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

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Abstract

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.

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References

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Blackburn, N., Fenchel, T., and Mitchell, J. 1998. Microscale nutrient patches in planktonic habitats shown by chemotactic bacteria. Science 282:2254–2256.

    Article  PubMed  CAS  Google Scholar 

  • Brendelberger, H. 1995. Dietary preference of three freshwater gastropods for eight natural foods of different energetic content. Malacologia 36:147–153.

    Google Scholar 

  • Brendelberger, H. 1997. Determination of digestive enzyme kinetics: a new method to define trophic niches in freshwater snails. Oecologia 109:34–40.

    Article  Google Scholar 

  • 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 

  • Calow, P. and Calow, L. J. 1975. Cellulase activity and niche separation in freshwater gastropods. Nature 255:478–480.

    Article  PubMed  CAS  Google Scholar 

  • Cattaneo, A. 1990. The effect of fetch on periphyton spatial variation. Hydrobiologia 206:1–10.

    Article  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Croll, R. P. 1983. Gastropod chemoreception. Biol. Rev. 58:293–319.

    Article  Google Scholar 

  • Croll, R. P. and Chase, R. 1980. Plasticity of olfactory orientation to foods in the snail Achatina fulica. J. Comp. Physiol. 136:267–277.

    Article  Google Scholar 

  • Denny, M. 1980. Locomotion: The cost of gastropod crawling. Science 208:1288–1290.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Evans, W. G. 1982. Oscillatoria sp. (Cyanophyta) mat metabolites implicated in habitat selection in Bembidion obtusidens (Coleoptera: Carabidae). J. Chem. Ecol. 8:671–678.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Gardner, H. W. 1991. Recent investigations into the lipoxygenase pathway of plants. Biochim. Biophys. Acta 1084:221–239.

    PubMed  CAS  Google Scholar 

  • Guillard, R. R. L. and Lorenzen, C. J. 1972. Yellow-green algae with chlorophyllide c. J. Phycol. 8:10–14.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Harborne, J. B. 1995. Ökologische Biochemie. Eine Einführung. Spektrum Akademischer Verlag, Heidelberg.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • ITIS 2004. Integrated Taxonomic Information System. http://www.cbif.gc.ca/itis.

  • Izaguirre, G. and Taylor, W. D. 1995. Geosmin and 2-methylisoborneol production in a major aqueduct system. Water Sci. Technol. 31:41–48.

    Article  CAS  Google Scholar 

  • 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 

  • Jüttner, F. 1987. Volatile organic substances, pp. 453–469, in P. Fay C. and Van Baalen (eds.). The Cyanobacteria. Elsevier, Amsterdam.

    Google Scholar 

  • Jüttner, F. 1988a. Biochemistry of biogenic off-flavour compounds in surface waters. Water Sci. Technol. 20:107–116.

    Google Scholar 

  • Jüttner, F. 1988b. Quantitative trace analysis of volatile organic compounds. Methods Enzymol. 167:609–616.

    Article  Google Scholar 

  • Jüttner, F. 1995. Physiology and biochemistry of odorous compounds from fresh-water cyanobacteria and algae. Water Sci. Technol. 31:69–78.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Jüttner, F. 2005. Evidence that polyunsaturated aldehydes of diatoms are repellents for pelagic crustacean grazers. Aquat. Ecol. 39:271–282.

    Article  CAS  Google Scholar 

  • Jüttner, F. and Dürst, U. 1997. High lipoxygenase activities in epilithic biofilms of diatoms. Arch. Hydrobiol. 138:451–463.

    Google Scholar 

  • 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 

  • Kessler, A. and Baldwin, I. T. 2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Lodge, D. M. 1986. Selective grazing on periphyton: a determinant of freshwater gastropod microdistributions. Freshw. Biol. 16:831–841.

    Article  Google Scholar 

  • Madsen, H. 1992. Food selection by freshwater snails in the gezira irrigation canals sudan. Hydrobiologia 228:203–217.

    Google Scholar 

  • Metcalf, R. L. 1987. Plant volatiles as insect attractants. CRC Crit. Rev. Plant Sci. 5:251–301.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Müller, D. G., Jaenicke, L., Donike, M., and Akintobi, T. 1971. Sex attractant in a brown alga—chemical structure. Science 171:815.

    Article  PubMed  Google Scholar 

  • Pinckney, J. L. and Zingmark, R. G. 1993. Modeling the annual production of intertidal benthic microalgae in estuarine ecosystems. J. Phycol. 29:396–407.

    Article  Google Scholar 

  • Pohnert, G. 2000. Wound-activated chemical defense in unicellular planktonic algae. Angew. Chem. Int. Ed. 39:4352–4354.

    Article  CAS  Google Scholar 

  • Pohnert, G. 2002. Phospholipase A2 activity triggers the wound-activated chemical defense in the diatom Thalassiosira rotula. Plant Physiol. 129:103–111.

    Article  PubMed  CAS  Google Scholar 

  • Pohnert, G. and Boland, W. 1996. Biosynthesis of the algal pheromone hormosirene by the freshwater diatom Gomphonema parvulum (Bacillariophyceae). Tetrahedron 52:10073–10082.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Reisser, W. 1993. Viruses and virus-like particles of fresh-water and marine eukaryotic algae—a review. Arch. Protistenkd. 143:257–265.

    Google Scholar 

  • Ruther, J., Meiners, T., and Steidle, J. L. M. 2002. Rich in phenomena—lacking in terms. A classification of kairomones. Chemoecology 12:161–167.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Stevenson, R. J., Bothwell, M. L., and Lowe, R. L. 1996. Algal Ecology: Freshwater Benthic Ecosystems. Academic Press, San Diego.

    Google Scholar 

  • 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 

  • Teyke, T. 1995. Food attraction conditioning in the snail Helix pomatia. J. Comp. Physiol. A. 177:409–414.

    Article  Google Scholar 

  • Thomas, J. D. 1986. The chemical ecology of Biomphalaria glabrata (Say): Sugars as attractants and arrestants. Comp. Biochem. Physiol. A 83:457–460.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Watson, S. B. 2003. Cyanobacterial and eukaryotic algal odour compounds: signals or by-products? A review of their biological activity. Phycologia 42:332–350.

    Article  Google Scholar 

  • Watson, S. B. and Ridal, J. 2004. Periphyton: a primary source of widespread and severe taste and odour. Water Sci. Technol. 49:33–39.

    PubMed  CAS  Google Scholar 

  • Wedemeyer, H. and Schild, D. 1995. Chemosensitivity of the osphradium of the pond snail Lymnaea stagnalis. J. Exp. Biol. 198:1743–1754.

    PubMed  Google Scholar 

  • Wendel, T. and Jüttner, F. 1996. Lipoxygenase-mediated formation of hydrocarbons and unsaturated aldehydes in freshwater diatoms. Phytochemistry 41:1445–1449.

    Article  CAS  Google Scholar 

  • Wisenden, B. D. 2000. Olfactory assessment of predation risk in the aquatic environment. Philos. Trans. R. Soc. Lond. B 355:1205–1208.

    Article  CAS  Google Scholar 

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Acknowledgments

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.”

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  1. Patrick Fink

    Present address: Max-Planck-Institute for Limnology, Department for Physiological Ecology, August-Thienemann-Str. 2, D-24306, Plön, Germany

  2. Eric von Elert

    Present address: Zoological Institute, University of Cologne, Weyertal 119, D-50923, Cologne, Germany

Authors and Affiliations

  1. Limnological Institute, University of Konstanz, D-78457, Konstanz, Germany

    Patrick Fink & Eric von Elert

  2. Institute of Plant Biology, Limnological Station, Seestr. 187, CH-8802, Kilchberg, Switzerland

    Friedrich Jüttner

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Fink, P., von Elert, E. & Jüttner, F. Volatile Foraging Kairomones in the Littoral Zone: Attraction of an Herbivorous Freshwater Gastropod to Algal Odors. J Chem Ecol 32, 1867–1881 (2006). https://doi.org/10.1007/s10886-006-9115-y

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