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Multifunctional and Diverse Floral Scents Mediate Biotic Interactions Embedded in Communities

  • Robert R. JunkerEmail author
Part of the Signaling and Communication in Plants book series (SIGCOMM)

Abstract

Floral scent bouquets are both chemically and functionally highly diverse and are composed of volatile organic compounds (VOCs) that are attractive to pollinators, repellent to antagonistic animals and have the potential to regulate the establishment and growth of microorganisms. After briefly summarizing the biochemical basis for the diversity of floral scents, I will focus on their ecological significance in pair-wise interactions and communities. The multifunctionality of floral scent bouquets is based on the composition of VOCs that mediate one or more distinct biotic interactions. Additionally, the multifunctionality is also supported by the dynamics in emission rates of floral scents enabling flowers to synchronize with the activity patterns of pollinators in a diel rhythm and to quickly respond to biotic interactions. Finally, I will discuss how the chemical ecology of flowers can be integrated into a community ecological context where floral scents are treated as hyperdiverse functional traits involved in important ecosystem processes.

Keywords

Conditioned Stimulus Emission Rate Flower Visitor Floral Scent Floral Resource 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgement

I thank James Blande and Robert Glinwood for inviting me to contribute to this book. I also thank Nico Blüthgen and many colleagues for discussions that helped to shape the ideas presented here and Stefan Dötterl for providing me the opportunity to continue the research on floral scents in an inspiring atmosphere. Benoit Boachon, Stefan Dötterl, Annemarie Heiduk, Anja Hörger, Jonas Kuppler, Anne-Amélie C. Larue-Kontic and Irmgard Schäffler provided valuable comments on a previous version and/or contributed to the figures. My work on floral scents was supported by the Graduate School ‘Evolutionary Networks: Organisms, Reactions, Molecules’ (E-Norm) of the Heinrich-Heine-University, Düsseldorf, the Glockner-Öko-Fonds and the Deutsche Forschungsgemeinschaft (DFG JU 2856/1-1 and JU 2856/2-2).

References

  1. Ackerman JD (1986) Coping with the epiphytic existence: pollination strategies. Selbyana 9:52–60Google Scholar
  2. Alvarez-Perez S, Herrera CM, de Vega C (2012) Zooming-in on floral nectar: a first exploration of nectar-associated bacteria in wild plant communities. FEMS Microbiol Ecol 80:591–602PubMedCrossRefGoogle Scholar
  3. Andersson S, Nilsson LA, Groth I, Bergström G (2002) Floral scents in butterfly-pollinated plants: possible convergence in chemical composition. Bot J Linn Soc 140:129–153CrossRefGoogle Scholar
  4. Andrews ES, Theis N, Adler LS (2007) Pollinator and herbivore attraction to Cucurbita floral volatiles. J Chem Ecol 33:1682–1691PubMedCrossRefGoogle Scholar
  5. Ashman TL, Bradburn M, Cole DH, Blaney BH, Raguso RA (2005) The scent of a male: the role of floral volatiles in pollination of a gender dimorphic plant. Ecology 86:2099–2105CrossRefGoogle Scholar
  6. Bak S, Beisson F, Bishop G, Hamberger B, Höfer R, Paquette S, Werck-Reichhart D (2011) Cytochromes P450. The Arabidopsis Book 9:e0144Google Scholar
  7. Bertoli A, Menichini F, Mazzetti M, Spinelli G, Morelli I (2003) Volatile constituents of the leaves and flowers of Hypericum triquetrifolium Turra. Flavour Fragance J 18:91–94CrossRefGoogle Scholar
  8. Biesmeijer JC, Roberts SPM, Reemer M, Ohlemuller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD, Settele J, Kunin WE (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354PubMedCrossRefGoogle Scholar
  9. Blüthgen N, Menzel F, Hovestadt T, Fiala B, Blüthgen N (2007) Specialization, constraints, and conflicting interests in mutualistic networks. Curr Biol 17:341–346PubMedCrossRefGoogle Scholar
  10. Boachon B, Junker RR, Miesch L, Bassard J-E, Höfer R, Cailleaudeaux R, Seidel DE, Lesot A, Heinrich C, Ginglinger J-F, Allouche L, Vincent B, Wahyuni DSC, Paetz C, Beran F, Miesch M, Schneider B, Leiss K, Werck-Reichhart D (2015) CYP76C1 (Cytochrome P450)-mediated linalool metabolism and the formation of volatile and soluble linalool oxides in Arabidopsis flowers: a strategy for defense against floral antagonists. Plant Cell 27:2972–2990PubMedPubMedCentralGoogle Scholar
  11. Bodenhausen N, Bortfeld-Miller M, Ackermann M, Vorholt JA (2014) A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. PLoS Genet 10(4):e1004283PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bruinsma M, Lucas-Barbosa D, ten Broeke CJM, van Dam NM, van Beek TA, Dicke M, van Loon JJA (2014) Folivory affects composition of nectar, floral odor and modifies pollinator behavior. J Chem Ecol 40:39–49PubMedCrossRefGoogle Scholar
  13. Buban T, Orosz-Kovacs Z, Farkas A (2003) The nectary as the primary site of infection by Erwinia amylovora (Burr.). Plant Syst Evol 238:183–194CrossRefGoogle Scholar
  14. Burdon RCF, Raguso RA, Kessler A, Parachnowitsch AL (2015) Spatiotemporal floral scent variation of Penstemon digitalis. J Chem Ecol 41:641–650PubMedCrossRefGoogle Scholar
  15. Burger H, Dotterl S, Haberlein CM, Schulz S, Ayasse M (2012) An arthropod deterrent attracts specialised bees to their host plants. Oecologia 168:727–736PubMedCrossRefGoogle Scholar
  16. Cadotte M, Albert CH, Walker SC (2013) The ecology of differences: assessing community assembly with trait and evolutionary distances. Ecol Lett 16:1234–1244PubMedCrossRefGoogle Scholar
  17. Campbell AJ, Biesmeijer JC, Varma V, Wackers FL (2012) Realising multiple ecosystem services based on the response of three beneficial insect groups to floral traits and trait diversity. Basic Appl Ecol 13:363–370CrossRefGoogle Scholar
  18. Carlsson M, Hansson B (2006) Detection and coding of flower volatiles in nectar-foraging insects. In: Dudareva N, Pichersky E (eds) Biology of floral scent. CRC Press, Boca Raton, FL, pp 147–198Google Scholar
  19. Carvalheiro L, Biesmeijer J, Benadi G, Fruend J, Stang M, Bartomeus I, Kaiser-Bunbury C, Baude M, Gomes S, Merckx V, Baldock K, Bennett A, Boada R, Bommarco R, Cartar R, Chacoff N, Danhardt J, Dicks L, Ekroos J, Henson K, Holzschuh A, Junker RR, Lopezaraiza-Mikel M, Memmott J, Montero-Castaño A, Nelson I, Petanidou T, Power E, Rundlöf M, Smith H, Stout J, Temitope K, Tscharntke T, Tscheulin T, Vila M, Kunin W (2014) The potential for indirect effects between co-flowering plants via shared pollinators depends on resource abundance, accessibility and relatedness. Ecol Lett 17:1389–1399PubMedCrossRefGoogle Scholar
  20. Chen C, Song QS, Proffit M, Bessiere JM, Li ZB, Hossaert-McKey M (2009) Private channel: a single unusual compound assures specific pollinator attraction in Ficus semicordata. Funct Ecol 23:941–950CrossRefGoogle Scholar
  21. Chittka L, Thomson JD (2001) Cognitive ecology of pollination: animal behaviour and floral evolution. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  22. Courtois EA, Paine CET, Blandinieres PA, Stien D, Bessiere JM, Houel E, Baraloto C, Chave J (2009) Diversity of the volatile organic compounds emitted by 55 species of tropical trees: a survey in French Guiana. J Chem Ecol 35:1349–1362PubMedCrossRefGoogle Scholar
  23. Daly KC, Carrell LA, Mwilaria E (2007) Detection versus perception: physiological and behavioral analysis of olfactory sensitivity in the moth (Manduca sexta). Behav Neurosci 121:794–807PubMedCrossRefGoogle Scholar
  24. Darwin C (1862) On the various contrivances by which British and foreign orchids are fertilised by insects. John Murray, LondonGoogle Scholar
  25. Degenhardt J, Köllner TG, Gershenzon J (2009) Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 70:1621–1637PubMedCrossRefGoogle Scholar
  26. Del Giudice L, Massardo DR, Pontieri P, Bertea CM, Mombello D, Carata E, Tredici SM, Tala A, Mucciarelli M, Groudeva VI, De Stefano M, Vigliotta G, Maffei ME, Alifano P (2008) The microbial community of Vetiver root and its involvement into essential oil biogenesis. Environ Microbiol 10:2824–2841PubMedCrossRefGoogle Scholar
  27. Devictor V, Mouillot D, Meynard C, Jiguet F, Thuiller W, Mouquet N (2010) Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: the need for integrative conservation strategies in a changing world. Ecol Lett 13:1030–1040PubMedGoogle Scholar
  28. Dobson HEM (2006) Relationship between floral fragrance composition and type of pollinator. In: Dudareva N, Pichersky E (eds) Biology of floral scent. CRC Press, Boca Raton, FL, pp 147–198CrossRefGoogle Scholar
  29. Dötterl S, Vereecken NJ (2010) The chemical ecology and evolution of bee–flower interactions: a review and perspectives. Can J Zool 88:668–697CrossRefGoogle Scholar
  30. Dötterl S, Wolfe LM, Jürgens A (2005) Qualitative and quantitative analyses of flower scent in Silene latifolia. Phytochemistry 66:203–213PubMedCrossRefGoogle Scholar
  31. 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 169:707–718PubMedCrossRefGoogle Scholar
  32. Dötterl S, David A, Boland W, Silberbauer-Gottsberger I, Gottsberger G (2012a) Evidence for behavioral attractiveness of methoxylated aromatics in a Dynastid Scarab beetle-pollinated Araceae. J Chem Ecol 38:1539–1543PubMedCrossRefGoogle Scholar
  33. Dötterl S, Jahreiss K, Jhumur US, Jürgens A (2012b) Temporal variation of flower scent in Silene otites (Caryophyllaceae): a species with a mixed pollination system. Bot J Linn Soc 169:447–460CrossRefGoogle Scholar
  34. Dudareva N, Pichersky E (2000) Biochemical and molecular genetic aspects of floral scents. Plant Phys 122:627–633CrossRefGoogle Scholar
  35. Dudareva N, Pichersky E (2006a) Biology of floral scent. CRC Press, Boca Raton, FLGoogle Scholar
  36. Dudareva N, Pichersky E (2006b) Floral scent metabolic pathways: their regulation and evolution. In: Dudareva N, Pichersky E (eds) Biology of floral scent. CRC Press, Boca Raton, FL, pp 55–78Google Scholar
  37. Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198:16–32PubMedCrossRefGoogle Scholar
  38. Dukas R, Morse DH (2003) Crab spiders affect flower visitation by bees. Oikos 101:157–163CrossRefGoogle Scholar
  39. Dupuy F, Sandoz JC, Giurfa M, Josens R (2006) Individual olfactory learning in Camponotus ants. Anim Behav 72:1081–1091CrossRefGoogle Scholar
  40. Effmert U, Buss D, Rohrbeck D, Piechulla B (2006) Localization of the synthesis and emission of scent compounds within the flowers. In: Dudareva N, Pichersky E (eds) Biology of floral scent. CRC Press, Boca Raton, FL, pp 105–124Google Scholar
  41. Faegri K, Pijl L (1979) The principles of pollination ecology, 3rd edn. Pergamon Press, Toronto, ONGoogle Scholar
  42. Farré-Armengol G, Filella I, Llusia J, Penuelas J (2013) Floral volatile organic compounds: between attraction and deterrence of visitors under global change. Perspect Plant Ecol 15:56–67CrossRefGoogle Scholar
  43. Farré-Armengol G, Filella I, Llusia J, Niinemets Ü, Penuelas J (2014) Changes in floral bouquets from compound-specific responses to increasing temperatures. Glob Chang Biol 20:3660–3669PubMedCrossRefGoogle Scholar
  44. Filella I, Primante C, Llusia J, Gonzalez AMM, Seco R, Farré-Armengol G, Rodrigo A, Bosch J, Penuelas J (2013) Floral advertisement scent in a changing plant–pollinators market. Sci Rep 3:3434PubMedPubMedCentralCrossRefGoogle Scholar
  45. Fontaine C, Dajoz I, Meriguet J, Loreau M (2006) Functional diversity of plant–pollinator interaction webs enhances the persistence of plant communities. PLoS Biol 4:129–135CrossRefGoogle Scholar
  46. Friberg M, Schwind C, Roark LC, Raguso RA, Thompson JN (2014) Floral scent contributes to interaction specificity in coevolving plants and their insect pollinators. J Chem Ecol 40:955–965PubMedCrossRefGoogle Scholar
  47. Fridman S, Izhaki I, Gerchman Y, Halpern M (2012) Bacterial communities in floral nectar. Environ Microbiol Rep 4:97–104PubMedCrossRefGoogle Scholar
  48. Fründ J, Dormann CF, Tscharntke T (2011) Linne’s floral clock is slow without pollinators—flower closure and plant–pollinator interaction webs. Ecol Lett 14:896–904PubMedCrossRefGoogle Scholar
  49. Fründ J, Dormann CF, Holzschuh A, Tscharntke T (2013) Bee diversity effects on pollination depend on functional complementarity and niche shifts. Ecology 94:2042–2054PubMedCrossRefGoogle Scholar
  50. Fuernkranz M, Lukesch B, Müller H, Huss H, Grube M, Berg G (2012) Microbial diversity inside pumpkins: microhabitat-specific communities display a high antagonistic potential against phytopathogens. Microb Ecol 63:418–428CrossRefGoogle Scholar
  51. Funk JL, Cleland EE, Suding KN, Zavaleta ES (2008) Restoration through reassembly: plant traits and invasion resistance. Trends Ecol Evol 23:695–703PubMedCrossRefGoogle Scholar
  52. Galbally IE, Kirstine W (2002) The production of methanol by flowering plants and the global cycle of methanol. J Atmos Chem 43:195–229CrossRefGoogle Scholar
  53. Galen C (1999) Flowers and enemies: predation by nectar-thieving ants in relation to variation in floral form of an alpine wildflower, Polemonium viscosum. Oikos 85:426–434CrossRefGoogle Scholar
  54. Galen C, Kaczorowski R, Todd SL, Geib J, Raguso RA (2011) Dosage-dependent impacts of a floral volatile compound on pollinators, larcenists, and the potential for floral evolution in the Alpine Skypilot Polemonium viscosum. Am Nat 177:258–272PubMedCrossRefGoogle Scholar
  55. Gallai N, Salles JM, Settele J, Vaissiere BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68:810–821CrossRefGoogle Scholar
  56. Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3:408–414PubMedCrossRefGoogle Scholar
  57. Gomez JM, Perfectti F, Abdelaziz M, Lorite J, Munoz-Pajares AJ, Valverde J (2015) Evolution of pollination niches in a generalist plant clade. New Phytol 205:440–453PubMedCrossRefGoogle Scholar
  58. Graham L, Jones KN (1996) Resource partitioning and per-flower foraging efficiency in two bumble bee species. Am Midl Nat 136:401–406CrossRefGoogle Scholar
  59. Guenther A (1999) Modeling biogenic volatile organic compound emissions to the athmosphere. In: Hewitt CN (ed) Reactive hydrocarbons in the atmosphere. Academic Press, San Diego, CAGoogle Scholar
  60. Guenther A, Hewitt CN, Erickson D, Fall R, Geron C, Graedel T, Harley P, Klinger L, Lerdau M, Mckay WA, Pierce T, Scholes B, Steinbrecher R, Tallamraju R, Taylor J, Zimmerman P (1995) A global-model of natural volatile organic-compound emissions. J Geophys Res Atmos 100:8873–8892CrossRefGoogle Scholar
  61. Guerrieri F, Schubert M, Sandoz J-C, Giurfa M (2005) Perceptual and neural olfactory similarity in honeybees. PLoS Biol 3(4):e60PubMedPubMedCentralCrossRefGoogle Scholar
  62. Hargreaves AL, Harder LD, Johnson SD (2009) Consumptive emasculation: the ecological and evolutionary consequences of pollen theft. Biol Rev 84:259–276PubMedCrossRefGoogle Scholar
  63. Heiduk A, Brake I, Tolasch T, Frank J, Jurgens A, Meve U, Dotterl S (2010) Scent chemistry and pollinator attraction in the deceptive trap flowers of Ceropegia dolichophylla. South Afr J Bot 76:762–769CrossRefGoogle Scholar
  64. Heiduk A, Kong H, Brake I, von Tschirnhaus M, Till T, Tröger AG, Wittenberg E, Francke W, Meve U, Dötterl S (2015) Deceptive Ceropegia dolichophylla fools its kleptoparasitic fly pollinators with exceptional floral scent. Front Ecol Evol 3:66CrossRefGoogle Scholar
  65. Herrera CM, Garcia IM, Perez R (2008) Invisible floral larcenies: microbial communities degrade floral nectar of bumble bee-pollinated plants. Ecology 89:2369–2376PubMedCrossRefGoogle Scholar
  66. Herrera CM, Pozo MI, Medrano M (2013) Yeasts in nectar of an early-blooming herb: sought by bumble bees, detrimental to plant fecundity. Ecology 94:273–279PubMedCrossRefGoogle Scholar
  67. Huang M, Sanchez-Moreiras AM, Abel C, Sohrabi R, Lee S, Gershenzon J, Tholl D (2012) The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-b-caryophyllene, is a defense against a bacterial pathogen. New Phytol 193:997–1008PubMedCrossRefGoogle Scholar
  68. Hull CD, Cunningham JP, Moore CJ, Zalucki MP, Cribb BW (2004) Discrepancy between antennal and behavioral responses for enantiomers of alpha-pinene: electrophysiology and behavior of Helicoverpa armigera (Lepidoptera). J Chem Ecol 30:2071–2084PubMedCrossRefGoogle Scholar
  69. Ings TC, Montoya JM, Bascompte J, Blüthgen N, Brown L, Dormann CF, Edwards F, Figueroa D, Jacob U, Jones JI, Lauridsen RB, Ledger ME, Lewis HM, Olesen JM, Veen FJF, Warren PH, Woodward G (2009) Ecological networks—beyond food webs. J Anim Ecol 78:253–269PubMedCrossRefGoogle Scholar
  70. Inouye DW (1980) The terminology of floral larceny. Ecology 61:1251–1253CrossRefGoogle Scholar
  71. Jhumur US, Dötterl S, Jürgens A (2008) Floral odors of Silene otites: their variability and attractiveness to mosquitoes. J Chem Ecol 34:14–25PubMedCrossRefGoogle Scholar
  72. Johnson RA (1986) Intraspecific resource partitioning in the bumble bees Bombus ternarius and Bombus pennsylvanicus. Ecology 67:133–138CrossRefGoogle Scholar
  73. Junker RR (2010) Scents as floral defence: impact on species and communities, mechanisms and ecological consequences. University Würzburg, WürzburgGoogle Scholar
  74. Junker RR, Blüthgen N (2008) Floral scents repel potentially nectar-thieving ants. Evol Ecol Res 10:295–308Google Scholar
  75. Junker RR, Blüthgen N (2010) Floral scents repel facultative flower visitors, but attract obligate ones. Ann Bot 105:777–782PubMedPubMedCentralCrossRefGoogle Scholar
  76. Junker RR, Keller A (2015) Microhabitat heterogeneity across leaves and flower organs promotes bacterial diversity. FEMS Microbiol Ecol 91:fiv097PubMedCrossRefGoogle Scholar
  77. Junker RR, Parachnowitsch AL (2015) Working towards a holistic view on flower traits—how floral scents mediate plant–animal interactions in concert with other floral characters. J Indian Inst Sci 95:44–67Google Scholar
  78. Junker RR, Tholl D (2013) Volatile organic compound mediated interactions at the plant–microbe interface. J Chem Ecol 39:810–825PubMedCrossRefGoogle Scholar
  79. Junker RR, Heidinger IMM, Blüthgen N (2010a) Floral scent terpenoids deter the facultative florivore Metrioptera bicolor (Ensifera, Tettigoniidae, Decticinae). J Orthop Res 19:69–74CrossRefGoogle Scholar
  80. Junker RR, Höcherl N, Blüthgen N (2010b) Responses to olfactory signals reflect network structure of flower–visitor interactions. J Anim Ecol 79:818–823PubMedGoogle Scholar
  81. Junker RR, Bretscher S, Dötterl S, Blüthgen N (2011a) Phytochemical cues affect hunting site choices of a nursery web spider (Pisaura mirabilis) but not of a crab spider (Misumena vatia). J Arachnol 39:113–117CrossRefGoogle Scholar
  82. Junker RR, Daehler CC, Dötterl S, Keller A, Blüthgen N (2011b) Hawaiian ant-flower networks: nectar-thieving ants prefer undefended native over introduced plants with floral defenses. Ecol Monogr 81:295–311CrossRefGoogle Scholar
  83. Junker RR, Gershenzon J, Unsicker SB (2011c) Floral odour bouquet loses its ant repellent properties after inhibition of terpene biosynthesis. J Chem Ecol 37:1323–1331PubMedCrossRefGoogle Scholar
  84. Junker RR, Loewel C, Gross R, Dötterl S, Keller A, Blüthgen N (2011d) Composition of epiphytic bacterial communities differs on petals and leaves. Plant Biol 13:918–924PubMedCrossRefGoogle Scholar
  85. Junker RR, Blüthgen N, Brehm T, Binkenstein J, Paulus J, Schaefer HM, Stang M (2013) Specialization on traits as basis for the niche-breadth of flower visitors and as structuring mechanism of ecological networks. Funct Ecol 27:329–341CrossRefGoogle Scholar
  86. Junker RR, Romeike T, Keller A, Langen D (2014) Density-dependent negative responses by bumblebees to bacteria isolated from flowers. Apidologie 45:467–477CrossRefGoogle Scholar
  87. Junker RR, Blüthgen N, Keller A (2015) Functional and phylogenetic diversity of communities differently affect the structure of flower–visitor interactions and reveal convergences in floral traits. Evol Ecol 29:437–450CrossRefGoogle Scholar
  88. Jürgens A, Webber AC, Gottsberger G (2000) Floral scent compounds of Amazonian Annonaceae species pollinated by small beetles and thrips. Phytochemistry 55:551–558PubMedCrossRefGoogle Scholar
  89. Jürgens A, Glück U, Aas G, Dötterl S (2014) Diel fragrance pattern correlates with olfactory preferences of diurnal and nocturnal flower visitors in Salix caprea (Salicaceae). Bot J Linn Soc 175:624–640CrossRefGoogle Scholar
  90. Kaiser-Bunbury CN, Vázquez DP, Stang M, Ghazoul J (2014) Determinants of the microstructure of plant–pollinator networks. Ecology 95:3314–3324CrossRefGoogle Scholar
  91. Katzenberger TD, Lunau K, Junker RR (2013) Salience of multimodal flower cues manipulates initial responses and facilitates learning performance of bumblebees. Behav Ecol Sociobiol 67:1587–1599CrossRefGoogle Scholar
  92. Kerner A (1879) Die Schutzmittel der Blüthen gegen unberufene Gäste. Verlag der Wagner’schen Universitäts-Buchhandlung, InnsbruckGoogle Scholar
  93. Kessler D, Baldwin IT (2007) Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. Plant J 49:840–854PubMedCrossRefGoogle Scholar
  94. Kessler A, Halitschke R (2009) Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study. Funct Ecol 23:901–912CrossRefGoogle Scholar
  95. Kessler D, Gase K, Baldwin IT (2008) Field experiments with transformed plants reveal the sense of floral scents. Science 321:1200–1202PubMedCrossRefGoogle Scholar
  96. Kessler A, Halitschke R, Poveda K (2011) Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant–pollinator interactions. Ecology 92:1769–1780PubMedCrossRefGoogle Scholar
  97. Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc Biol Sci 274:303–313PubMedCrossRefGoogle Scholar
  98. Knudsen JT (2002) Variation in floral scent composition within and between populations of Geonoma macrostachys (Arecaceae) in the western Amazon. Am J Bot 89:1772–1778PubMedCrossRefGoogle Scholar
  99. Knudsen JT, Gershenzon J (2006) The chemical diversity of floral scent. In: Dudareva N, Pichersky E (eds) Biology of floral scent. CRC Press, Boca Raton, FLGoogle Scholar
  100. Knudsen JT, Tollsten L (1993) Trends in floral scent chemistry in pollination syndromes—floral scent composition in moth-pollinated taxa. Bot J Linn Soc 113:263–284CrossRefGoogle Scholar
  101. Knudsen JT, Tollsten L (1995) Floral scent in bat-pollinated plants—a case of convergent evolution. Bot J Linn Soc 119:45–57CrossRefGoogle Scholar
  102. Knudsen JT, Tollsten L, Groth I, Bergström G, Raguso RA (2004) Trends in floral scent chemistry in pollination syndromes: floral scent composition in hummingbird–pollinated taxa. Bot J Linn Soc 146:191–199CrossRefGoogle Scholar
  103. Knudsen JT, Eriksson R, Gershenzon J, Stahl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120CrossRefGoogle Scholar
  104. Kraft NJB, Godoy O, Levine JM (2015) Plant functional traits and the multidimensional nature of species coexistence. Proc Natl Acad Sci USA 112:797–802PubMedPubMedCentralCrossRefGoogle Scholar
  105. Laloi D, Bailez O, Blight MM, Roger B, Pham-Delegue M-H, Wadhams LJ (2000) Recognition of complex odors by restrained and free-flying honeybees, Apis mellifera. J Chem Ecol 26:2307–2319CrossRefGoogle Scholar
  106. Larue AAC, Raguso RA, Junker RR (2016) Experimental manipulation of floral scent bouquets restructures flower–visitor networks in the field. J Anim Ecol 85:396-408 Google Scholar
  107. Lee S, Badieyan S, Bevan DR, Herde M, Gatz C, Tholl D (2010) Herbivore-induced and floral homoterpene volatiles are biosynthesized by a single P450 enzyme (CYP82G1) in Arabidopsis. Proc Natl Acad Sci USA 107:21205–21210PubMedPubMedCentralCrossRefGoogle Scholar
  108. Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883PubMedPubMedCentralCrossRefGoogle Scholar
  109. Liu JJ, Zhang XX, Song FF, Zhou SR, Cadotte MW, Bradshaw CJA (2015) Explaining maximum variation in productivity requires phylogenetic diversity and single functional traits. Ecology 96:176–183PubMedCrossRefGoogle Scholar
  110. Lucas-Barbosa D, van Loon JJA, Dicke M (2011) The effects of herbivore-induced plant volatiles on interactions between plants and flower-visiting insects. Phytochemistry 72:1647–1654PubMedCrossRefGoogle Scholar
  111. Lucas-Barbosa D, Sunab P, Hakman A, van Beek TA, van Loon JJA, Dicke M (2015) Visual and odours cues: plant responses to pollination and herbivory affect the behaviour of flower visitors. Funct Ecol 30:431–441Google Scholar
  112. Magnard J-L, Roccia A, Caissard J-C, Vergne P, Sun P, Hecquet R, Dubois A, Hibrand-Saint Oyant L, Jullien F, Nicolè F, Raymond O, Huguet S, Baltenweck R, Meyer S, Claudel P, Jeauffre J, Rohmer M, Foucher F, Hugueney P, Bendahmane M, Baudino S (2015) Biosynthesis of monoterpene scent compounds in roses. Science 349:81–83PubMedCrossRefGoogle Scholar
  113. Mason NWH, de Bello F (2013) Functional diversity: a tool for answering challenging ecological questions. J Veg Sci 24:777–780CrossRefGoogle Scholar
  114. McCall AC, Irwin RE (2006) Florivory: the intersection of pollination and herbivory. Ecol Lett 9:1351–1365PubMedCrossRefGoogle Scholar
  115. McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185PubMedCrossRefGoogle Scholar
  116. Mouchet MA, Villeger S, Mason NWH, Mouillot D (2010) Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Funct Ecol 24:867–876CrossRefGoogle Scholar
  117. Muhlemann JK, Waelti MO, Widmer A, Schiestl FP (2006) Postpollination changes in floral odor in Silene latifolia: adaptive mechanisms for seed-predator avoidance? J Chem Ecol 32:1855–1860PubMedCrossRefGoogle Scholar
  118. Muhlemann JK, Klempien A, Dudareva N (2014) Floral volatiles: from biosynthesis to function. Plant Cell Environ 37:1936–1949PubMedCrossRefGoogle Scholar
  119. Negre F, Kish CM, Boatright J, Underwood B, Shibuya K, Wagner C, Clark DG, Dudareva N (2003) Regulation of methylbenzoate emission after pollination in snapdragon and petunia flowers. Plant Cell 15:2992–3006PubMedPubMedCentralCrossRefGoogle Scholar
  120. Oelschlägel B, Nuss M, von Tschirnhaus M, Patzold C, Neinhuis C, Dötterl S, Wanke S (2015) The betrayed thief—the extraordinary strategy of Aristolochia rotunda to deceive its pollinators. New Phytol 206:342–351PubMedCrossRefGoogle Scholar
  121. Ollerton J, Alarcon 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 103:1471–1480PubMedPubMedCentralCrossRefGoogle Scholar
  122. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326CrossRefGoogle Scholar
  123. Omura H, Honda K, Hayashi N (2000) Floral scent of Osmanthus fragrans discourages foraging behavior of cabbage butterfly, Pieris rapae. J Chem Ecol 26:655–666CrossRefGoogle Scholar
  124. Owen SM, Boissard C, Hewitt CN (2001) Volatile organic compounds (VOCs) emitted from 40 Mediterranean plant species: VOC speciation and extrapolation to habitat scale. Atmos Environ 35:5393–5409CrossRefGoogle Scholar
  125. Pierik R, Ballare CL, Dicke M (2014) Ecology of plant volatiles: taking a plant community perspective. Plant Cell Environ 37:1845–1853PubMedCrossRefGoogle Scholar
  126. Pozo MI, Lachance MA, Herrera CM (2012) Nectar yeasts of two southern Spanish plants: the roles of immigration and physiological traits in community assembly. FEMS Microbiol Ecol 80:281–293PubMedCrossRefGoogle Scholar
  127. Raguso RA (2008a) Start making scents: the challenge of integrating chemistry into pollination ecology. Entomol Exp Appl 128:196–207CrossRefGoogle Scholar
  128. Raguso RA (2008b) Wake up and smell the roses: the ecology and evolution of floral scent. Annu Rev Ecol Evol Syst 39:549–569CrossRefGoogle Scholar
  129. Raguso RA (2012) New synthesis: exploring the chemical links in ecological food webs. J Chem Ecol 38:441–441PubMedCrossRefGoogle Scholar
  130. Randlkofer B, Obermaier E, Hilker M, Meiners T (2010) Vegetation complexity—the influence of plant species diversity and plant structures on plant chemical complexity and arthropods. Basic Appl Ecol 11:383–395CrossRefGoogle Scholar
  131. Reinhard J, Sinclair M, Srinivasan MV, Claudianos C (2010) Honeybees learn odour mixtures via a selection of key odorants. PLoS One 5:e9110PubMedPubMedCentralCrossRefGoogle Scholar
  132. Riffell JA, Lei H, Christensen TA, Hildebrand JG (2009) Characterization and coding of behaviorally significant odor mixtures. Curr Biol 19:335–340PubMedPubMedCentralCrossRefGoogle Scholar
  133. Riffell JA, Shlizerman E, Sanders E, Abrell L, Medina B, Hinterwirth AJ, Kutz JN (2014) Flower discrimination by pollinators in a dynamic chemical environment. Science 344:1515–1518PubMedCrossRefGoogle Scholar
  134. Schaefer HM, Ruxton GD (2011) Plant–animal communication. Oxford University Press, OxfordCrossRefGoogle Scholar
  135. Schäffler I, Balao F, Dotterl S (2012) Floral and vegetative cues in oil-secreting and non-oil-secreting Lysimachia species. Ann Bot 110:125–138PubMedPubMedCentralCrossRefGoogle Scholar
  136. Schäffler I, Steiner KE, Haid M, van Berkel SS, Gerlach G, Johnson SD, Wessjohann L, Dötterl S (2015) Diacetin, a reliable cue and private communication channel in a specialized pollination system. Sci Rep 5:12779PubMedPubMedCentralCrossRefGoogle Scholar
  137. Schie CCN, Haring MA, Schuurink RC (2006) Regulation of terpenoid and benzenoid production in flowers. Curr Opin Plant Biol 9:203–208PubMedCrossRefGoogle Scholar
  138. Schiestl FP, Ayasse M (2001) Post-pollination emission of a repellent compound in a sexually deceptive orchid: a new mechanism for maximising reproductive success? Oecologia 126:531–534CrossRefGoogle Scholar
  139. Schiestl FP, Dötterl S (2012) The evolution of floral scent and olfactory preferences in pollinators: coevolution or pre-existing bias? Evolution 66:2042–2055PubMedCrossRefGoogle Scholar
  140. Schiestl FP, Johnson SD (2013) Pollinator-mediated evolution of floral signals. Trends Ecol Evol 28:307–315PubMedCrossRefGoogle Scholar
  141. Schiestl FP, Ayasse M, Paulus HF, Erdmann D, Francke W (1997) Variation of floral scent emission and postpollination changes in individual flowers of Ophrys sphegodes subsp. sphegodes. J Chem Ecol 23:2881–2895CrossRefGoogle Scholar
  142. Schiestl FP, Kirk H, Bigler L, Cozzolino S, Desurmont GA (2014) Herbivory and floral signaling: phenotypic plasticity and tradeoffs between reproduction and indirect defense. New Phytol 203:257–266PubMedCrossRefGoogle Scholar
  143. Smith BH, Cobey S (1994) The olfactory memory of the honeybee Apis mellifera—blocking between odorants in binary-mixtures. J Exp Biol 195:91–108PubMedGoogle Scholar
  144. Smith BH, Wright GA, Daly KC (2006) Learning-based recognition and discrimination of floral odors. In: Dudareva N, Pichersky E (eds) Biology of floral scent. CRC Press, Boca Raton, FLGoogle Scholar
  145. Soler C, Hossaert-McKey M, Buatois B, Bessiere JM, Schatz B, Proffit M (2011) Geographic variation of floral scent in a highly specialized pollination mutualism. Phytochemistry 72:74–81PubMedCrossRefGoogle Scholar
  146. Spasojevic MJ, Suding KN (2012) Inferring community assembly mechanisms from functional diversity patterns: the importance of multiple assembly processes. J Ecol 100:652–661CrossRefGoogle Scholar
  147. Sprengel CK (1793) Das entdeckte Geheimnis der Natur im Bau und in der Befruchtung der Blumen, 1893rd edn. Mayer & Müller, Berlin, Facsimile-DruckCrossRefGoogle Scholar
  148. Stäger R (1931) Über die Einwirkung von Duftstoffen und Pflanzenduften auf Ameisen. Z Wiss Insektenbiol 26:55–65Google Scholar
  149. Stang M, Klinkhamer PGL, Meijden E (2007) Asymmetric specialization and extinction risk in plant–flower visitor webs: a matter of morphology or abundance? Oecologia 151:442–453PubMedCrossRefGoogle Scholar
  150. Svensson GP, Okamoto T, Kawakita A, Goto R, Kato M (2010) Chemical ecology of obligate pollination mutualisms: testing the ‘private channel’ hypothesis in the Breynia–Epicephala association. New Phytol 186:995–1004PubMedCrossRefGoogle Scholar
  151. Theis N (2006) Fragrance of Canada Thistle (Cirsium arvense) attracts both floral herbivores and pollinators. J Chem Ecol 32:917–927PubMedCrossRefGoogle Scholar
  152. Theis N, Kesler K, Adler LS (2009) Leaf herbivory increases floral fragrance in male but not female Cucurbita pepo subsp. texana (Cucurbitaceae) flowers. Am J Bot 96:897–903PubMedCrossRefGoogle Scholar
  153. Turnbull LA, Levine JM, Loreau M, Hector A (2013) Coexistence, niches and biodiversity effects on ecosystem functioning. Ecol Lett 16:116–127PubMedCrossRefGoogle Scholar
  154. Vannette RL, Gauthier M-PL, Fukami T (2012) Nectar bacteria, but not yeast, weaken a plant–pollinator mutualism. Proc R Soc B 280:20122601PubMedCrossRefGoogle Scholar
  155. von Frisch K (1967) The dancing language and orientation of bees. Havard University Press, Cambridge, MAGoogle Scholar
  156. 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
  157. Wardhaugh CW, Stork NE, Edwards W, Grimbacher PS (2012) The overlooked biodiversity of flower-visiting invertebrates. Plos One 7:e45796PubMedPubMedCentralCrossRefGoogle Scholar
  158. Waser NM, Ollerton J (2006) Plant–pollinator interactions: from specialization to generalization. University of Chicago Press, ChicagoGoogle Scholar
  159. Whitham TG, Bailey JK, Schweitzer JA, Shuster SM, Bangert RK, Leroy CJ, Lonsdorf EV, Allan GJ, DiFazio SP, Potts BM, Fischer DG, Gehring CA, Lindroth RL, Marks JC, Hart SC, Wimp GM, Wooley SC (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7:510–523PubMedCrossRefGoogle Scholar
  160. Widhalm JR, Jaini R, Morgan JA, Dudareva N (2015) Rethinking how volatiles are released from plant cells. Trends Plant Sci. doi: 10.1016/j.tplants.2015.06.009 PubMedGoogle Scholar
  161. Willmer PG, Nuttman CV, Raine NE, Stone GN, Pattrick JG, Henson K, Stillman P, McIlroy L, Potts SG, Knudsen JT (2009) Floral volatiles controlling ant behaviour. Funct Ecol 23:888–900CrossRefGoogle Scholar
  162. Wright GA, Schiestl FP (2009) The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Funct Ecol 23:841–851CrossRefGoogle Scholar
  163. Wright GA, Smith BH (2004) Variation in complex olfactory stimuli and its influence on odour recognition. Proc R Soc Lond B 271:147–152CrossRefGoogle Scholar
  164. Zangerl AR, Berenbaum MR (2009) Effects of florivory on floral volatile emissions and pollination success in the wild parsnip. Arthropod Plant Interact 3:181–191CrossRefGoogle Scholar

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© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Ecology and EvolutionUniversity of SalzburgSalzburgAustria

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