Advertisement

Plant Systematics and Evolution

, Volume 305, Issue 9, pp 727–741 | Cite as

Interspecific variation of inflorescence scents and insect visitors in Allium (Amaryllidaceae: Allioideae)

  • Pietro ZitoEmail author
  • Francesca Tavella
  • Davide Pacifico
  • Viviana Campanella
  • Maurizio Sajeva
  • Francesco Carimi
  • Andreas W. Ebmer
  • Stefan Dötterl
Original Article
  • 151 Downloads

Abstract

Allium is a large monocotyledonous genus, with many species of high economic importance. Knowledge of the pollination biology and the chemical ecology of pollination in this genus is far from being complete. We studied flower visitors of some Allium species in their native habitat and how these interaction partners communicate by olfactory cues. Floral volatiles of five Mediterranean species were investigated by dynamic headspace and thermal desorption-gas chromatography/mass spectrometry. Floral visitors were observed and captured. The physiological activity of scent components in antennae of flower visitors and congeneric species was tested by gas chromatographic/electroantennographic detections. In the scent samples of the five species, 36 volatile organic compounds (VOCs) were detected. The species-specific scent profiles were dominated either by one or two aromatic compounds, or by a monoterpene. We recorded several insects on the flowers/inflorescences of the different Allium species, mainly bees and flies, with only a few visitor taxa shared among the studied species. In the physiological measurements, specific/congeneric visitors did not only respond to VOCs of the species they visited, but also to VOCs of species on which they were not recorded. Our study shows that inflorescence scent and visitor patterns do not correlate, and that although single visitors detected compounds of various Allium species, there was only a limited overlap in visitor spectrum among the species. Our study also adds several compounds to the list of floral scents being EAD-active in bees and flies.

Keywords

Apis Eristalis GC/EAD GC/MS Lasioglossum Pollination 

Notes

Acknowledgements

We thank Dr. Irmgard Schäffler for supporting the scent analyses and for constructive discussions.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

606_2019_1601_MOESM1_ESM.pdf (135 kb)
Supplementary material 1 (PDF 135 kb)
606_2019_1601_MOESM2_ESM.pdf (292 kb)
Supplementary material 2 (PDF 292 kb)
606_2019_1601_MOESM3_ESM.pdf (338 kb)
Supplementary material 3 (PDF 338 kb)

References

  1. Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectrometry. Allured Publishing Corporation, Carol StreamGoogle Scholar
  2. Akbarzadeh K, Wallman JF, Sulakova H, Szpila K (2015) Species identification of Middle Eastern blowflies (Diptera: Calliphoridae) of forensic importance. Parasitol Res 114:1463–1472.  https://doi.org/10.1007/s00436-015-4329-y CrossRefPubMedPubMedCentralGoogle Scholar
  3. Amiet F (1996) Hymenoptera Apidae, 1. Teil. Allgemeiner Teil, Gattungsschlüssel, Die Gattungen Apis, Bombus und Psithyrus. Insecta Helvetica, vol. 12. Musée d'histoire naturelle, NeuchâtelGoogle Scholar
  4. Amiet F, Hermann M, Müller A, Neumeyer R (2001) Apidae 4. Anthidium, Chelostoma, Coelioxys, Dioxys, Heriades, Lithurgus, Megachile, Osmia, Stelis. Fauna Helvetica, vol. 9. CSCF und SEG, NeuchâtelGoogle Scholar
  5. Amiet F, Hermann M, Müller A, Neumeyer R (2010) Apidae 6. Andrena, Melitturga, Panurginus, Panurgus. Fauna Helvetica, vol. 26. CSCF und SEG, NeuchâtelGoogle Scholar
  6. Åström H, Hæggström CA (2004) Generative reproduction in Allium oleraceum (Alliaceae). Ann Bot Fenn 41:1–14. https://www.jstor.org/stable/23727168 Google Scholar
  7. Braunschmid H, Mükisch B, Rupp T, Schäffler I, Zito P, Birtele D, Dötterl S (2017) Interpopulation variation in pollinators and floral scent of the lady’s-slipper orchid Cypripedium calceolus L. Arthropod-Pl Interact 11:363–379.  https://doi.org/10.1007/s11829-017-9512-x CrossRefGoogle Scholar
  8. Brullo S, Pavone P, Salmeri C, Tzanoudakis D (1994) Cytotaxonomical revision or the Allium obtusiflorum group (Alliaceae). Fl Medit 4:179–190.  https://doi.org/10.7320/FlMedit CrossRefGoogle Scholar
  9. Burger H, Dötterl S, Ayasse M (2010) Host-plant finding and recognition by visual and olfactory floral cues in an oligolectic bee. Funct Ecol 24:1234–1240.  https://doi.org/10.1111/j.1365-2435.2010.01744.x CrossRefGoogle Scholar
  10. Byers KJRP, Bradshaw HD, Riffell JA (2014) Three floral volatiles contribute to differential pollinator attraction in monkeyflowers (Mimulus). J Exp Biol 217:614–623.  https://doi.org/10.1242/jeb.092213 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chittka L, Raine NE (2006) Recognition of flowers by pollinators. Curr Opin Pl Biol 9:428–435.  https://doi.org/10.1016/j.pbi.2006.05.002 CrossRefGoogle Scholar
  12. Clarke KR, Gorley RN (2015) PRIMER V7: user manual/tutorial. PRIMER-E, PlymouthGoogle Scholar
  13. Currah L, Ockendon DJ (1978) Protandry and the sequence of flower opening in the onion (Allium cepa L.). New Phytol 81:419–428.  https://doi.org/10.1111/j.1469-8137.1978.tb02647.x CrossRefGoogle Scholar
  14. Dathe HH, Scheuchl E, Ockermüller E (2016) Illustrierte Bestimmungstabelle für die Arten der Gattung Hylaeus F. (Maskenbienen) in Deutschland, Österreich und der Schweiz. Entomol Austr 1:51Google Scholar
  15. Dellinger AS, Scheer LM, Artuso S, Fernández-Fernández DM, Sornoza F, Penneys DS, Tenhaken R, Dötterl S, Schönenberger J (2019) Bimodal pollination systems in Andean Melastomataceae involving birds, bats and rodents. Amer Naturalist 194:104–116.  https://doi.org/10.1086/703517 CrossRefGoogle Scholar
  16. Devi S, Gulati R, Tehri K, Poonia A (2015) The pollination biology of onion (Allium cepa L.). A review. Agric Rev 36:1–13.  https://doi.org/10.5958/0976-0741.2015.00001.X CrossRefGoogle Scholar
  17. Dobson HEM, Arroyo J, Bergström G, Groth I (1997) Interspecifc variation in floral fragrances within the genus Narcissus (Amaryllidaceae). Biochem Syst Ecol 25:686–706.  https://doi.org/10.1016/S0305-1978(97)00059-8 CrossRefGoogle Scholar
  18. Donnini D, Branca F (2011) Allium lehmannii. The IUCN red list of threatened species 2011: e.T172236A6854855. Available at:  https://doi.org/10.2305/IUCN.UK.2011-1.RLTS.T172236A6854855.en
  19. Dötterl S, Vereecken NJ (2010) The chemical ecology and evolution of bee–flower interactions: a review and perspectives. Canad J Zool 88:668–697.  https://doi.org/10.1139/Z10-031 CrossRefGoogle Scholar
  20. 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 169:447–460.  https://doi.org/10.1111/j.1095-8339.2012.01239.x CrossRefGoogle Scholar
  21. Ebmer AW (1969) Die Bienen des Genus Halictus LATR. s.l. im Großraum von Linz (Hymenoptera, Apidae). Teil I. Naturk Jahrb Stadt Linz 1969:133–184Google Scholar
  22. Ebmer AW (1970) Die Bienen des Genus Halictus LATR. s.l. im Großraum von Linz (Hymenoptera, Apidae). Teil II. Naturk Jahrb Stadt Linz 1970:19–82Google Scholar
  23. Ebmer AW (1971) Die Bienen des Genus Halictus LATR. s.l. im Großraum von Linz (Hymenoptera, Apidae). Teil III. Naturk Jahrb Stadt Linz 1971:63–156Google Scholar
  24. Ebmer AW (1974) Die Bienen des Genus Halictus LATR. s.l. im Großraum von Linz (Hymenoptera, Apoidea). Nachtrag und zweiter Anhang. Naturk Jahrb Stadt Linz 1973:123–158Google Scholar
  25. Ebmer AW (1987) Die europäischen Arten der Gattung Halictus LATREILLE 1804 und Lasioglossum CURTIS 1833 mit illustrierten Bestimmungstabellen (Insecta: Hymenoptera: Apoidea: Halictidae: Halictinae.). 1 Allgemeiner Teil, Tabelle der Gattungen. Senckenberg Biol 68:59–148Google Scholar
  26. Ekşi G, Koyuncu M, Özkan AMG (2016) Allium ekimianum: a new species (Amaryllidaceae) from Turkey. PhytoKeys 62:83–93.  https://doi.org/10.3897/phytokeys.62.7796 CrossRefGoogle Scholar
  27. El-Sayed AM (2018) The pherobase: database of pheromones and semiochemicals. Available at: http://www.pherobase.com. Accessed 23 Sept 2018
  28. Ervik F, Tollsten L, Knudsen JT (1999) Floral scent chemistry and pollination ecology in phytelephantoid palms (Arecaceae). Pl Syst Evol 217:279–297. https://www.jstor.org/stable/23643677 CrossRefGoogle Scholar
  29. Farré-Armengol G, Filella I, Llusia J, Peñuelas J (2015) Relationships among floral VOC emissions, floral rewards and visits of pollinators in five plant species of a Mediterranean shrubland. Pl Ecol Evol 148:90–99.  https://doi.org/10.5091/plecevo.2015.963 CrossRefGoogle Scholar
  30. Filella I, Primante C, Llusia J, Martín González AM, Seco R, Farré-Armengol G, Rodrigo A, Bosch J, Peñuelas J (2013) Floral advertisement scent in a changing plant-pollinators market. Sci Rep 3:3434.  https://doi.org/10.1038/srep03434 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Fritsch RM, Blattner FR, Gurushidze M (2010) New classification of Allium L. subg. Melanocrommyum (Webb & Berthel) Rouy (Alliaceae) based on molecular and morphological characters. Phyton (Horn) 49:145–220Google Scholar
  32. Füssel U, Dötterl S, Jürgens A, Aas G (2007) Inter- and intraspecific variation in floral scent in the genus Salix and its implication for pollination. J Chem Ecol 33:749–765.  https://doi.org/10.1007/s10886-007-9257-6 CrossRefPubMedGoogle Scholar
  33. Garbari F, Raimondo FM (1987) Sulla tipificazione di Allium lehmannii Lojac. (Alliaceae), specie di Sicilia e di Calabria. Giorn Bot Ital 121:47–54.  https://doi.org/10.1080/11263508709431645 CrossRefGoogle Scholar
  34. Heiduk A, Brake I, Tschirnhaus M, Haenni JP, Miller R, Hash J, Prieto-Benítez S, Jürgens A, Johnson SD, Schulz S, Liede-Schumann S, Meve U, Dötterl S (2017) Floral scent and pollinators of Ceropegia trap flower. Flora 232:169–182.  https://doi.org/10.1016/j.flora.2017.02.001 CrossRefGoogle Scholar
  35. James DG (2005) Further field evaluation of synthetic herbivore-induced plan volatiles as attractants for beneficial insects. J Chem Ecol 31:481–495.  https://doi.org/10.1007/s10886-005-2020-y CrossRefPubMedGoogle Scholar
  36. 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 175:624–640.  https://doi.org/10.1111/boj.12183 CrossRefGoogle Scholar
  37. Kamenetsky R, Rabinowitch HD (2006) The genus Allium: a developmental and horticultural analysis. Hortic Rev 32:329–337.  https://doi.org/10.1002/9780470767986.ch7 CrossRefGoogle Scholar
  38. Kell SP (2011) Allium obtusiflorum. The IUCN red list of threatened species 2011: e.T172148A6837426. Available at:  https://doi.org/10.2305/IUCN.UK.2011-1.RLTS.T172148A6837426.en
  39. Knudsen JT, Eriksson R, Gershenzon J, Ståhl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120.  https://doi.org/10.1663/0006-8101(2006)72%5b1:DADOFS%5d2.0.CO;2 CrossRefGoogle Scholar
  40. Kobayashi K, Arai M, Tanaka A, Matsuyama S, Honda H, Ohsawa R (2012) Variation in floral scent compounds recognized by honeybees in Brassicaceae crop species. Breeding Sci 62:293–302.  https://doi.org/10.1270/jsbbs.62.293 CrossRefGoogle Scholar
  41. Laloi D, Bailez O, Blight MM, Roger B, Pham-Delègue MH, Wadhams LJ (2000) Recognition of complex odors by restrained and free-flying honeybees, Apis mellifera. J Chem Ecol 26:2307–2319.  https://doi.org/10.1023/A:1005522826673 CrossRefGoogle Scholar
  42. Lanzotti V, Scala F, Bonanomi G (2014) Compounds from Allium species with cytotoxic and antimicrobial activity. Phytochem Rev 13:769–791.  https://doi.org/10.1007/s11101-014-9366-0 CrossRefGoogle Scholar
  43. Li QQ, Zhou SD, He XJ, Yu Y, Zhang YC, Wei XQ (2010) Phylogeny and biogeography of Allium (Amaryllidaceae: Allieae) based on nuclear ribosomal internal transcribed spacer and chloroplast rps16 sequences, focusing on the inclusion of species endemic to China. Ann Bot (Oxfrod) 106:709–733.  https://doi.org/10.1093/aob/mcq177 CrossRefGoogle Scholar
  44. Maia ACD, Dötterl S, Kaiser R, Silberbauer-Gottsberger I, Teichert H, Gibernau M, Navarro DMAF, Schlindwein C, Gottsberger G (2012) The key role of 4-methyl-5-vinylthiazole in the attraction of scarab beetle pollinators: a unique olfactory floral signal shared by Annonaceae and Araceae. J Chem Ecol 38:1072–1080.  https://doi.org/10.1007/s10886-012-0173-z CrossRefPubMedGoogle Scholar
  45. Marotz-Clausen G, Jürschik S, Fuchs R, Schäffler I, Sulzer P, Gibernau M, Dötterl S (2018) Incomplete synchrony of inflorescence scent and temperature patterns in Arum maculatum L. (Araceae). Phytochemistry 154:77–84.  https://doi.org/10.1016/j.phytochem.2018.07.001 CrossRefPubMedGoogle Scholar
  46. Mas F, Harper A, Horner R, Welsh T, Jaksons P, Suckling DM (2018) The importance of key floral bioactive compounds to honey bees for the detection and attraction of hybrid vegetable crops and increased seed yield. J Sci Food Agric 98:4445–4453.  https://doi.org/10.1002/jsfa.8967 CrossRefPubMedGoogle Scholar
  47. Milet-Pinheiro P, Ayasse M, Schlindwein C, Dobson HEM, Dötterl S (2012) Host location by visual and olfactory floral cues in an oligolectic bee: innate and learned behavior. Behav Ecol 23:531–538.  https://doi.org/10.1093/beheco/arr219 CrossRefGoogle Scholar
  48. Pignatti S (1982) Flora d’Italia. Edagricole, BolognaGoogle Scholar
  49. Povolný D, Verves Y (1997) The flesh-flies of Central Europe (Insecta, Diptera, Sarcophagidae). Spixiana Suppl 24:1–260Google Scholar
  50. Raguso RA (2008) Wake up and smell the roses: the ecology and evolution of floral scent. Annual Rev Ecol Evol Syst 39:549–569.  https://doi.org/10.1146/annurev.ecolsys.38.091206.095601 CrossRefGoogle Scholar
  51. Salzmann CC, Nardella AM, Cozzolino S, Schiestl FP (2007) Variability in floral scent in rewarding and deceptive orchids: the signature of pollinator-imposed selection? Ann Bot (Oxford) 100:757–765.  https://doi.org/10.1093/aob/mcm161 CrossRefGoogle Scholar
  52. Scheuchl E, Willner W (2016) Taschenlexikon der Wildbienen Mitteleuropas. Quelle & Meyer Verlag, WiebelsheimGoogle Scholar
  53. Séguy E (1923) Diptères: anthomyides. No. 6. Paris: Éditions Faune de France. Available at: http://faunedefrance.org/bibliotheque/docs/E.SEGUY(FdeFr06)Dipt.Anthomyides.pdf
  54. Séguy E (1926) Diptères (Brachycères): Stratomyiidae, Erinnidae, Coenomyiidae, Rhagionidae, Tabanidae, Oncodidae, Nemestrinidae, Mydaidae, Bombyliidae, Therevidae, Omphralidae. No 13. Paris: Éditions Faune de France. Available at: http://faunedefrance.org/bibliotheque/docs/E.SEGUY(FdeFr13)Dipteres.pdf
  55. Séguy E (1934) Diptères (Brachycères): Muscidae acalypterae et Scatophagidae. No. 28. Paris: Éditions Faune de France. Available at: http://www.faunedefrance.org/bibliotheque/docs/E.SEGUY(FdeFr28)Dipt.Brachyceres.pdf
  56. Shemesh E, Scholten O, Rabinowitch HD, Kamenetsky R (2008) Unlocking variability: inherent variation and developmental traits of garlic plants originated from sexual reproduction. Planta 227:1013–1024.  https://doi.org/10.1007/s00425-007-0675-z CrossRefPubMedGoogle Scholar
  57. Smith KGV (1969) Diptera: Conopidae. Royal entomological society of London handbook, vol. 10, part 3a. Royal Entomological Society, London. Avilable at: https://www.royensoc.co.uk/sites/default/files/Vol10_Part03a.pdf
  58. Sobolewska D, Michalska K, Podolak I, Grabowska K (2016) Steroidal saponins from the genus Allium. Phytochem Rev 15:1–35.  https://doi.org/10.1007/s11101-014-9381-1 CrossRefPubMedGoogle Scholar
  59. Soto VC, Maldonado IB, Jofré VP, Galmarini CR, Silva MF (2015) Direct analysis of nectar and floral volatile organic compounds in hybrid onions by HS-SPME/GC–MS: relationship with pollination and seed production. Microchem J 122:110–118.  https://doi.org/10.1016/j.microc.2015.04.017 CrossRefGoogle Scholar
  60. Speight MCD, Sarthou JP (2014) StN key for the identification of the genera of European Syrphidae (Diptera). Syrph the Net, the database of European Syrphidae. Syrph the Net Publications, DublinGoogle Scholar
  61. Urru I, Stökl J, Linz J, Kruegel T, Stensmyr MC, Hansson BS (2010) Pollination strategies in Cretan Arum lilies. Biol J Linn Soc 101:991–1001.  https://doi.org/10.1111/j.1095-8312.2010.01537.x CrossRefGoogle Scholar
  62. Waser NM, Ollerton J (2006) Plant-pollinator interactions: from specialization to generalization. University of Chicago Press, ChicagoGoogle Scholar
  63. Westrich P (1989) Die Wildbienen Baden-Württembergs. 2 Bände. E. Ulmer, StuttgartGoogle Scholar
  64. Wiemer AP, More M, Benitez-Vieyra S, Cocucci AA, Raguso RA, Sersic AN (2009) A simple floral fragrance and unusual osmophore structure in Cyclopogon elatus (Orchidaceae). Pl Biol 11:506–514.  https://doi.org/10.1111/j.1438-8677.2008.00140.x CrossRefGoogle Scholar
  65. Zammouri J, Guetat A, Neffati M (2009) Morpho-phenological characterization of Allium roseum L. (Alliaceae) from different bioclimatic zones in Tunisia. Afric J Agric Res 4:1004–1014.  https://doi.org/10.5897/AJAR CrossRefGoogle Scholar
  66. Zhu JW, Park KC (2005) Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. J Chem Ecol 31:1733–1746.  https://doi.org/10.1007/s10886-005-5923-8 CrossRefPubMedGoogle Scholar
  67. Zito P, Tavella F, Sajeva M, Carimi F, Dötterl S (2018) Inflorescence scents of Calendula maritima, Calendula suffruticosa subsp. fulgida, and their hybrid. Int J Pl Sci 179:415–421.  https://doi.org/10.1086/697240 CrossRefGoogle Scholar
  68. Zuraw B, Weryszko-Chmielewska E, Laskowska H, Pogroszewska E (2009) The structure of septal nectaries and nectar presentation in the flowers of Allium aflatunense B. Fedtsch. Acta Agrobotanica 62:31–41CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biological, Chemical and Pharmaceutical Sciences and TechnologiesUniversity of PalermoPalermoItaly
  2. 2.Institute of Biosciences and Bioresources, Division of PalermoNational Research Council of ItalyPalermoItaly
  3. 3.PuchenauAustria
  4. 4.Department of BiosciencesParis Lodron University of SalzburgSalzburgAustria

Personalised recommendations