Journal of Chemical Ecology

, Volume 41, Issue 12, pp 1095–1104 | Cite as

Diel Variation in Flower Scent Reveals Poor Consistency of Diurnal and Nocturnal Pollination Syndromes in Sileneae

  • Samuel Prieto-BenítezEmail author
  • Stefan Dötterl
  • Luis Giménez-Benavides


The composition of flower scent and the timing of emission are crucial for chemical communication between plants and their pollinators; hence, they are key traits for the characterization of pollination syndromes. In many plants, however, plants are assigned to a syndrome based on inexpensive to measure flower traits, such as color, time of flower opening, and shape. We compared day and night scents from 31 Sileneae species and tested for quantitative and semi-quantitative differences in scent among species classified a priori as diurnal or nocturnal. As most Sileneae species are not only visited by either diurnal or nocturnal animals as predicted by their syndrome, we hypothesized that, even if flower scent were preferentially emitted during the day or at night, most species also would emit some scents during the opposing periods of the day. This phenomenon would contribute to the generalized assemblage of flower visitors usually observed in Sileneae species. We found that diel variations of scent often were not congruent with the syndrome definition, but could partially be explained by taxonomy and sampling times. Most species emitted compounds with attractive potential to insects during both the night and day. Our results highlight the current opinion that syndromes are not watertight compartments evolved to exclude some flower visitors. Thus, important information may be lost when scents are collected either during day- or night-time, depending on the a priori classification of the species as diurnal or nocturnal.


Silene Floral scent Nyctinasty Pollination syndrome 



We thank the seed banks and botanical gardens listed in Table 1 for providing seeds and M. Buide and E. Narbona for sampling the Sect. Psammophilae. We also thank J. L. Margalet for caring for the plants. This work was supported by the MINECO research project of the Spanish Government [CGL2009-08755].

Supplementary material

10886_2015_645_MOESM1_ESM.docx (96 kb)
ESM 1 (DOCX 95.8 kb)
10886_2015_645_MOESM2_ESM.docx (17 kb)
ESM 2 (DOCX 17.3 kb)


  1. Adams RP (2008) Identification of essential oil components by gas chromatography/mass spectrometry. Allured Publishing Corporation, Carol Stream, IL, USAGoogle Scholar
  2. Anderson MJ, Gorley RN, Clark KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, PlymouthGoogle Scholar
  3. Andersson S (2003) Antennal responses to floral scents in the butterflies Inachis io, aglais urticae (Nymphalidae), and Gonepteryx rhamni (Pieridae). Chemoecology 13:13–20CrossRefGoogle Scholar
  4. Armbruster S, Fenster C, Dudash M (2000) Pollination'principles' revisited: specialization, pollination syndromes, and the evolution of flowers. The Scandinavian Association for Pollination Ecology Honours Knut Faegri 39:179–200Google Scholar
  5. Bergström G, Birgersson G, Groth I, Nilsson LA (1992) Floral fragrance disparity between three taxa of lady's slipper Cypripedium calceolus (Orchidaceae). Phytochemistry 31:2315–2319CrossRefGoogle Scholar
  6. Bittrich V (1993) Caryophyllaceae. In: Kubitzki K, Rohwer G, Bittrich V (eds) Flowering plants· dicotyledons. Springer, Berlin Heidelberg, pp. 206–236CrossRefGoogle Scholar
  7. Brittain C, Williams N, Kremen C, Klein AM (2013) Synergistic effects of non-apis bees and honey bees for pollination services. Proc R Soc B 280:20122767PubMedCentralCrossRefPubMedGoogle Scholar
  8. Byers KJ, Vela JP, Peng F, Riffell JA, Bradshaw HD (2014) Floral volatile alleles can contribute to pollinator-mediated reproductive isolation in monkeyflowers (Mimulus). The Plant Journal 80:1031–1042PubMedCentralCrossRefPubMedGoogle Scholar
  9. Castillo DM, Kula AAR, Dötterl S, Dudash MR, Fenster CB (2014) Invasive Silene latifolia may benefit from a native pollinating seed predator, Hadena ectypa, in North America. Int J Plant Sci 175:80–91CrossRefGoogle Scholar
  10. Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E Ltd, Plymouth, UKGoogle Scholar
  11. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E Ltd, PlymouthGoogle Scholar
  12. Desfeux C, Lejeune B (1996) Systematics of euromediterranean Silene (Caryophyllaceae): evidence from a phylogenetic analysis using ITS sequences. C R Acad Sci, Ser III 319:351–358Google Scholar
  13. Dobson HEM (2006) Relationship between floral fragrance composition and type of pollinator. In: Dudareva N, Pichersky E (eds) Biology of floral scent. Taylor & Francis Group, Boca Raton, pp. 147–198CrossRefGoogle Scholar
  14. Dötterl S, Jürgens A (2005) Spatial fragrance patterns in flowers of Silene latifolia: lilac compounds as olfactory nectar guides? Plant Syst Evol 255:99–109CrossRefGoogle Scholar
  15. Dötterl S, Wolfe LM, Jürgens A (2005) Qualitative and quantitative analyses of flower scent in Silene latifolia. Phytochemistry 66:203–213CrossRefPubMedGoogle Scholar
  16. Dötterl S, Jürgens A, Seifert K, Laube T, Weissbecker B, Schütz S (2006) Nursery pollination by a moth in Silene latifolia: the role of odours in eliciting antennal and behavioural responses. New Phytol 169:707–718CrossRefPubMedGoogle Scholar
  17. Dötterl S, Jahreiß K, Jhumur US, Jürgens A (2012) Temporal variation of flower scent in Silene otites (Caryophyllaceae): a species with a mixed pollination system. Bot J Linn Soc 169:447–460CrossRefGoogle Scholar
  18. Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 35:375–403CrossRefGoogle Scholar
  19. Feulner M, Pointner S, Heuss L, Aas G, Paule J, Dötterl S (2014) Floral scent and its correlation with AFLP data in Sorbus. Org Divers Evol 14:339–348CrossRefGoogle Scholar
  20. Fishbein M, Venable DL (1996) Diversity and temporal change in the effective pollinators of Asclepias tuberosa. Ecology 77:1061–1073CrossRefGoogle Scholar
  21. Giménez-Benavides L, Dötterl S, Jürgens A, Escudero A, Iriondo JM (2007) Generalist diurnal pollination provides greater fitness in a plant with nocturnal pollination syndrome: assessing the effects of a Silene-Hadena interaction. Oikos 116:1461–1472Google Scholar
  22. Greenberg AK, Donoghue MJ (2011) Molecular systematics and character evolution in Caryophyllaceae. Taxon:1637–1652.Google Scholar
  23. Gregg KB (1983) Variation in floral fragrances and morphology: incipient speciation in Cycnoches? Bot Gaz 144:566–576CrossRefGoogle Scholar
  24. Greuter W (1995) Silene (caryophyllaceae) in Greece: a subgeneric and sectional classification. Taxon 44:543–581CrossRefGoogle Scholar
  25. Harbaugh DT, Nepokroeff M, Rabeler RK, McNeill J, Zimmer EA, Wagner WL (2010) A new lineage-based tribal classification of the family Caryophyllaceae. Int J Plant Sci 171:85–198CrossRefGoogle Scholar
  26. Herrera CM (1996) Floral traits and plant adaptation to insect pollinators: a devil’s advocate approach. In: Barrett S (ed) Lloyd D. Floral Biology, Springer US, pp. 65–87Google Scholar
  27. Honda K, Ômura H, Hayashi N (1998) Identification of floral volatiles from Ligustrum japonicum that stimulate flower-visiting by cabbage butterfly, Pieris rapae. J Chem Ecol 24:2167–2180CrossRefGoogle Scholar
  28. Javorek SK, Mackenzie KE, Vander Kloet SP (2002) Comparative pollination effectiveness among bees (Hymenoptera: Apoidea) on lowbush blueberry (Ericaceae: Vaccinium angustifolium). Ann Entomol Soc Am 95:345–351CrossRefGoogle Scholar
  29. Junker RR, Blüthgen N (2010) Floral scents repel facultative flower visitors, but attract obligate ones. Ann Bot 105:777–782PubMedCentralCrossRefPubMedGoogle Scholar
  30. Jürgens A (2004) Flowerscent composition in diurnal Silene species (Caryophyllaceae): phylogenetic constraints or adaption to flower visitors? Biochem Syst Ecol 32:841–859CrossRefGoogle Scholar
  31. Jürgens A, Witt T, Gottsberger G (1996) Reproduction and pollination in central European populations of Silene and Saponaria species. Bot Acta 109:316–324CrossRefGoogle Scholar
  32. Jürgens A, Witt T, Gottsberger G (2002a) Pollen grain numbers, ovule numbers and pollen-ovule ratios in Caryophylloideae: correlation with breeding system, pollination, life form, style number, and sexual system. Sex Plant Reprod 14:279–289CrossRefGoogle Scholar
  33. Jürgens A, Witt T, Gottsberger G (2002b) Flower scent composition in night-flowering Silene species (Caryophyllaceae). Biochem Syst Ecol 30:383–397CrossRefGoogle Scholar
  34. Jürgens A, Witt T, Gottsberger G (2003) Flower scent composition in Dianthus and Saponaria species (Caryophyllaceae) and its relevance for pollination biology and taxonomy. Biochem Syst Ecol 31:345–357CrossRefGoogle Scholar
  35. Jürgens A, Witt T, Gottsberger G (2012) Pollen grain size variation in Caryophylloideae: a mixed strategy for pollen deposition along styles with long stigmatic areas? Plant Syst Evol 298:9–24CrossRefGoogle Scholar
  36. Kephart S, Reynolds RJ, Rutter MT, Fenster CB, Dudash MR (2006) Pollination and seed predation by moths on Silene and allied Caryophyllaceae: evaluating a model system to study the evolution of mutualisms. New Phytol 169:667–680CrossRefPubMedGoogle Scholar
  37. Knudsen JT, Tollsten L (1993) Trends in floral scent chemistry in pollination syndromes: floral scent composition in moth taxa. Bot J Linn Soc 113:263–284Google Scholar
  38. Knudsen JT, Eriksson R, Gershenzon J (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120CrossRefGoogle Scholar
  39. Levin RA, McDade LA, Raguso RA (2003) The systematic utility of floral and vegetative fragrance in two genera of Nyctaginaceae. Syst Biol 52:334–351CrossRefPubMedGoogle Scholar
  40. Light DM, Flath RA, Buttery RG, Zalom FG, Rice RE, Dickens JC, Jang EB (1993) Host-plant green-leaf volatiles synergize the synthetic sex pheromones of the corn earworm and codling moth (Lepidoptera). Chemoecology 4:145–152CrossRefGoogle Scholar
  41. Lindman CAM (1897) Remarques sur la floraison du genre Silene L. Acta Horti Bergiana 3:3–28Google Scholar
  42. Martinell MC, Dötterl S, Blanché C, Rovira A, Massó S, Bosch M (2010) Nocturnal pollination of the endemic Silene sennenii (Caryophyllaceae): an endangered mutualism? Plant Ecol 211:203–218CrossRefGoogle Scholar
  43. Miyake T, Yamaoka R, Yahara T (1998) Floral scents of hawkmoth-pollinated flowers in Japan. J Plant Res 111:199–205CrossRefGoogle Scholar
  44. Motten AF, Campbell DR, Alexander DE, Miller HL (1981) Pollination effectiveness of specialist and generalist visitors to a North Carolina population of Claytonia virginica. Ecology 62:1278–1287CrossRefGoogle Scholar
  45. 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 103:1471–1480PubMedCentralCrossRefPubMedGoogle Scholar
  46. Oxelman B, Lidén M (1995) Generic boundaries in the tribe Sileneae (Caryophyllaceae) as inferred from nuclear rDNA sequences. Taxon 44:525–542CrossRefGoogle Scholar
  47. Oxelman B, Rautenberg A, Thollesson M, Larsson A, Frajman B, Eggens F, Petri A, Aydin Z, Töpel, M, Brandtberg-Falkman A (2013) Sileneae taxonomy and systematics.
  48. Pettersson MW (1991) Pollination by a guild of fluctuating moth populations: option for unspecialization in Silene vulgaris. J Ecol 79:591–604CrossRefGoogle Scholar
  49. Pichersky E, Raguso RA, Lewinsohn E, Croteau R (1994) Floral scent production in Clarkia (onagraceae). I. Localization and developmental modulation of monoterpene emission and linalool synthase activity. Plant Physiol 106:1533–1540PubMedCentralPubMedGoogle Scholar
  50. Plepys D, Ibarra F, Löfstedt C (2002) Volatiles from flowers of Platanthera bifolia (Orchidaceae) attractive to the silver Y moth, Autographa gamma (Lepidoptera: Noctuidae). Oikos 99:69–74CrossRefGoogle Scholar
  51. Raguso RA, Light DM (1998) Electroantennogram responses of male Sphinx perelegans hawkmoths to floral and ‘green-leaf volatiles’. Entomol Exp Appl 86:287–293CrossRefGoogle Scholar
  52. Raguso RA, Light DM, Pickersky E (1996) Electroantennogram responses of Hyles lineata (Sphingidae: Lepidoptera) to volatile compounds from Clarkia breweri (Onagraceae) and other moth-pollinated flowers. J Chem Ecol 22:1735–1766CrossRefPubMedGoogle Scholar
  53. Reynolds RJ, Westbrook MJ, Rohde AS, Cridland JM, Fenster CB, Dudash MR (2009) Pollinator specialization and pollination syndromes of three related north American Silene. Ecology 90:2077–2087CrossRefPubMedGoogle Scholar
  54. Reynolds RJ, Kula AA, Fenster CB, Dudash MR (2012) Variable nursery pollinator importance and its effect on plant reproductive success. Oecologia 168:439–448CrossRefPubMedGoogle Scholar
  55. Rosas-Guerrero V, Aguilar R, Martén-Rodríguez S, Ahsworth L, Lopezaraiza-Mikel M, Bastida JM, Quesada M (2014) A quantitative review of pollination syndrome: do floral traits predict effective pollinators? Ecol Lett 17:388–400CrossRefPubMedGoogle Scholar
  56. Schiestl FP (2010) The evolution of floral scent and insect chemical communication. Ecol Lett 13:643–656CrossRefPubMedGoogle Scholar
  57. Schlumpberger BO, Raguso RA (2008) Geographic variation in floral scent of Echinopsis ancistrophora (Cactaceae); evidence for constraints on hawkmoth attraction. Oikos 117:801–814CrossRefGoogle Scholar
  58. Thompson JN (1994) The coevolutionary process. University of Chicago PressGoogle Scholar
  59. Thompson JN (1999) Specific hypotheses on the geographic mosaic of coevolution. Am Nat 153:1–14CrossRefGoogle Scholar
  60. Visser JH, VAN Straten S, Maarse H (1979) Isolation and identification of volatiles in the foliage of potato, Solanum tuberosum, a host plant of the Colorado beetle, Leptinotarsa decemlineata. J Chem Ecol 5:13–25CrossRefGoogle Scholar
  61. Waelti MO, Muhlemann JK, Widmer A, Schiestl FP (2008) Floral odour and reproductive isolation in two species of Silene. J Evol Biol 21:111–121PubMedGoogle Scholar
  62. Waser NM, Price MV (1990) Pollination efficiency and effectiveness of bumble bees and hummingbirds visiting Delphinium nelsonii. Collect Bot 19:9–20CrossRefGoogle Scholar
  63. Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060CrossRefGoogle Scholar
  64. Witt T, Jürgens A, Gottsberger G (2013) Nectar sugar composition of European Caryophylloideae (Caryophyllaceae) in relation to flower length, pollination biology and phylogeny. J Evol Biol 26:2244–2259CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Samuel Prieto-Benítez
    • 1
    Email author
  • Stefan Dötterl
    • 2
  • Luis Giménez-Benavides
    • 1
  1. 1.Dep. Biología y Geología, Física y Química InorgánicaUniversidad Rey Juan Carlos-ESCETMóstolesSpain
  2. 2.Department of Ecology & Evolution, Plant EcologyUniversity of SalzburgHellbrunnerstrAustria

Personalised recommendations