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Journal of Chemical Ecology

, Volume 32, Issue 6, pp 1289–1300 | Cite as

Ethanol and Methanol as Possible Odor Cues for Egyptian Fruit Bats (Rousettus aegyptiacus)

  • Francisco Sánchez
  • Carmi Korine
  • Marco Steeghs
  • Luc-Jan Laarhoven
  • Simona M. Cristescu
  • Frans J. M. Harren
  • Robert Dudley
  • Berry Pinshow
Article

Abstract

Frugivorous bats from the Old and New World use odor cues to locate and assess fruit condition. We hypothesized that Egyptian fruit bats (Rousettus aegyptiacus) use as odor cues those volatile compounds that increase in emission rate as fruit ripens. We examined whether the smell of fermentation products may indicate the degree of ripeness to fruit bats. We analyzed volatile compounds in the headspace (the gas space above a fruit in a closed container) of dates (Phoenix dactylifera) and rusty figs (Ficus rubiginosa), both of which are consumed by fruit bats, to elucidate which compounds originate from fermentative pathways and to determine which change in emission rate during ripening. Ethanol, acetaldehyde, and acetic acid were the only volatile compounds detected as products of fermentation in both fruits. In dates, emission rates of these compounds increased during maturation, whereas in rusty figs, they decreased or remained constant. Methanol, although not a fermentation product, increased in emission rate during ripening in both fruits. We found that R. aegyptiacus was neither attracted nor deterred by the smell of methanol at any of the concentrations used. Although the odor of ethanol emanating from food containing concentrations similar to those found in ripe fruit did not attract the bats, at relatively high concentrations (≥1%), the smell of ethanol deterred them. Thus, ethanol at high concentrations may serve as a signal for bats to avoid overripe, unpalatable fruit.

Keywords

Ethanol Fermentation Ficus rubiginosa Food selection Fruit-eating bats Methanol Odorcues Olfaction Phoenix dactylifera Rousettus aegyptiacus Volatile compounds 

Notes

Acknowledgments

We thank A. Zabari, A. Fennec, and R. Glukhikh for their help capturing and maintaining the bats and to Prigat International Ltd. for contributing mango juice. We also thank two anonymous reviewers for constructive comments. Support by US–Israel Binational Science Foundation grant number 2001038 to C.K., B.P., and R.D., a stipend and a student research grant from the Mitrani Department of Desert Ecology (MDDE) to F.S., and a grant from the European Community, Access to Research Infrastructure–Improving Human Potential Programme to F.S. are gratefully acknowledged. This is paper number 571 of the MDDE.

References

  1. Acharya, K. K., Roy, A., and Krishna, A. 1998. Relative role of olfactory cues and certain non-olfactory factors in foraging of fruit-eating bats. Behav. Processes 44:59–64.CrossRefGoogle Scholar
  2. Black, K. A., Eells, J. T., Noker, P. E., Hawtrey, C. A., and Tephly, T. R. 1985. Role of tetrahydrofolate in the species differences in methanol toxicity. Proc. Natl. Acad. Sci. USA 82:3854–3858.PubMedCrossRefGoogle Scholar
  3. Boamfa, E. I., Steeghs, M. M. L., Cristescu, S. M., and Harren, F. J. M. 2004. Trace gas detection from fermentation processes in apples; an intercomparison study between proton-transfer-reaction mass spectrometry and laser photoacoustics. Int. J. Mass Spectrom. 239:193–201.CrossRefGoogle Scholar
  4. Cosse, A. A., Endris, J. J., Millar, J. G., and Baker, T. C. 1994. Identification of volatile compounds from fungus-infected date fruit that stimulate upwind flight in female Ectomyelois ceratoniae. Entomol. Exp. Appl. 72:233–238.CrossRefGoogle Scholar
  5. Dominy, N. J. 2004. Fruits, fingers, and fermentation: the sensory cues available to foraging Primates. Integr. Comp. Biol. 44:295–303.CrossRefGoogle Scholar
  6. Dudley, R. 2000. Evolutionary origins of human alcoholism in primate frugivory. Q. Rev. Biol. 75:3–15.CrossRefPubMedGoogle Scholar
  7. Dudley, R. 2002. Fermenting fruit and the historical ecology of ethanol ingestion: is alcoholism in modern humans an evolutionary hangover? Addiction 97:381–388.CrossRefPubMedGoogle Scholar
  8. Dudley, R. 2004. Ethanol, fruit ripening, and the historical origins of human alcoholism in primate frugivory. Integr. Comp. Biol. 44:315–323.CrossRefGoogle Scholar
  9. Fadda, F. and Rossetti, Z. L. 1998. Chronic ethanol consumption: from neuroadaptation to neurodegeneration. Prog. Neurobiol. 56:385–431.CrossRefPubMedGoogle Scholar
  10. Fleet, G. H. 2003. Yeast interactions and wine flavour. Int. J. Food Microbiol. 86:11–22.CrossRefPubMedGoogle Scholar
  11. Fleming, T. H., Haithaus, E. R., and Sawyer, W. B. 1977. An experimental analysis of the food location behavior of frugivorous bats. Ecology 58:619–627.CrossRefGoogle Scholar
  12. Frenkel, C., Peters, J. S., Tieman, D. M., Tiznado, M. E., and Handa, A. K. 1998. Pectin methylesterase regulates methanol and ethanol accumulation in ripening tomato (Lycopersicon esculentum) fruit. J. Biol. Chem. 273:4293–4295.CrossRefPubMedGoogle Scholar
  13. Hoffmann, A. A. and Parsons, P. A. 1984. Olfactory response and resource utilization in Drosophila: interspecific comparisons. Biol. J. Linn. Soc. 22:43–53.CrossRefGoogle Scholar
  14. Janzen, D. H. 1977. Why fruits rot, seeds mold, and meat spoils. Am. Nat. 111:691–713.CrossRefGoogle Scholar
  15. Kalko, E. K. V., Herre, E. A., and Handley, C. O. 1996. Relation of fig fruit characteristics to fruit-eating bats in the New and Old World tropics. J. Biogeogr. 23:565–576.CrossRefGoogle Scholar
  16. Korine, C., Izhaki, I., and Arad, Z. 1999. Is the Egyptian fruit-bat Rousettus aegyptiacus a pest in Israel? An analysis of the bat's diet and implications for its conservation. Biol. Conserv. 88:301–306.CrossRefGoogle Scholar
  17. Korine, C. and Kalko, E. K. V. 2005. Fruit detection and discrimination by small fruit-eating bats (Phyllostomidae): echolocation call design and olfaction. Behav. Ecol. Sociobiol. 59:12–23.CrossRefGoogle Scholar
  18. Laska, M. 1990. Olfactory sensitivity to food odor components in the short-tailed fruit bat, Carollia perspicillata (Phyllostomatidae, Chiroptera). J. Comp. Physiol. A 166:395–399.CrossRefGoogle Scholar
  19. Laska, M. and Schmidt, U. 1986. Olfactory orientation in Carollia perspicillata (Chiroptera). Mamm. Biol. 51:129–138.Google Scholar
  20. Laska, M. and Seibt, A. 2002. Olfactory sensitivity for aliphatic alcohols in squirrel monkeys and pigtail macaques. J. Exp. Biol. 205:1633–1643.Google Scholar
  21. Lefever, G., Vieuille, M., Delage, N., D'harlingue, A., De Monteclerc, J., and Bompeix, G. 2004. Characterization of cell wall enzyme activities, pectin composition, and technological criteria of strawberry cultivars (Fragaria × ananassa Duch). J. Food Sci. 69:221–226.Google Scholar
  22. Lieber, C. S. 2000. Alcohol: its metabolism and interaction with nutrients. Annu. Rev. Nutr. 20:395–430.CrossRefPubMedGoogle Scholar
  23. Lindinger, W., Hansel, A., and Jordan, A. 1998. On-line monitoring of volatile organic compounds at ppt levels by means of Proton Transfer Reaction Mass Spectrometry (PTR-MS): medical applications, food control and environmental research. Int. J. Mass Spectrom. 173:191–241.CrossRefGoogle Scholar
  24. Luft, S., Curio, E., and Tacud, B. 2003. The use of olfaction in the foraging behaviour of the golden-mantled flying fox, Pteropus pumilus, and the greater musky fruit bat, Ptenochirus jagori (Megachiroptera: Pteropodidae). Naturwissenschaften 90:84–87.PubMedGoogle Scholar
  25. Makar, A. B. and Tephly, T. R. 1976. Methanol poisoning in the folate-deficient rat. Nature 261:715–716.CrossRefPubMedGoogle Scholar
  26. Mangas, J. J., Cabranes, C., Moreno, J., and Gomis, D. B. 1994. Influence of cider-making technology on cider taste. Lebensm.-Wiss. Technol. 27:583–586.CrossRefGoogle Scholar
  27. Nursten, H. E. 1970. Volatile compounds: the aroma of fruits, pp. 239–268, in A. C. Hulme (ed.). The Biochemistry of Fruits and Their Products. Academic Press, London.Google Scholar
  28. Rieger, J. F. and Jakob, E. M. 1988. The use of olfaction in food location by frugivorous bats. Biotropica 20:161–164.CrossRefGoogle Scholar
  29. Rochat, D., Nagnan-Le Meillour, P., Esteban-Duran, J. R., Malosse, C., Perthuis, B., Morin, J. P., and Descoins, C. 2000. Identification of pheromone synergists in American palm weevil, Rhynchophorus palmarum, and attraction of related Dynamis borassi. J. Chem. Ecol. 26:155–187.CrossRefGoogle Scholar
  30. Rohan, T. A. 1972. The chemistry of flavor, pp. 57–69, in J. B. Harborne (ed.). Phytochemical Ecology. Proceedings of the Phytochemical Society Symposium No. 8. Academic Press, London.Google Scholar
  31. Sánchez, F., Korine, C., Pinshow, B., and Dudley, R. 2004. The possible roles of ethanol in the relationship between plants and frugivores: first experiments with Egyptian fruit bats. Integr. Comp. Biol. 44:290–294.CrossRefGoogle Scholar
  32. Senesi, E., Di Cesare, L. F., Prinzivalli, C., and Lo Scalzo, R. 2005. Influence of ripening stage on volatiles composition, physicochemical indexes and sensory evaluation in two varieties of muskmelon (Cucumis melo L var reticulates Naud). J. Sci. Agric. 85:1241–1251.CrossRefGoogle Scholar
  33. Sharaf, A., Ahmend, F. A., and El-Saadany, S. S. 1989. Biochemical changes in some fruits at different ripening stages. Food Chem. 31:19–28.CrossRefGoogle Scholar
  34. Shusterman, D., Osterloh, J. D., Ambre, J., Becker, C., Borak, J., Cannella, J., Kipen, H., Jackson, R. J., Rodnick, J., and Wummer, B. A. 1993. Methanol toxicity. Am. Fam. Physician. 47:163–171.PubMedGoogle Scholar
  35. Steeghs, M., Bais, H. P., De Gouw, J., Goldan, P., Kuster, W., Northway, M., Fall, R., and Vivanco, J. M. 2004. Proton-transfer-reaction mass spectrometry as a new tool for real time analysis of root-secreted volatile organic compounds in Arabidopsis. Plant Physiol. 135:47–58.CrossRefPubMedGoogle Scholar
  36. Supriyadi, S., Suzuki, M., Wu, S. Q., Tomita, N., Fujita, A., and Watanabe, N. 2003. Biogenesis of volatile methyl esters in snake fruit (Salacca edulis, Reinw) cv. Pondoh. Biosci. Biotechnol. Biochem. 67:1267–1271.CrossRefPubMedGoogle Scholar
  37. Tucker, G. A. 1993. Introduction, pp. 1–51, in G. B. Seymour, J. E. Taylor, and G. A. Tucker (eds.). Biochemistry of Fruit Ripening. Chapman & Hall, London.Google Scholar
  38. Utrio, P. and Eriksson, K. 1977. Volatile fermentation products as attractants for Macrolepidoptera. Ann. Zool. Fenn. 14:98–104.Google Scholar
  39. Vidrih, R. and Hribar, J. 1999. Synthesis of higher alcohols during cider processing. Food Chem. 67:287–294.CrossRefGoogle Scholar
  40. Zar, J. H. 1999. Biostatistical Analysis. Prentice Hall, Upper Saddle River, NJ.Google Scholar

Copyright information

© Springer Science + Business Media, Inc. 2006

Authors and Affiliations

  • Francisco Sánchez
    • 1
  • Carmi Korine
    • 1
  • Marco Steeghs
    • 2
  • Luc-Jan Laarhoven
    • 2
  • Simona M. Cristescu
    • 2
  • Frans J. M. Harren
    • 2
  • Robert Dudley
    • 3
  • Berry Pinshow
    • 1
  1. 1.Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert ResearchBen-Gurion University of the NegevMidreshet Ben-GurionIsrael
  2. 2.Life Science Trace Gas Facility, Department of Molecular and Laser PhysicsRadboud University of NijmegenNijmegenThe Netherlands
  3. 3.Department of Integrative BiologyUniversity of CaliforniaBerkeleyUSA

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