Abstract
Adult Vanessa indica and Argyreus hyperbius frequently forage on flower nectar, but the former also utilizes tree sap and rotting fruits. Compared to flower nectar, these rotting foods are characterized by low sugar concentrations and the presence of fermentation products (ethanol and acetic acid). We suspected that gustatory responses by the receptors on the proboscis might differ in these species. Among the three sugars tested, sucrose elicited the greatest probing (behavioral) responses and was followed by fructose and glucose. A. hyperbius showed higher sugar sensitivity than V. indica in probing responsiveness. In electrophysiological responses of the proboscis sensilla, V. indica was slightly more sensitive than A. hyperbius to glucose and lower concentrations of the other sugars. The sugar reception in A. hyperbius was strongly inhibited by fermentation products, particularly acetic acid at natural concentrations. In contrast, V. indica was noticeably less susceptible to them than A. hyperbius, and its behavioral and sensory responses to sucrose were enhanced by 5–20% (w/v) ethanol. Thus, V. indica not only possesses tolerance to fermentation products but may perceive them as synergists for sugar reception. To utilize rotting foods, such tolerance might be more necessary than high sugar sensitivity.
Similar content being viewed by others
References
Adler PH (1989) Sugar feeding of the adult corn earworm (Lepidoptera: Noctuidae) in the laboratory. J Econ Entomol 82:1344–1349
Altner H, Altner I (1986) Sensilla with both, terminal pore and wall pores on the proboscis of the moth, Rhodogastria bubo Walker (Lepidoptera: Arctiidae). Zool Anz 216:129–150
Bernays EA, Glendinning JI, Chapman RF (1998) Plant acids modulate chemosensory responses in Manduca sexta larvae. Physiol Entomol 23:193–201
Blaney WM, Simmonds MSJ (1988) Food selection in adults and larvae of three species of Lepidoptera: a behavioural and electrophysiological study. Entomol Exp Appl 49:111–121
Chadwick LE, Dethier VG (1947) The relationship between chemical structure and the response of blowflies to tarsal stimulation by aliphatic acids. J Gen Physiol 30:255–262
Chapman (2003) Contact chemoreception in feeding by phytophagous insects. Annu Rev Entomol 48:455–484
Dethier VG, Chadwick LE (1947) Rejection thresholds of the blowfly for a series of aliphatic alcohols. J Gen Physiol 30:247–253
Frings H, Frings M (1949) The loci of contact chemoreceptors in insects. A review with new evidence. Am Midl Nat 41:602–658
Frings H, Frings M (1956) The loci of contact chemoreceptors involved in feeding reactions in certain Lepidoptera. Biol Bull 110:291–299
Guyenot E (1912) Les papilles de la trompe des Lepidopteres. Bull Biol Fr Belg 46:279–343
Hodgson ES (1958) Electrophysiological studies of arthropod chemoreception. III. Chemoreceptors of terrestrial and fresh-water arthropods. Biol Bull 115:114–125
Kawazoe A, Wakabayasi M (1976) Colored illustrations of the butterflies of Japan. Hoikusha, Osaka (in Japanese)
Krenn HW (1998) Proboscis sensilla in Vanessa cardui (Nymphalidae, Lepidoptera): functional morphology and significance in flower-probing. Zoomorphology 118:23–30
Krenn HW, Zulka KP, Gatschnegg T (2001) Proboscis morphology and food preference in nymphalid butterflies (Lepidoptera: Nymphalidae). J Zool Lond 254:17–26
Krenn HW, Plant JD, Szucsich NU (2005) Mouthparts of flower-visiting insects. Arthropod Struct Dev 34:1–40
Kristensen NP (2003) Lepidoptera: moths and butterflies 2. Handbook of zoology IV, vol 35. De Gruyter, Berlin
Lopez JD Jr, Lingren PD, Bull DL (1995) Proboscis extension response of adult Helicoverpa zea (Lepidoptera: Noctuidae) to dry sugars. J Econ Entomol 88:1271–1278
Marion-Poll F, van der Pers J (1996) Un-filtered recordings from insect taste sensilla. Entomol Exp Appl 80:113–115
McCutchan MC (1969) Behavioral and electrophysiological responses of the blowfly, Phormia regina Meigen, to acids. Z Vgl Physiol 65:131–152
Mitchell BK (1987) Interactions of alkaloids with galeal chemosensory cells of Colorado potato beetle. J Chem Ecol 13:2009–2022
Molleman F, Krenn HW, van Alphen ME, Brakefield PM, Devries PJ, Zwaan BJ (2005) Food intake of fruit-feeding butterflies: evidence for adaptive variation in proboscis morphology. Biol J Linn Soc 86:333–343
Morita H (1959) Inhibition of spike potentials in contact chemosensory hairs of insects. III. D. C. stimulation and generator potentials of labellar chemoreceptor of Calliphora. J Cell Comp Physiol 54:189–204
Omand E, Dethier VG (1969) An electrophysiological analysis of the action of carbohydrates on the sugar receptor of the blowfly. Proc Natl Acad Sci USA 62:136–143
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 49:1031–1038
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 25:281–287
Ômura H, Honda K, Hayashi N (2001) Corrigendum. Physiol Entomol 26:283
Ozaki M, Tominaga Y (1999) Contact chemoreceptors. In: Eguchi E, Tominaga Y (eds) Atlas of arthropod sensory receptors. dynamic morphology in relation to function. Springer, Tokyo, pp 143–154
Paulus HF, Krenn HW (1996) Vergleichende Morphologie des Schmetterlingsrüssels und seiner Sensillen – Ein Beitrag zur phylogenetischen Systematik der Papilionoidea (Insecta, Lepidoptera). J Zool Syst Evol Res 34:203–216
Pellmyr O (1992) Evolution of insect pollination and angiosperm diversification. Trend Ecol Evol 7:46–49
Petr D, Stewart KW (2004) Comparative morphology of sensilla styloconica on the proboscis of North American Nymphalidae and other selected taxa (Lepidoptera): systematic and ecological considerations. Trans Am Entomol Soc 130:293–409
Ramaswamy SB, Cohen NE, Hanson FE (1992) Deterrence of feeding and oviposition responses of adult Heliothis virescens by some compounds bitter-tasting to humans. Entomol Exp Appl 65:81–93
Rüth E (1976) Elektrophysiologie der Sensilla Chaetica auf den Antennen von Periplaneta americana. J Comp Physiol 105:55–64
Salama HS, Khalifa A, Azmy N, Sharaby A (1984) Gustation in the lepidopterous moth Spodoptera littoralis (Boisd.). Zool Jb Physiol 88:165–178
Schoonhoven LM (1982) Biological aspects of antifeedants. Entomol Exp Appl 31:57–69
Schoonhoven LM, Blaney WM, Simmonds MSJ (1992) Sensory coding of feeding deterrents in phytophagous insects. In: Bernays EA (ed) Insect–plant interactions, vol 4. CRC Press, Boca Raton, pp 59–79
Städler E, Seabrook WD (1975) Chemoreceptors on the proboscis of the female eastern spruce budworm: electrophysiological study. Entomol Exp Appl 18:153–160
Städler E, Städler-Steinbrüchel M, Seabrook WD (1974) Chemoreceptors on the proboscis of the female eastern spruce budworm. Morphological and histological study. Mitt Schweiz Entomol Gesellsch 47:63–68
Takeda K (1961) The nature of impulses of single tarsal chemoreceptors in the butterfly, Vanessa indica. J Cell Comp Physiol 58:233–245
van Loon JJA (1990) Chemoreception of phenolic acids and flavonoids in larvae of two species of Pieris. J Comp Physiol A 166:889–899
van Loon JJA (1996) Chemosensory basis of oviposition and feeding behaviour in herbivorous insects. Entomol Exp Appl 80:7–13
Walters BD, Albert PJ, Zacharuk RY (1998) Morphology and ultrastructure of sensilla on the proboscis of the adult spruce budworm, Choristoneura fumiferana (Clem.) (Lepidoptera: Tortricidae). Can J Zool 76:466–479
Acknowledgements
This study was financially supported in part by the Sasakawa Scientific Research Grant from the Japan Science Society and by a Grant-in-Aid (No. 18780036) from the Japan Society for the Promotion of Science to H. Ômura.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ômura, H., Honda, K., Asaoka, K. et al. Tolerance to fermentation products in sugar reception: gustatory adaptation of adult butterfly proboscis for feeding on rotting foods. J Comp Physiol A 194, 545–555 (2008). https://doi.org/10.1007/s00359-008-0330-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-008-0330-6