Journal of Chemical Ecology

, Volume 32, Issue 9, pp 1867–1881 | Cite as

Volatile Foraging Kairomones in the Littoral Zone: Attraction of an Herbivorous Freshwater Gastropod to Algal Odors

  • Patrick FinkEmail author
  • Eric von Elert
  • Friedrich Jüttner


Volatile organic compounds (VOCs) produced by algae and cyanobacteria are primarily responsible for odors in fresh waters. Among other functions, VOCs may serve as important infochemicals in biofilms of benthic primary producers. VOCs liberated by benthic, mat-forming cyanobacteria can be used as habitat-finding cues by insects, nematodes, and possibly other organisms. We developed a new gastropod behavioral assay that allows detection of food preference without offering food, thus allowing the distinction between taste, which requires direct contact with the food source, and the detection of odorous infochemicals, which work over distance. We demonstrated that VOCs released from disintegrated cells of a benthic, mat-forming, green alga (Ulothrix fimbriata) are food-finding cues (“foraging kairomones”) that attract the herbivorous freshwater snail Radix ovata. A mixture of three C5 lipoxygenase compounds and 2(E),4(E)-heptadienal that mimic the major VOCs released by U. fimbriata attracted the snails, whereas neither the mixture of C5 compounds nor 2(E),4(E)-heptadienal were effective when given alone. This study suggests that VOCs can play a steering role as infochemicals in freshwater benthic habitats, as has been established for many organismic interactions in terrestrial ecosystems.


Attractant Food choice Infochemicals Lipoxygenase products Nor-carotenoids Oxylipins Radix ovata Unsaturated aldehydes Ulothrix fimbriata Volatile organic compounds (VOC) Pulmonate Snail 



We thank P. Merkel and E. Loher for technical assistance with the VOC analyses and S. Boekhoff, B. Kumpfmüller, and T. Basen for assistance with the food choice assays. W. Nagl gave advice on the statistical analyses, and L. Peters helped with the figure of the experimental containers. We are indebted to M. Wolf for manufacturing the experimental containers and to K. Brune for language correction. This study was supported by the Deutsche Forschungsgemeinschaft within the Collaborative Research Centre SFB 454—“Littoral of Lake Constance.”


  1. Batten, J. H., Stutte, G. W., and Wheeler, R. M. 1995. Effect of crop development on biogenic emissions from plant populations grown in closed plant growth chambers. Phytochemistry 39:1351–1357.PubMedCrossRefGoogle Scholar
  2. Blackburn, N., Fenchel, T., and Mitchell, J. 1998. Microscale nutrient patches in planktonic habitats shown by chemotactic bacteria. Science 282:2254–2256.PubMedCrossRefGoogle Scholar
  3. Brendelberger, H. 1995. Dietary preference of three freshwater gastropods for eight natural foods of different energetic content. Malacologia 36:147–153.Google Scholar
  4. Brendelberger, H. 1997. Determination of digestive enzyme kinetics: a new method to define trophic niches in freshwater snails. Oecologia 109:34–40.CrossRefGoogle Scholar
  5. Calow, P. 1970. Studies on the natural diet of Lymnaea pereger obtusa (Kobelt) and its possible ecological implications. Proc. Malac. Soc. Lond. 39:203–215.Google Scholar
  6. Calow, P. and Calow, L. J. 1975. Cellulase activity and niche separation in freshwater gastropods. Nature 255:478–480.PubMedCrossRefGoogle Scholar
  7. Cattaneo, A. 1990. The effect of fetch on periphyton spatial variation. Hydrobiologia 206:1–10.CrossRefGoogle Scholar
  8. Croft, K. P. C., Jüttner, F., and Slusarenko, A. J. 1993. Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L) leaves inoculated with Pseudomonas syringae Pv-phaseolicola. Plant Physiol. 101:13–24.PubMedGoogle Scholar
  9. Croll, R. P. 1983. Gastropod chemoreception. Biol. Rev. 58:293–319.CrossRefGoogle Scholar
  10. Croll, R. P. and Chase, R. 1980. Plasticity of olfactory orientation to foods in the snail Achatina fulica. J. Comp. Physiol. 136:267–277.CrossRefGoogle Scholar
  11. Denny, M. 1980. Locomotion: The cost of gastropod crawling. Science 208:1288–1290.PubMedCrossRefGoogle Scholar
  12. Durrer, M., Zimmermann, U., and Jüttner, F. 1999. Dissolved and particle-bound geosmin in a mesotrophic lake (Lake Zürich): Spatial and seasonal distribution and the effect of grazers. Water Res. 33:3628–3636.CrossRefGoogle Scholar
  13. Evans, W. G. 1982. Oscillatoria sp. (Cyanophyta) mat metabolites implicated in habitat selection in Bembidion obtusidens (Coleoptera: Carabidae). J. Chem. Ecol. 8:671–678.CrossRefGoogle Scholar
  14. Fratini, S., Cannicci, S., and Vannini, M. 2001. Feeding clusters and olfaction in the mangrove snail Terebralia palustris (Linnaeus) (Potamididae: Gastropoda). J. Exp. Mar. Biol. Ecol. 261:173–183.PubMedCrossRefGoogle Scholar
  15. Gal, J., Bobkova, M. V., Zhukov, V. V., Shepeleva, I. P., and Meyer-Ruchow, V. B. 2004. Fixed focal-length optics in pulmonate snails (Mollusca, Gastropoda): Squaring phylogenetic background and ecophysiological needs (II). Inv. Biol. 123:116–127.CrossRefGoogle Scholar
  16. Gardner, H. W. 1991. Recent investigations into the lipoxygenase pathway of plants. Biochim. Biophys. Acta 1084:221–239.PubMedGoogle Scholar
  17. Guillard, R. R. L. and Lorenzen, C. J. 1972. Yellow-green algae with chlorophyllide c. J. Phycol. 8:10–14.Google Scholar
  18. Halitschke, R., Ziegler, J., Keinänen, M., and Baldwin, I. T. 2004. Silencing of hydroperoxide lyase and allene oxide synthase reveals substrate and defense signalling crosstalk in Nicotiana attenuata. Plant J. 40:35–46.PubMedCrossRefGoogle Scholar
  19. Harborne, J. B. 1995. Ökologische Biochemie. Eine Einführung. Spektrum Akademischer Verlag, Heidelberg.Google Scholar
  20. Höckelmann, C. and Jüttner, F. 2004. Volatile organic compound (VOC) analysis and sources of limonene, cyclohexanone and straight chain aldehydes in axenic cultures of Calothrix and Plectonema. Water Sci. Technol. 49:47–54.PubMedGoogle Scholar
  21. Höckelmann, C., Moens, T., and Jüttner, F. 2004. Odor compounds from cyanobacterial biofilms acting as attractants and repellents for free-living nematodes. Limnol. Oceanogr. 49:1809–1819.CrossRefGoogle Scholar
  22. Ianora, A., Miralto, A., Poulet, S. A., Carotenuto, Y., Buttino, I., Romano, G., Casotti, R., Pohnert, G., Wichard, T., Colucci-D'Amato, L., Terrazzano, G., and Smetacek, V. 2004. Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom. Nature 429:403–407.PubMedCrossRefGoogle Scholar
  23. ITIS 2004. Integrated Taxonomic Information System.
  24. Izaguirre, G. and Taylor, W. D. 1995. Geosmin and 2-methylisoborneol production in a major aqueduct system. Water Sci. Technol. 31:41–48.CrossRefGoogle Scholar
  25. John, D. M. 2002. Orders Chaetophorales, Klebshormidiales, Microsporales, Ulotrichales, pp. 714, in D. M. John, B. A. Whitton, and A. J. Brook (eds.). The Freshwater Algal Flora of the British Isles: An Identification Guide to Freshwater and Terrestrial Algae. Cambridge University Press, Cambridge, UK.Google Scholar
  26. Jüttner, F. 1987. Volatile organic substances, pp. 453–469, in P. Fay C. and Van Baalen (eds.). The Cyanobacteria. Elsevier, Amsterdam.Google Scholar
  27. Jüttner, F. 1988a. Biochemistry of biogenic off-flavour compounds in surface waters. Water Sci. Technol. 20:107–116.Google Scholar
  28. Jüttner, F. 1988b. Quantitative trace analysis of volatile organic compounds. Methods Enzymol. 167:609–616.CrossRefGoogle Scholar
  29. Jüttner, F. 1995. Physiology and biochemistry of odorous compounds from fresh-water cyanobacteria and algae. Water Sci. Technol. 31:69–78.CrossRefGoogle Scholar
  30. Jüttner, F. 2001. Liberation of 5,8,11,14,17-eicosapentaenoic acid and other polyunsaturated fatty acids from lipids as a grazer defense reaction in epilithic diatom biofilms. J. Phycol. 37:744–755.CrossRefGoogle Scholar
  31. Jüttner, F. 2005. Evidence that polyunsaturated aldehydes of diatoms are repellents for pelagic crustacean grazers. Aquat. Ecol. 39:271–282.CrossRefGoogle Scholar
  32. Jüttner, F. and Dürst, U. 1997. High lipoxygenase activities in epilithic biofilms of diatoms. Arch. Hydrobiol. 138:451–463.Google Scholar
  33. Jüttner, F., Leonhardt, J., and Möhren, S. 1983. Environmental factors affecting the formation of mesityloxide, dimethylallylic alcohol and other volatile compounds excreted by Anabaena cylindrica. J. Gen. Microbiol. 129:407–412.Google Scholar
  34. Kessler, A. and Baldwin, I. T. 2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144.PubMedCrossRefGoogle Scholar
  35. Klumpp, D. W., Salita-Espinosa, J. S., and Fortes, M. D. 1992. The role of ephiphytic periphyton and macroinvertebrate grazing in the trophic flux of a tropical seagrass community. Aquat. Bot. 43:327–349.CrossRefGoogle Scholar
  36. Lamberti, G. A., Gregory, S. V., Ashkenas, L. R., Li, J. L., Steinman, A. D., and McIntire, C. D. 1995. Influence of grazer type and abundance on plant-herbivore interactions in streams. Hydrobiologia. 306:179–188.CrossRefGoogle Scholar
  37. Lodge, D. M. 1986. Selective grazing on periphyton: a determinant of freshwater gastropod microdistributions. Freshw. Biol. 16:831–841.CrossRefGoogle Scholar
  38. Madsen, H. 1992. Food selection by freshwater snails in the gezira irrigation canals sudan. Hydrobiologia 228:203–217.Google Scholar
  39. Metcalf, R. L. 1987. Plant volatiles as insect attractants. CRC Crit. Rev. Plant Sci. 5:251–301.CrossRefGoogle Scholar
  40. Miralto, A., Barone, G., Romano, G., Poulet, S. A., Ianora, A., Russo, G. L., Buttino, I., Mazzarella, G., Laabir, M., Cabrini, M., and Glacobbe, M. G. 1999. The insidious effect of diatoms on copepod reproduction. Nature 402:173–176.CrossRefGoogle Scholar
  41. Müller, D. G., Jaenicke, L., Donike, M., and Akintobi, T. 1971. Sex attractant in a brown alga—chemical structure. Science 171:815.PubMedCrossRefGoogle Scholar
  42. Pinckney, J. L. and Zingmark, R. G. 1993. Modeling the annual production of intertidal benthic microalgae in estuarine ecosystems. J. Phycol. 29:396–407.CrossRefGoogle Scholar
  43. Pohnert, G. 2000. Wound-activated chemical defense in unicellular planktonic algae. Angew. Chem. Int. Ed. 39:4352–4354.CrossRefGoogle Scholar
  44. Pohnert, G. 2002. Phospholipase A2 activity triggers the wound-activated chemical defense in the diatom Thalassiosira rotula. Plant Physiol. 129:103–111.PubMedCrossRefGoogle Scholar
  45. Pohnert, G. and Boland, W. 1996. Biosynthesis of the algal pheromone hormosirene by the freshwater diatom Gomphonema parvulum (Bacillariophyceae). Tetrahedron 52:10073–10082.CrossRefGoogle Scholar
  46. Pohnert, G., Lumineau, O., Cueff, A., Adolph, S., Cordevant, C., Lange, M., and Poulet, S. 2002. Are volatile unsaturated aldehydes from diatoms the main line of chemical defence against copepods? Mar. Ecol. Prog. Ser. 245:33–45.CrossRefGoogle Scholar
  47. Reisser, W. 1993. Viruses and virus-like particles of fresh-water and marine eukaryotic algae—a review. Arch. Protistenkd. 143:257–265.Google Scholar
  48. Ruther, J., Meiners, T., and Steidle, J. L. M. 2002. Rich in phenomena—lacking in terms. A classification of kairomones. Chemoecology 12:161–167.CrossRefGoogle Scholar
  49. Simkin, A. J., Schwartz, S. H., Auldridge, M., Taylor, M. G., and Klee, H. J. 2004. The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles beta-ionone, pseudoionone, and geranylacetone. Plant J. 40:882–892.PubMedCrossRefGoogle Scholar
  50. Steinman, A. D., Mulholland, P. J., and Beauchamp, J. J. 1995. Effects of biomass, light, and grazing on phosphorus cycling in stream periphyton communities. J. N. Am. Benthol. Soc. 14:371–381.CrossRefGoogle Scholar
  51. Stevenson, R. J., Bothwell, M. L., and Lowe, R. L. 1996. Algal Ecology: Freshwater Benthic Ecosystems. Academic Press, San Diego.Google Scholar
  52. Streit, B. 1981. Food searching and exploitation by a primary consumer (Ancylus fluviatilis) in a stochastic environment—nonrandom movement patterns. Rev. Suisse Zool. 88:887.Google Scholar
  53. Teyke, T. 1995. Food attraction conditioning in the snail Helix pomatia. J. Comp. Physiol. A. 177:409–414.CrossRefGoogle Scholar
  54. Thomas, J. D. 1986. The chemical ecology of Biomphalaria glabrata (Say): Sugars as attractants and arrestants. Comp. Biochem. Physiol. A 83:457–460.CrossRefGoogle Scholar
  55. Thomas, J. D., Cowley, C., and Ofosu-Barko, J. 1980. Behavioural responses to amino acids and related compounds, including propionic acid, by adult Biomphalaria glabrata (Say), the snail host of Schistosoma mansoni. Comp. Biochem. Physiol. C. 66:17–27.CrossRefGoogle Scholar
  56. Thomas, J. D., Ofosu-Barko, J., and Patience, R. L. 1983. Behavioural responses to carboxylic and amino acids by Biomphalaria glabrata (Say), the snail host of Schistosoma mansoni (Sambon), and other freshwater molluscs. Comp. Biochem. Physiol. C. 75:57–76.CrossRefGoogle Scholar
  57. Thomas, J. D., Sterry, P. R., Jones, H., Gubala, M., and Grealy, B. M. 1986. The chemical ecology of Biomphalaria glabrata (Say): Sugars as phagostimulants. Comp. Biochem. Physiol. A. 83:461–475.CrossRefGoogle Scholar
  58. Thomas, J. D., Kowalczyk, C., and Somasundaram, B. 1989. The biochemical ecology of Biomphalaria glabrata, a snail host of Schistosoma mansoni: Short chain carboxylic and amino acids as phagostimulants. Comp. Biochem. Physiol. A. 93:899–911.PubMedCrossRefGoogle Scholar
  59. Turner, A. M., Bernot, R. J., and Boes, C. M. 2000. Chemical cues modify species interactions: the ecological consequences of predator avoidance by freshwater snails. Oikos 88:148–158.CrossRefGoogle Scholar
  60. Van Donk, E. 1989. The role of fungal parasites in phytoplankton succession, pp. 171–194, in U. Sommer (ed.). Plankton Ecology. Springer, Berlin.Google Scholar
  61. von Elert, E. and Loose, C. J. 1996. Predator-induced diel vertical migration in Daphnia: enrichment and preliminary chemical characterization of a kairomone exuded by fish. J. Chem. Ecol. 22:885–895.CrossRefGoogle Scholar
  62. Wakefield, R. L. and Murray, S. N. 1998. Factors influencing food choice by the seaweed-eating marine snail Norrisia norrisi (Trochidae). Mar. Biol. 130:631–642.CrossRefGoogle Scholar
  63. Watson, S. B. 2003. Cyanobacterial and eukaryotic algal odour compounds: signals or by-products? A review of their biological activity. Phycologia 42:332–350.CrossRefGoogle Scholar
  64. Watson, S. B. and Ridal, J. 2004. Periphyton: a primary source of widespread and severe taste and odour. Water Sci. Technol. 49:33–39.PubMedGoogle Scholar
  65. Wedemeyer, H. and Schild, D. 1995. Chemosensitivity of the osphradium of the pond snail Lymnaea stagnalis. J. Exp. Biol. 198:1743–1754.PubMedGoogle Scholar
  66. Wendel, T. and Jüttner, F. 1996. Lipoxygenase-mediated formation of hydrocarbons and unsaturated aldehydes in freshwater diatoms. Phytochemistry 41:1445–1449.CrossRefGoogle Scholar
  67. Wisenden, B. D. 2000. Olfactory assessment of predation risk in the aquatic environment. Philos. Trans. R. Soc. Lond. B 355:1205–1208.CrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2006

Authors and Affiliations

  • Patrick Fink
    • 1
    Email author
  • Eric von Elert
    • 1
  • Friedrich Jüttner
    • 2
  1. 1.Limnological InstituteUniversity of KonstanzKonstanzGermany
  2. 2.Institute of Plant BiologyLimnological StationKilchbergSwitzerland

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