww2.bgbm.org/EuroPlusMed/.

  52. 52.

    Kaiser, R. & Kraft, P. Neue und ungewöhnliche Naturstoffe faszinierender Blütendüfte. Chem. Unserer Zeit 1, 8–23 (2001).

    Article  Google Scholar 

  53. 53.

    Arnold, S. E. J., Faruq, S., Savolainen, V., McOwan, P. W. & Chittka, L. FReD: the floral reflectance database—a web portal for analyses of flower colour. PLoS ONE 5, e14287 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Shrestha, M., Dyer, A. G., Bhattarai, P., Burd, M. & Shefferson, R. Flower colour and phylogeny along an altitudinal gradient in the Himalayas of Nepal. J. Ecol. 102, 126–135 (2014).

    Article  Google Scholar 

  55. 55.

    Perry, M. et al. Molecular logic behind the three-way stochastic choices that expand butterfly colour vision. Nature 535, 280–284 (2016).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Stoddard, M. C. & Prum, R. O. Evolution of avian plumage color in a tetrahedral color space: a phylogenetic analysis of new world buntings. Am. Nat. 171, 755–776 (2008).

    Article  PubMed  Google Scholar 

  57. 57.

    Bremer, B. et al. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot. J. Linn. Soc. 161, 105–121 (2009).

    Article  Google Scholar 

  58. 58.

    Webb, C. O. & Donoghue, M. J. Phylomatic: tree assembly for applied phylogenetics. Mol. Ecol. Notes 5, 181–183 (2005).

    Article  Google Scholar 

  59. 59.

    Webb, C. O., Ackerly, D. D. & Kembel, S. W. Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24, 2098–2100 (2008).

    CAS  Article  PubMed  Google Scholar 

  60. 60.

    Blomberg, S. P., Garland, T. Jr & Ives, A. R. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57, 717–745 (2003).

    Article  PubMed  Google Scholar 

  61. 61.

    Fritz, S. A. & Purvis, A. Selectivity in mammalian extinction risk and threat types: a new measure of phylogenetic signal strength in binary traits. Conserv. Biol. 24, 1042–1051 (2010).

    Article  PubMed  Google Scholar 

  62. 62.

    Paleo-López, R. et al. A phylogenetic analysis of macroevolutionary patterns in fermentative yeasts. Ecol. Evol. 6, 3851–3861 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  63. 63.

    Wang, Y., Naumann, U., Wright, S., Eddelbuettel, D. & Warton, D. mvabund: Statistical Methods for Analysing Multivariate Abundance Data. R package version 3.11.9 (R Foundation for Statistical Computing, Vienna, 2016); https://CRAN.R-project.org/package=mvabund.

  64. 64.

    Wang, Y., Naumann, U., Wright, S. T. & Warton, D. I. mvabund—an R package for model-based analysis of multivariate abundance data. Methods Ecol. Evol. 3, 471–474 (2012).

    Article  Google Scholar 

  65. 65.

    Guimerà, R. & Nunes Amaral, L. A. Functional cartography of complex metabolic networks. Nature 433, 895–900 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  66. 66.

    Freckleton, R. P., Harvey, P. H. & Pagel, M. Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 160, 712–726 (1985).

    Article  Google Scholar 

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Acknowledgements

This research was co-financed by the European Union (European Social Fund) and Greek national funds through the operational programme ‘Education and Lifelong Learning’ of the National Strategic Reference Framework – Research Funding Program: Heraclitus II (2324-1/WP17/30340). A.K. and T.P. are grateful to T. Lekkas, M. Aloupi, T. Tscheulin, P. Davies, T. Kallimanis, O. Davias, Korres S.A. Natural Products, O.-I. Kalantzi and P. Magiatis for multifaceted support.

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A.K. and T.P. designed the study. A.K. collected the data and performed chemical analyses. A.K., A.G.D., R.A.R. and S.P.S. analysed the data. The manuscript was written primarily by A.K. with major contributions by all other co-authors.

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Correspondence to Aphrodite Kantsa.

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Kantsa, A., Raguso, R.A., Dyer, A.G. et al. Community-wide integration of floral colour and scent in a Mediterranean scrubland. Nat Ecol Evol 1, 1502–1510 (2017). https://doi.org/10.1038/s41559-017-0298-0

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