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Oecologia

, Volume 142, Issue 4, pp 588–596 | Cite as

Priority of color over scent during flower visitation by adult Vanessa indica butterflies

  • Hisashi Ômura
  • Keiichi Honda
Plant Animal Interactions

Abstract

Most flower visitors innately prefer a particular color and scent, and use them as cues for flower recognition and selection. However, in most cases, since color and scent serve as a combined signal, not only does the preference for an individual cue, but also the preference hierarchy among different cues, influence their flower visitation. In the present study, we attempted to reveal (1) the chromatic and (2) the olfactory cues that stimulate flower visiting, and (3) the preference hierarchy between these cues, using the naïve adult butterfly Vanessa indica. When we offered 12 different-colored (six chromatic and six achromatic) paper flower models, V. indica showed a color preference for yellow and blue. When we examined the proboscis extension reflex (PER) of V. indica towards 16 individual compounds identified in the floral scents from two nectar plants belonging to the family Compositae, Taraxacum officinale and Cirsium japonicum, six compounds were found to have relatively high PER-eliciting activities, including benzaldehyde, acetophenone, and (E+Z)-nerolidol. When we combined color and scent cues in two-choice bioassays, where butterflies were offered flower models that were purple (a relatively unattractive color), the models scented with these active compounds were significantly more attractive than the odorless controls. In addition, synthetic blends mimicking the floral scents of T. officinale and C. japonicum (at doses equivalent to that of ten flowers) enhanced the number of visits to the scented models. However, the effect of odorizing was not conspicuous in parallel bioassays when yellow flower models were used, and the butterflies also significantly preferred odorless yellow models to scented purple models. These results demonstrate that V. indica depends primarily on color and secondarily on scent during flower visitation.

Keywords

Flower selection Attractive color and scent Preference hierarchy Taraxacum officinale Cirsium japonicum 

Notes

Acknowledgements

This study was partially supported by a grant from the Interdisciplinary Research Institute of Environmental Sciences.

References

  1. Ômura H, Honda K (2003) Feeding responses of adult butterflies, Nymphalis xanthomelas, Kaniska canace and Vanessa indica, to components in tree sap and rotting fruits: synergistic effects of ethanol and acetic acid on sugar responsiveness. J Insect Physiol 49:1031–1038CrossRefPubMedGoogle Scholar
  2. Ômura H, Honda K, Hayashi N (1999) Chemical and chromatic bases for preferential visiting by the cabbage butterfly, Pieris rapae, to rape flowers. J Chem Ecol 25:1895–1906CrossRefGoogle Scholar
  3. Ômura H, Honda K, Hayashi N (2000) Identification of feeding attractants in oak sap for adults of two nymphalid butterflies, Kaniska canace and Vanessa indica. Physiol Entomol 25:281–287CrossRefGoogle Scholar
  4. Andersson S (2003) Foraging responses in the butterflies Inachis io, Aglais urticae (Nymphalidae), and Gonepteryx rhamni (Pieridae) to floral scents. Chemoecology 13:1–11CrossRefGoogle Scholar
  5. Andersson S, Dobson HEM (2003) Behavioral foraging responses by the butterfly Heliconius melpomene to Lantana camara floral scent. J Chem Ecol 29:2303–2318CrossRefPubMedGoogle Scholar
  6. Andersson S, Nilson 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
  7. Arikawa K, Inokuma K, Eguchi E (1987) Pentachromatic visual system in a butterfly. Naturwissenschaften 74:297–298CrossRefGoogle Scholar
  8. Barth FG (1991) Insects and flowers. The biology of a partnership. Princeton University Press, Princeton, NJGoogle Scholar
  9. Bolg-Karlson A-K (1990) Chemical and ethological studies of pollination in the genus Ophrys (Orchidaceae). Phytochemistry 29:1359–1387CrossRefGoogle Scholar
  10. Borges RM, Gowda V, Zacharias M (2003) Butterfly pollination and high-contrast visual signals in a low-density distylous plant. Oecologia 136:571–573CrossRefPubMedGoogle Scholar
  11. Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510CrossRefPubMedGoogle Scholar
  12. Briscoe AD, Bernard GD, Szeto AS, Nagy LM, White RH (2003) Not all butterfly eyes are created equal: rhodopsin absorption spectra, molecular identification, and localization of ultraviolet-, blue-, and green-sensitive rhodopsin-encoding mRNAs in the retina of Vanessa cardui. J Comp Neurol 458:334–349CrossRefPubMedGoogle Scholar
  13. Cantelo WW, Jacobson M (1979) Phenylacetaldehyde attracts moth to bladder flower and to blacklight traps. Environ Entomol 8:444–447Google Scholar
  14. Chittka L, Spaethe J, Schmidt A, Hickelsberger A (2001) Adaptation, constraint, and chance in the evolution of flower color and pollinator color vision. In: Chittka L, Thomson JD (eds) Cognitive ecology of pollination: animal behaviour and floral evolution. Cambridge University Press, Cambridge, pp 106–126Google Scholar
  15. Connick WJJ, French RC (1991) Volatiles emitted during the sexual stage of the Canada thistle rust fungus and by thistle flowers. J Agric Food Chem 39:185–188Google Scholar
  16. Dobson HEM (1994) Floral volatiles in insect biology. In: Bernays E (ed) Insect-plant interactions, vol 5. CRC Press, Boca Raton, FL, pp 47–81Google Scholar
  17. Goulson D, Cory JS (1993) Flower constancy and learning in foraging preferences of the green-veined white butterfly Pieris napi. Ecol Entomol 18:315–320Google Scholar
  18. Goulson D, Ollerton J, Sluman C (1997) Foraging strategies in the small skipper butterfly, Thymelicus flavus: when to switch? Anim Behav 53:1009–1016CrossRefGoogle Scholar
  19. Gumbert A, Kunze J (2001) Colour similarity to rewarding model plants affects pollination in a food deceptive orchid, Orchis boryi. Biol J Linn Soc 72:419–433CrossRefGoogle Scholar
  20. Haynes KF, Zhao JZ, Latif A (1991) Identification of floral compounds from Abelia grandiflora that stimulate upwind flight in cabbage looper moths. J Chem Ecol 17:637–646Google Scholar
  21. Heath RR, Landolt PJ, Dueben B, Lenczewski B (1992) Identification of floral compounds of night-blooming jessamine attractive to cabbage looper moths. Environ Entomol 21:854–859Google Scholar
  22. von Helversen O, Winkler L, Bestmann HJ (2000) Sulphur-containing “perfumes” attract flower-visiting bats. J Comp Physiol A 186:143–153CrossRefPubMedGoogle Scholar
  23. Honda K (1973) Olfactory response of adults of butterflies to odorous compounds I. Sasakia charonda Hewitson. Nat Insect (in Japanese) 8:21–24Google Scholar
  24. Honda K (1976) The role of olfactory and color senses in the feeding behavior in the adults of Nymphalis xanthomelas japonica Stichel (Lepidoptera: Nymphalidae), with description of the preference on colors of flowers in the flower-visiting behavior. Trans Lepid Soc Jpn (in Japanese with English summary) 27:52–58Google Scholar
  25. 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
  26. Ilse D (1928) Über den Farbensinn der Tagfalter. Z Verg Physiol 8:658–692CrossRefGoogle Scholar
  27. Ilse D, Vaidya VG (1956) Spontaneous feeding response to colours in Papilio demoleus L. Proc Indian Acad Sci Sec B 43:23–31Google Scholar
  28. Kandori I, Ohsaki N (1996) The learning abilities of the white cabbage butterfly, Pieris rapae, foraging for flowers. Res Popul Ecol 38:111–117Google Scholar
  29. Kelber A (1997) Innate preferences for flower features in the hawkmoth Macroglossum stellatarum. J Exp Biol 199:1227–1231Google Scholar
  30. Kelber A (2002) Pattern discrimination in a hawkmoth: innate preferences, learning performance and ecology. Proc R Soc Lond B Biol Sci 269:2573–2577CrossRefPubMedGoogle Scholar
  31. Kelber A, Pfaff M (1999) True colour vision in the orchard butterfly, Papilio aegeus. Naturwissenschaften 86:221–224CrossRefGoogle Scholar
  32. Kevan PG, Baker HG (1983) Insect as flower visitors and pollinators. Annu Rev Entomol 28:407–453CrossRefGoogle Scholar
  33. Kinoshita M, Shimada N, Arikawa K (1999) Colour vision of the foraging swallowtail butterfly Papilio xuthus. J Exp Biol 202:95–102PubMedGoogle Scholar
  34. Knudsen JT, Tollsten L, Bergström LG (1993) Floral scents—a checklist of volatile compounds isolated by head-space techniques. Phytochemistry 33:253–280CrossRefGoogle Scholar
  35. Kroutov V, Mayer MS, Emmel TC (1999) Olfactory conditioning of the butterfly Agraulis vanillae (L.) (Lepidoptera, Nymphalidae) to floral but not host-plant odors. J Insect Behav 12:833–843CrossRefGoogle Scholar
  36. 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 12:447–456CrossRefGoogle Scholar
  37. Leal WS, Ono M, Hasegawa M, Sawada M (1994) Kairomone from dandelion, Taraxacum officinale, attractant for scarab beetle Anomala octiescostata. J Chem Ecol 20:1697–1704Google Scholar
  38. Levin RA, Raguso RA, McDade LA (2001) Fragrance chemistry and pollinator affinities in Nyctaginaceae. Phytochemistry 58:429–440CrossRefPubMedGoogle Scholar
  39. Lewis AC (1989) Flower visit consistency in Pieris rapae, the cabbage butterfly. J Anim Ecol 58:1–13Google Scholar
  40. Lewis AC, Lipani GA (1990) Learning and flower use in butterflies: hypotheses from honey bees. In: Bernays EA (ed) Insect-plant interactions, vol 2. CRC Press, Boca Raton, FL, pp 95–110Google Scholar
  41. Lunau K (1993) Interspecific diversity and uniformity of flower colour patterns as cues for learned discrimination and innate detection of flowers. Experientia 49:1002–1010Google Scholar
  42. Lunau K, Maier EJ (1995) Innate colour preferences of flower visitors. J Comp Physiol A 177:1–19CrossRefGoogle Scholar
  43. Miyakawa M (1976) Flower-visiting behavior of small white butterfly, Pieris rapae crucivora. Annot Zool Jpn 49:261–273Google Scholar
  44. Pellmyr O (1986) Three pollination morphs in Cimicifuga simplex; incipient speciation due to inferiority in competition. Oecologia 68:304–307CrossRefGoogle Scholar
  45. Plepys D, Ibarra F, Francke W, Löfstedt C (2002) Odour-mediated nectar foraging in the silver Y moth, Autographa gamma (Lepidoptera: Noctuidae): behavioural and electrophysiological responses to floral volatiles. Oikos 99:75–82CrossRefGoogle Scholar
  46. Raguso RA, Willis MA (2002) Synergy between visual and olfactory cues in nectar feeding by naïve hawkmoths, Manduca sexta. Anim Behav 64:685–695CrossRefGoogle Scholar
  47. Raguso RA, Levin RA, Foose SE, Holmberg MW, McDade LA (2003) Fragrance chemistry, nocturnal rhythms and pollination “syndrome” in Nicotiana. Phytochemistry 63:265–284CrossRefPubMedGoogle Scholar
  48. Roy BA, Raguso RA (1997) Olfactory versus visual cues in a floral mimicry system. Oecologia 109:411–426CrossRefGoogle Scholar
  49. Roy BA, Widmer A (1999) Floral mimicry: a fascinating yet poorly understood phenomenon. Trends Plant Sci 4:325–330CrossRefPubMedGoogle Scholar
  50. Scherer C, Kolb G (1987a) Behavioral experiments on the visual processing of color stimuli in Pieris brassicae L. (Lepidoptera). J Comp Physiol A 160:645–656Google Scholar
  51. Scherer C, Kolb G (1987b) The influence of color stimuli on visually controlled behavior in Aglais urticae L. and Pararge aegeria L. (Lepidoptera). J Comp Physiol A 161:891–898Google Scholar
  52. Schoonhoven LM, Jermy T, van Loon JJA (1998) Insects and flowers: the beauty of mutualism. In: Schoonhoven LM, Jermy T, van Loon JJA (eds) Insect–plant biology. Chapman and Hall, London, pp 315–342Google Scholar
  53. Swihart SL (1970) The neural basis of colour vision in the butterfly, Papilio troilus. J Insect Physiol 16:1623–1636CrossRefGoogle Scholar
  54. Swihart CA, Swihart SL (1970) Colour selection and learned feeding preferences in the butterfly, Heliconius charitonius Linn. Anim Behav 18:60–64Google Scholar
  55. Vaidya VG (1969) Form perception in Papilio demouleus L. (Papilionidae, Lepidoptera). Behaviour 33:212–221PubMedGoogle Scholar
  56. Weiss MR (1997) Innate colour preferences and flexible colour learning in the pipevine swallowtail. Anim Behav 53:1043–1052CrossRefGoogle Scholar
  57. Weiss MR (2001) Vision and learning in some neglected pollinators: beetles, flies, moths, and butterflies. In: Chittka L, Thomson JD (eds) Cognitive ecology of pollination—animal behaviour and floral evolution. Cambridge University Press, Cambridge, pp 171–190Google Scholar
  58. Weiss MR, Papaj DR (2003) Colour learning in two behavioural contexts: how much can a butterfly keep in mind? Anim Behav 65:425–434CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Division of Environmental Sciences, Faculty of Integrated Arts and SciencesHiroshima UniversityHigashihiroshima, HiroshimaJapan

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