Journal of Chemical Ecology

, Volume 44, Issue 4, pp 406–415 | Cite as

Identification of Floral Volatiles and Pollinator Responses in Kiwifruit Cultivars, Actinidia chinensis var. chinensis

  • A. M. Twidle
  • D. Barker
  • A. G. Seal
  • B. Fedrizzi
  • D. M. Suckling


Volatiles emitted from unpollinated in situ flowers were collected from two male cultivars, ‘M33’, ‘M91’, and one female cultivar ‘Zesy002’ (Gold3) of kiwifruit (Actinidia chinensis var. chinensis). The samples were found to contain 48 compounds across the three cultivars with terpenes and straight chain alkenes dominating the headspace. Electrophysiological responses of honey bees (Apis mellifera) and bumble bees (Bombus terrestris) to the headspace of the kiwifruit flowers were recorded. Honey bees consistently responded to 11 floral volatiles from Gold3 pistillate flowers while bumble bees consistently responded to only five compounds from the pistillate flowers. Nonanal, 2-phenylethanol, 4-oxoisophorone and (3E,6E)-α-farnesene from pistillate flowers elicited responses from both bee species. Overall, honey bees were more sensitive to the straight chain hydrocarbons of the kiwifruit flowers than the bumble bees, which represented one of the main differences between the responses of the two bee species. The floral volatiles from staminate flowers of the male cultivars ‘M33’ and ‘M91’ varied greatly from those of the pistillate flowers of the female cultivar Gold3, with most of the bee active compounds significantly different from those in the Gold3 flower headspace. The total floral emissions of ‘M33’ flowers were significantly less than those of the Gold3 flowers, while the total floral emissions of the ‘M91’ flowers were significantly greater than those of the Gold3 flowers.


Floral volatiles Kiwifruit Bombus terrestris Apis mellifera Electroantennogram 



Funding for this project was provided by the New Zealand Ministry of Business, Innovation and Employment (Contract # C11X1309). We thank Flore Mas and Kye Chung Park for useful discussions and Ruth Butler for advice on statistical analyses. We are grateful to Heywood Orchards Ltd. for access to kiwifruit vines, and thank Shona Seymour for identifying vine cultivars.


  1. Ando T, S-i I, Yamamoto M (2004) Lepidopteran sex pheromones. In: Schulz S (ed) The chemistry of pheromones and other Semiochemicals I. Springer, Berlin Heidelberg, Berlin, pp 51–96CrossRefGoogle Scholar
  2. Appelgren M, Bergstrom G, Svensson BG, Cederberg B (1991) Marking pheromones of megabombus bumble bee males. Acta Chem Scand 45:972–974. CrossRefGoogle Scholar
  3. Birch MC, Haynes KF (1982) Insect pheromones. Edward Arnold, LondonGoogle Scholar
  4. Clarke D, Whitney H, Sutton G, Robert D (2013) Detection and learning of floral electric fields by bumblebees. Science 340:66–69. CrossRefPubMedGoogle Scholar
  5. Costa G, Ferguson AR (2015) Bacterial canker of kiwifruit: response to a threat. Acta Hortic (1095):27-40.
  6. Craig JL, Stewart AM, Pomeroy N, Heath ACG, Goodwin RM, Craig JL, Stewart AM (1988) A review of kiwifruit pollination - where to next. N Z J Exp Agric 16:385–399Google Scholar
  7. Dani FR, Jones GR, Corsi S, Beard R, Pradella D, Turillazzi S (2005) Nestmate recognition cues in the honey bee: differential importance of Cuticular alkanes and alkenes. Chem Senses 30:477–489. CrossRefPubMedGoogle Scholar
  8. Del Piccolo F, Nazzi F, Della Vedova G, Milani N (2010) Selection of Apis mellifera workers by the parasitic mite Varroa destructor using host cuticular hydrocarbons. Parasitology 137:967–973. CrossRefPubMedGoogle Scholar
  9. Díaz P, Grüter C, Farina W (2007) Floral scents affect the distribution of hive bees around dancers. Behav Ecol Sociobiol 61:1589–1597. CrossRefGoogle Scholar
  10. Du Y-j, Millar JG (1999) Electroantennogram and oviposition bioassay responses of Culex quinquefasciatus and Culex tarsalis (Diptera: Culicidae) to Chemicals in Odors from Bermuda grass infusions. J Med Entomol 36(2):158–166. CrossRefPubMedGoogle Scholar
  11. El-Sayed AM (2017) The Pherobase: Database of Insect Pheromones and Semiochemicals. <> 2003-2017 - The Pherobase - Ashraf M. El-Sayed
  12. Farina WM, Grüter C, Díaz PC (2005) Social learning of floral odours inside the honeybee hive. Proc R Soc B Biol Sci 272:1923–1928. CrossRefGoogle Scholar
  13. Ferguson AR, Seal AG, Davison RM (1990) Cultivar improvement, genetics and breeding of kiwifruit. Acta Hortic (282):335-348.
  14. Goodwin M, Haine H (1995) How many bee visits to fully pollinate kiwifruit? N Z Kiwifruit 111:5Google Scholar
  15. Goodwin RM, Ten Houten A, Perry JH (1991) Feeding sugar syrup to honey bee colonies to improve kiwifruit pollen collection: a review. Acta Hortic (288):265-269.
  16. Goodwin RM, McBrydie HM, Taylor MA (2013) Wind and honey bee pollination of kiwifruit (Actinidia chinensis 'HORT16A'). N Z J Bot 51:229–240. CrossRefGoogle Scholar
  17. Greene MJ, Gordon DM (2003) Social insects: Cuticular hydrocarbons inform task decisions. Nature 423:32–32CrossRefPubMedGoogle Scholar
  18. Henning JA, Teuber LR (1992) Combined gas chromatography-electroantennogram characterization of alfalfa floral volatiles recognized by honey bees (hymenoptera: Apidae). J Econ Entomol 85:226–232CrossRefGoogle Scholar
  19. Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393. CrossRefPubMedGoogle Scholar
  20. Howlett BG, Read SFJ, Jesson LK, Benoist A, Evans LE, Pattemore DE (2017) Diurnal insect visitation patterns to ‘Hayward’ kiwifruit flowers in New Zealand. N Z Plant Prot 70:52–57Google Scholar
  21. Knudsen JT, Tollsten L, Bergström LG (1993) Floral scents—a checklist of volatile compounds isolated by head-space techniques. Phytochemistry 33:253–280. CrossRefGoogle Scholar
  22. 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. Breed Sci 62:293–302. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Kunze J, Gumbert A (2001) The combined effect of color and odor on flower choice behavior of bumble bees in flower mimicry systems. Behav Ecol 12:447–456. CrossRefGoogle Scholar
  24. Martin SJ, Carruthers JM, Williams PH, Drijfhout FP (2010) Host specific social parasites (Psithyrus) indicate chemical recognition system in bumblebees. J Chem Ecol 36:855–863. CrossRefPubMedGoogle Scholar
  25. Matheson AG (1991) Managing honey bee pollination of kiwifruit (Actinidia deliciosa) in New Zealand - a review. Acta Hortic (288):213–219Google Scholar
  26. Matich AJ, Young H, Allen JM, Wang MY, Fielder S, McNeilage MA, MacRae EA (2003) Actinidia arguta: volatile compounds in fruit and flowers. Phytochemistry 63:285–301. CrossRefPubMedGoogle Scholar
  27. Nazzi F, Milani N, Vedova GD (2002) (Z)-8-heptadecene from infested cells reduces the reproduction of Varroa destructor under laboratory conditions. J Chem Ecol 28:2181–2190CrossRefPubMedGoogle Scholar
  28. Nieuwenhuizen NJ, Wang MY, Matich AJ, Green SA, Chen XY, Yauk YK, Beuning LL, Nagegowda DA, Dudareva N, Atkinson RG (2009) Two terpene synthases are responsible for the major sesquiterpenes emitted from the flowers of kiwifruit (Actinidia deliciosa). J Exp Bot 60:3203–3219. CrossRefPubMedPubMedCentralGoogle Scholar
  29. O'Rourke AD (2016) World kiwifruit review. Belrose, Inc., PullmanGoogle Scholar
  30. Pomeroy N, Fisher RM (2002) Pollination of kiwifruit (Actinidia deliciosa) by bumble bees (Bombus terrestris): effects of bee density and patterns of flower visitation. N Z Entomol 25:41–49CrossRefGoogle Scholar
  31. Read PEC, Donovan BJ, Griffin RP (1989) Use of bumble bees, Bombus terrestris, as pollinators of kiwifruit and lucerne in New Zealand. N Z Entomol 12:19–23CrossRefGoogle Scholar
  32. Samadi-Maybodi A, Shariat MR, Zarei M, Rezai MB (2002) Headspace analysis of the male and female flowers of kiwifruit grown in Iran. J Essent Oil Res 14:414–415CrossRefGoogle Scholar
  33. Schiestl FP, Marion-Poll F (2002) Detection of physiologically active flower volatiles using gas chromatography coupled with Electroantennography. In: Jackson JF, Linskens HF (eds) Analysis of taste and aroma. Springer Berlin Heidelberg, BerlinGoogle Scholar
  34. Schroeder CA, Fletcher WA (1967) The Chinese gooseberry (Actinidia chinensis) in New Zealand. Econ Bot 21:81–92CrossRefGoogle Scholar
  35. Seal AG, Clark CJ, Sharrock KR, de Silva HN, Jaksons P, Wood ME (2017) Choice of pollen donor affects weight but not composition of Actinidia chinensis Var. chinensis ‘Zesy002’ (Gold3) kiwifruit. N Z J Crop Hortic Sci:1–11.
  36. Struble DL, Arn H (1984) Combined gas chromatography and Electroantennogram recording of insect olfactory responses. In: Hummel HE, Miller TA (eds) Techniques in pheromone research. Springer New York, New York, pp 161–178CrossRefGoogle Scholar
  37. Tatsuka K, Suekane S, Sakai Y, Sumitani H (1990) Volatile constituents of kiwifruit flowers: simultaneous distillation and extraction versus headspace sampling. J Agric Food Chem 38:2176–2180. CrossRefGoogle Scholar
  38. Thiery D, Bluet JM, Pham-Delegue MH, Etievant P, Masson C (1990) Sunflower aroma detection by the honeybee. Study by coupling gas chromatography and electroantennography. J Chem Ecol 16:701–711. CrossRefPubMedGoogle Scholar
  39. Twidle AM, Mas F, Harper AR, Horner RM, Welsh TJ, Suckling DM (2015) Kiwifruit flower odor perception and recognition by honey bees, Apis mellifera. J Agric Food Chem 63:5597–5602. CrossRefPubMedGoogle Scholar
  40. Twidle AM, Suckling DM, Seal AG, Fedrizzi B, Pilkington LI, Barker D (2017) Identification of in situ flower volatiles from kiwifruit (Actinidia chinensis Var. deliciosa) cultivars and their male pollenisers in a New Zealand orchard. Phytochemistry 141:61–69. CrossRefPubMedGoogle Scholar
  41. von Frisch K (1974) Decoding the language of the bee. Science (New York, NY) 185:663–668.

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • A. M. Twidle
    • 1
    • 2
  • D. Barker
    • 2
  • A. G. Seal
    • 3
  • B. Fedrizzi
    • 2
  • D. M. Suckling
    • 1
    • 4
  1. 1.The New Zealand Institute for Plant & Food Research Ltd, Canterbury Research CentreLincolnNew Zealand
  2. 2.School of Chemical SciencesUniversity of AucklandAucklandNew Zealand
  3. 3.The New Zealand Institute for Plant & Food Research LimitedTe PukeNew Zealand
  4. 4.School of Biological SciencesUniversity of AucklandAucklandNew Zealand

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