Journal of Ecology and Environment

The Ecological Society of Korea (한국생태학회)
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Comparative analysis of volatile organic compounds from flowers attractive to honey bees and bumblebees

  • Dekebo, Aman (Agricultural Science and Technology Institute, Andong National University) ;
  • Kim, Min-Jung (Agricultural Science and Technology Institute, Andong National University) ;
  • Son, Minwoong (Department of Plant Medicals, Andong National University) ;
  • Jung, Chuleui (Agricultural Science and Technology Institute, Andong National University)
  • Received : 2021.12.31
  • Accepted : 2022.02.14
  • Published : 2022.03.31
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Abstract

Background: Pollinators help plants to reproduce and support economically valuable food for humans and entire ecosystems. However, declines of pollinators along with population growth and increasing agricultural activities hamper this mutual interaction. Nectar and pollen are the major reward for pollinators and flower morphology and volatiles mediate the specialized plant-pollinator interactions. Limited information is available on the volatile profiles attractive to honey bees and bumblebees. In this study we analyzed the volatile organic compounds of the flowers of 9 different plant species that are predominantly visited by honey bees and bumblebees. The chemical compositions of the volatiles were determined using a head space gas chromatography-mass spectrometry (GC-MS) method, designed to understand the plant-pollinator chemical interaction. Results: Results showed the monoterpene 1,3,6-octatriene, 3,7-dimethyl-, (E) (E-𝞫-ocimene) was the dominating compound in most flowers analyzed, e.g., in proportion of 60.3% in Lonicera japonica, 48.8% in Diospyros lotus, 38.4% Amorpha fruticosa and 23.7% in Robinia pseudoacacia. Ailanthus altissima exhibited other monoterpenes such as 3,7-dimethyl-1,6-octadien-3-ol (𝞫-linalool) (39.1%) and (5E)-3,5-dimethylocta-1,5,7-trien-3-ol (hotrienol) (32.1%) as predominant compounds. Nitrogen containing volatile organic compounds (VOCs) were occurring principally in Corydalis speciosa; 1H-pyrrole, 2,3-dimethyl- (50.0%) and pyrimidine, 2-methyl- (40.2%), and in Diospyros kaki; 1-triazene, 3,3-dimethyl-1-phenyl (40.5%). Ligustrum obtusifolium flower scent contains isopropoxycarbamic acid, ethyl ester (21.1%) and n-octane (13.4%) as major compounds. In Castanea crenata the preeminent compound is 1-phenylethanone (acetophenone) (46.7%). Conclusions: Olfactory cues are important for pollinators to locate their floral resources. Based on our results we conclude monoterpenes might be used as major chemical mediators attractive to both honey bees and bumblebees to their host flowers. However, the mode of action of these chemicals and possible synergistic effects for olfaction need further investigation.

Keywords

Acknowledgement

We appreciate Prof. Victor Benno Meyer-Rochow for English correction and proof reading of the manuscript.

References

  1. Arenas A, Fernandez VM, Farina WM. Floral odor learning within the hive affects honeybees' foraging decisions. Naturwissenschaften. 2007;94(3):218-22. https://doi.org/10.1007/s00114-006-0176-0.
  2. Arenas A, Fernandez VM, Farina WM. Floral scents experienced within the colony affect long-term foraging preferences in honeybees. Apidologie. 2008;39(6):714-22. https://doi.org/10.1051/apido:2008053.
  3. Balkenius A, Rosen W, Kelber A. The relative importance of olfaction and vision in a diurnal and a nocturnal hawkmoth. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2006;192(4):431-7. https://doi.org/10.1007/s00359-005-0081-6.
  4. Beekman M. How long will honey bees (Apis mellifera L.) be stimulated by scent to revisit past-profitable forage sites? J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2005;191(12):1115-20. https://doi.org/10.1007/s00359-005-0033-1.
  5. Borg-Karlson AK, Unelius CR, Valterova I, Nilsson LA. Floral fragrance chemistry in the early flowering shrub Daphne mezereum. Phytochemistry. 1996;41(6):1477-83. https://doi.org/10.1016/0031-9422(95)00801-2.
  6. Chen C, Song Q. Responses of the pollinating wasp Ceratosolen solmsi marchali to odor variation between two floral stages of Ficus hispida. J Chem Ecol. 2008;34(12):1536-44. https://doi.org/10.1007/s10886-008-9558-4.
  7. Diaz PC, Gruter C, Farina WM. Floral scents affect the distribution of hive bees around dancers. Behav Ecol Sociobiol. 2007;61(10):1589-97. https://doi.org/10.1007/s00265-007-0391-5
  8. Dobson HE. Floral volatiles in insect biology. In: Bernays EA, editor. Insect-plant interactions. 5th ed. Boca Raton: CRC press; 2017. p. 47-82.
  9. Dobson HE. Relationship between floral fragrance composition and type of pollinator. In: Dudareva N, Pichersky E, editors. Biology of floral scent. Boca Raton: CRC press; 2006. p. 147-98.
  10. Dornhaus A, Chittka L. Evolutionary origins of bee dances. Nature. 1999;401(6748):38. https://doi.org/10.1038/43372.
  11. Dotterl S, Gluck U, Jurgens A, Woodring J, Aas G. Floral reward, advertisement and attractiveness to honey bees in dioecious Salix caprea. PLoS One. 2014;9(3):e93421. https://doi.org/10.1371/journal.pone.0093421.
  12. Dotterl S, Milchreit K, Schaffler I. Behavioural plasticity and sex differences in host finding of a specialized bee species. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2011;197(12):1119-26. https://doi.org/10.1007/s00359-011-0673-2.
  13. Dotterl S, Vereecken N. The chemical ecology and evolution of bee-flower interactions: a review and perspectives. Can J Zool. 2010;88(7):668-97. https://doi.org/10.1139/Z10-031.
  14. Dudareva N, Martin D, Kish CM, Kolosova N, Gorenstein N, Faldt J, et al. (E)-beta-ocimene and myrcene synthase genes of floral scent biosynthesis in snapdragon: function and expression of three terpene synthase genes of a new terpene synthase subfamily. Plant Cell. 2003;15(5):1227-41. https://doi.org/10.1105/tpc.011015.
  15. Effmert U, Grosse J, Rose US, Ehrig F, Kagi R, Piechulla B. Volatile composition, emission pattern, and localization of floral scent emission in Mirabilis jalapa (Nyctaginaceae). Am J Bot. 2005;92(1):2-12. https://doi.org/10.3732/ajb.92.1.2.
  16. Farre-Armengol G, Fernandez-Martinez M, Filella I, Junker RR, Penuelas J. Deciphering the biotic and climatic factors that influence floral scents: a systematic review of floral volatile emissions. Front Plant Sci. 2020;11:1154. https://doi.org/10.3389/fpls.2020.01154.
  17. Farre-Armengol G, Filella I, Llusia J, Penuelas J. Floral volatile organic compounds: between attraction and deterrence of visitors under global change. Perspect Plant Ecol Evol Syst. 2013;15(1):56-67. https://doi.org/10.1016/j.ppees.2012.12.002.
  18. Fernandes N, Silva FAN, de Aragao F, Zocolo GJ, Freitas BM. Volatile organic compounds role in selective pollinator visits to commercial melon types. J Agric Sci. 2019;11(3):93-108. https://doi.org/10.5539/jas.v11n3p93.
  19. Filella I, Primante C, Llusia J, Martin Gonzalez AM, Seco R, Farre-Armengol G, et al. Floral advertisement scent in a changing plant-pollinators market. Sci Rep. 2013;3(1):3434. https://doi.org/10.1038/srep03434.
  20. Free J. Influence of the odour of a honeybee colony's food stores on the behaviour of its foragers. Nature. 1969;222(5195):778. https://doi.org/10.1038/222778a0.
  21. Funamoto D. Plant-pollinator interactions in East Asia: a review. J Pollinat Ecol. 2019;25(6):46-68. https://doi.org/10.26786/1920-7603(2019)532.
  22. Getz WM, Smith KB. Olfactory sensitivity and discrimination of mixtures in the honeybeeApis mellifera. J Comp Physiol. 1987;160(2):239-45. https://doi.org/10.1007/BF00609729.
  23. Giurfa M, Vorobyev M, Kevan P, Menzel R. Detection of coloured stimuli by honeybees: minimum visual angles and receptor specific contrasts. J Comp Physiol A. 1996;178(5):699-709. https://doi.org/10.1007/BF00227381.
  24. Gong WC, Chen G, Vereecken NJ, Dunn BL, Ma YP, Sun WB. Floral scent composition predicts bee pollination system in five butterfly bush (Buddleja, Scrophulariaceae) species. Plant Biol (Stuttg). 2015;17(1):245-55. https://doi.org/10.1111/plb.12176.
  25. Granero AM, Sanz JM, Gonzalez FJ, Vidal JL, Dornhaus A, Ghani J, et al. Chemical compounds of the foraging recruitment pheromone in bumblebees. Naturwissenschaften. 2005;92(8):371-4. https://doi.org/10.1007/s00114-005-0002-0.
  26. Henning JA, Teuber LR. Cornbined gas chromatography-electroantennogram characterization of alfalfa floral volatiles recognized by honey bees (Hymenoptera: Apidae). J Econ Entomol. 1992;85(1):226-32. https://doi.org/10.1093/jee/85.1.226.
  27. Hiraiwa MK, Ushimaru A. Low functional diversity promotes niche changes in natural island pollinator communities. Proc Biol Sci. 2017;284(1846):20162218. https://doi.org/10.1098/rspb.2016.2218.
  28. Jakobsen H, Kristjansson K, Rohde B, Terkildsen M, Olsen CE. Can social bees be influenced to choose a specific feeding station by adding the scent of the station to the hive air? J Chem Ecol. 1995;21(11):1635-48. https://doi.org/10.1007/BF02033666.
  29. Johnson DL. Communication among honey bees with field experience. Anim Behav. 1967;15(4):487-92. https://doi.org/10.1016/0003-3472(67)90048-6.
  30. Johnson SD, More M, Amorim FW, Haber WA, Frankie GW, Stanley DA, et al. The long and the short of it: a global analysis of hawkmoth pollination niches and interaction networks. Funct Ecol. 2017;31(1):101-15. https://doi.org/10.1111/1365-2435.12753.
  31. Kaiser L, De Jong R. Multi-odour memory influenced by learning order. Behav Processes. 1993;30(2):175-83. https://doi.org/10.1016/0376-6357(93)90007-E.
  32. Kevan PG, Lane MA. Flower petal microtexture is a tactile cue for bees. Proc Natl Acad Sci U S A. 1985;82(14):4750-2. https://doi.org/10.1073/pnas.82.14.4750.
  33. Khalifa SA, Elshafiey EH, Shetaia AA, El-Wahed AAA, Algethami AF, Musharraf SG, et al. Overview of bee pollination and its economic value for crop production. Insects. 2021;12(8):688. https://doi.org/10.3390/insects12080688.
  34. Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, et al. Importance of pollinators in changing landscapes for world crops. Proc Biol Sci. 2007;274(1608):303-13. https://doi.org/10.1098/rspb.2006.3721.
  35. Koltermann R. [Learning and forgetting processes in the honey bee-demonstrated using scent exercises]. Z Vgl Physiol. 1969;63(3):310-34. German. https://doi.org/10.1007/BF00298165.
  36. Lacher V. [Electrophysiological studies on individual receptors for smell, carbon dioxide, air humidity and temperature on the antennae of worker bees and drones (Apis mellifica L.)]. Z Vgl Physiol. 1964;48:587-623. German. https://doi.org/10.1007/BF00333743.
  37. Lindauer M, Kerr WE. Communication between the workers of stingless bees. Bee World. 1960;41(2):29-41. https://doi.org/10.1080/0005772X.1960.11095309.
  38. Maisonnasse A, Lenoir JC, Beslay D, Crauser D, Le Conte Y. E-β-ocimene, a volatile brood pheromone involved in social regulation in the honey bee colony (Apis mellifera). PLoS One. 2010;5(10):e13531. https://doi.org/10.1371/journal.pone.0013531.
  39. Maisonnasse A, Lenoir JC, Costagliola G, Beslay D, Crauser D, Plettner E, et al. E-β-ocimene a new volatile primer pheromone that inhibits worker ovary development in honey bees. Paper presented at: International Union for the Study of Social Insects - French Section; 2009 Sep 2-4; Bondy, France. Tours: UIEIS, 2009. hal-02755737.
  40. Menzel R, Erber J, Masuhr T. Learning and memory in the honeybee. In: Barton Browne L, editor. Experimental analysis of insect behaviour. Berlin: Springer; 1974. p. 195-217.
  41. Menzel R. Learning in honey bees in an ecological and behavioral context. Fortschr Zool. 1985;31:55-74.
  42. Molet M, Chittka L, Raine NE. How floral odours are learned inside the bumblebee (Bombus terrestris) nest. Naturwissenschaften. 2009;96(2):213-9. https://doi.org/10.1007/s00114-008-0465-x.
  43. Ollerton J. Biogeography: are tropical species less specialised? Curr Biol. 2012;22(21):R914-5. https://doi.org/10.1016/j.cub.2012.09.023.
  44. Ollerton J. Pollinator diversity: distribution, ecological function, and conservation. Annu Rev Ecol Evol Syst. 2017;48:353-76. https://doi.org/10.1146/annurev-ecolsys-110316-022919.
  45. Omura H, Honda K. Priority of color over scent during flower visitation by adult Vanessa indica butterflies. Oecologia. 2005;142(4):588-96. https://doi.org/10.1007/s00442-004-1761-6.
  46. Pecetti L, Tava A, Felicioli A, Pinzauti M, Piano E. Effect of three volatile compounds from lucerne flowers on their attractiveness towards pollinators. Bull Insectol. 2002;55(1-2):21-7.
  47. Proctor M, Yeo P. The pollination of flowers. New York: Taplinger; 1973.
  48. R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2021.
  49. Raguso RA, Willis MA. Synergy between visual and olfactory cues in nectar feeding by naive hawkmoths, Manduca sexta. Anim Behav. 2002;64(5):685-95. https://doi.org/10.1006/anbe.2002.4010
  50. Reinhard J, Srinivasan MV, Guez D, Zhang SW. Floral scents induce recall of navigational and visual memories in honeybees. J Exp Biol. 2004a;207(Pt 25):4371-81. https://doi.org/10.1242/jeb.01306.
  51. Reinhard J, Srinivasan MV, Zhang S. Olfaction: scent-triggered navigation in honeybees. Nature. 2004b;427(6973):411. https://doi.org/10.1038/427411a.
  52. Ribbands CR. Communication between honeybees. I: The response of crop-attached bees to the scent of their crop. Proc R Entomol Soc Lond Ser A Gen Entomol. 1954;29(10-12):141-4. https://doi.org/10.1111/j.1365-3032.1954.tb01187.x.
  53. Roy BA, Raguso RA. Olfactory versus visual cues in a floral mimicry system. Oecologia. 1997;109(3):414-26. https://doi.org/10.1007/s004420050101.
  54. Shimada T, Endo T, Fujii H, Hara M, Omura M. Isolation and characterization of (E)-beta-ocimene and 1,8 cineole synthases in Citrus unshiu Marc. Plant Sci. 2005;168(4):987-95. https://doi.org/10.1016/j.plantsci.2004.11.012.
  55. Smith BH, Breed MD. The chemical basis for nestmate recognition and mate discrimination in social insects. In: Carde RT, Bell WJ, editors. Chemical ecology of insects 2. New York: Chapman & Hall; 1995. p. 287-317.
  56. Smith BH. The olfactory memory of the honeybee Apis Mellifera: I. Odorant modulation of short- and intermediate-term memory after single-trial conditioning. J Exp Biol. 1991;161(1):367-82. https://doi.org/10.1242/jeb.161.1.367.
  57. Vareschi E. [Odor discrimination in the honey bee-single cell recordings and behavioral responses]. Z Vgl Physiol. 1971;75(2):143-73. German. https://doi.org/10.1007/BF00335260.
  58. Ward JH. Hierarchical grouping to optimize an objective function. J Am Stat Assoc. 1963;58(301):236-44. https://doi.org/10.1080/01621459.1963.10500845
  59. Wenner AM, Wells PH, Johnson DL. Honey bee recruitment to food sources: olfaction or language? Science. 1969;164(3875):84-6. https://doi.org/10.1126/science.164.3875.84.
  60. Whitney HM, Kolle M, Andrew P, Chittka L, Steiner U, Glover BJ. Floral iridescence, produced by diffractive optics, acts as a cue for animal pollinators. Science. 2009;323(5910):130-3. https://doi.org/10.1126/science.1166256.
  61. Williams NH, Whitten WM. Orchid floral fragrances and male euglossine bees: methods and advances in the last sesquidecade. Biol Bull. 1983;164(3):355-95. https://doi.org/10.2307/1541248.
  62. Zanata TB, Dalsgaard B, Passos FC, Cotton PA, Roper JJ, Maruyama PK, et al. Global patterns of interaction specialization in bird-flower networks. J Biogeogr. 2017;44(8):1891-910. https://doi.org/10.1111/jbi.13045.
  63. Zhang S, Schwarz S, Pahl M, Zhu H, Tautz J. Honeybee memory: a honeybee knows what to do and when. J Exp Biol. 2006;209(Pt 22):4420-8. https://doi.org/10.1242/jeb.02522.