Abstract
Allelopathy, here defined as biochemical interactions between aquatic primary producers, has always been intriguing as a process explaining the dominance of certain plant or algal species over others. Negative chemical interference has been invoked as one of the steering mechanisms behind mutual dominance of either submerged macrophytes or phytoplankton in shallow eutrophic lakes. Yet, despite much effort, convincing evidence for allelopathic interactions in situ is still missing. Also, laboratory approaches often lack reality. Inspired by a series of talks at the Shallow Lakes 2005 meeting in Dalfsen, the Netherlands, we argue that there is circumstantial but strong evidence that allelopathic interference between submerged macrophytes and phytoplankton may indeed exist in aquatic ecosystems despite the problems associated with research in this field. We first discuss experimental approaches combining laboratory and field studies, based on examples presented at this meeting. We then discuss the impact of nutrient status of both producing and target organism and biotic factors such as herbivory or pathogens that might affect allelopathy. Further topics are the potential seasonality of effects and the species-specificity of certain allelochemicals. We conclude with some thoughts why a final proof for allelopathy in situ might remain difficult or even inaccessible in some cases, and why we nevertheless should not abandon this idea.
Similar content being viewed by others
References
Agami, M. & Y. Waisel, 1985. Inter-relationship between Najas marina L. and three other species of aquatic macrophytes. Hydrobiologia 126: 169–173.
Akehurst, S. C., 1931. Observations on pond life. Journal of the Royal Microscopic Society, London 51: 236–265.
Anthoni, U., C. Christophersen, N. Jacobsen & A. Svendsen, 1982. Synthesis of 4-methylthio-1,2-dithiolane and 5-methylthio-1,2,3-trithiane. Two naturally occurring bioactive compounds. Tetrahedron 38: 2425–2427.
Blindow, I., A. Hargeby & G. Andersson, 2002. Seasonal changes of mechanisms maintaining clear water in a shallow lake with abundant Chara vegetation. Aquatic Botany 72: 315–334.
Brönmark, C. & J. E. Vermaat, 1998. Complex fish-snail-epiphyton interactions and their effects on submerged freshwater macrophytes. In Jeppesen, E., M. Søndergaard, M. Søndergaard & K. Christoffersen (eds), The Structuring Role of Submerged Macrophytes in Lakes, Springer, New York. Ecological Studies 131: 47–68.
Bryant, J. P., F. S. Chapin III & D. R. Klein, 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40: 357–368.
Choi, C., C. Bareiss, O. Walenciak & E. M. Gross, 2002. Impact of polyphenols on the growth of the aquatic herbivore Acentria ephemerella (Lepidoptera: Pyralidae). Journal of Chemical Ecology 28: 2223–2235.
Cole, J. J., 1999. Aquatic microbiology for ecosystem scientists: new and recycled paradigms in ecological microbiology. Ecosystems 2: 215–225.
Cronin, G. & D. M. Lodge, 2003. Effect of light and nutrient availability on the growth, allocation, carbon/nitrogen balance, phenolic chemistry, and resistance to herbivory of two freshwater macrophytes. Oecologia 137: 32–41.
Elakovich, S. D. & J. W. Wooten, 1989. Allelopathic potential of 16 aquatic and wetland plants. Journal of Aquatic Plant Management 27: 78–84.
Elakovich, S. D. & J. W. Wooten, 1995. Allelopathic, herbaceous, vascular hydrophytes. In Inderjit, K. M. M. Dakshini & F. A. Einhellig (eds), Allelopathy—organisms, processes, and applications, ACS Symposium series 582. American Chemical Society, Washington, DC, pp 58–73.
Erhard, D. & E. M. Gross, 2006. Allelopathic activity of Elodea canadensis and E. nuttallii against epiphytes and phytoplankton. Aquatic Botany 85: 203–211.
Ervin, G. N. & R. G. Wetzel, 2000. Allelochemical autotoxicity in the emergent wetland macrophyte Juncus effusus (Juncaceae). American Journal of Botany 87: 853–860.
Fischer, N. H. & L. Quijano, 1985. Allelopathic agents from common weeds. In A. C. Thompson (ed.), The Chemistry of Allelopathy, ACS Symposium Series. American Chemical Society, Washington, D.C. 268: 133–147.
Fitzgerald, G. P., 1969. Some factors in the competition or antagonism among bacteria, algae and aquatic weeds. Journal of Phycology 5: 351–359.
Forsberg, C., 1965. Nutritional studies of Chara in axenic cultures. Physiologia Plantarum 18: 275–290.
Forsberg, C., S. Kleiven & T. Willen, 1990. Absence of allelopathic effects of Chara on phytoplankton in situ. Aquatic Botany 38: 289–294.
Gopal, B. & U. Goel, 1993. Competition and allelopathy in aquatic plant communities. Botanical Review 59: 155–210.
Gross, E. M., 1999. Allelopathy in benthic and littoral areas: Case studies on allelochemicals from benthic cyanobacteria and submersed macrophytes. In Inderjit, K. M. M. Dakshini & C. L. Foy (eds), Principles and practices in plant ecology: allelochemical interactions. CRC Press, LLC, Boca Raton, 179–199.
Gross, E. M., 2003a. Allelopathy of aquatic autotrophs. Critical Reviews in Plant Sciences 22: 313–339.
Gross, E. M., 2003b. Differential response of tellimagrandin II and total bioactive hydrolysable tannins in an aquatic angiosperm to changes in light and nitrogen. Oikos 103: 497–504.
Gross, E. M., D. Erhard & E. Ivanyi, 2003. Allelopathic activity of Ceratophyllum demersum L. and Najas marina ssp. intermedia. Hydrobiologia 506: 583–589.
Gross, E. M., R. L. Johnson, N. G. Hairston Jr., 2001. Experimental evidence for changes in submersed macrophyte species composition caused by the herbivore Acentria ephemerella (Lepidoptera). Oecologia 127: 105–114.
Gross, E. M., H. Meyer & G. Schilling, 1996. Release and ecological impact of algicidal hydrolyzable polyphenols in Myriophyllum spicatum. Phytochemistry 41: 133–138.
Gurevitch, J., S. M. Scheiner & G. A. Fox, 2002. The Ecology of Plants. Sinauer Associates Inc., Sunderland, MA, USA. See p. 193 for De-Wit replacement series.
Harder, R., 1917. Ernährungsphysiologische Untersuchungen an Cyanophyceen, hauptsächlich dem endophytischen Nostoc punctiforme. Zeitschrift für Botanik IX: 145–242.
Hasler, A. D. & E. Jones, 1949. Demonstration of the antagonistic action of large aquatic plants on algae and rotifers. Ecology 30: 359–364.
Hilt, S., 2006. Allelopathic inhibition of epiphytes by submerged macrophytes. Aquatic Botany 85: 252–256.
Hilt, S., M. Ghobrial & E. M. Gross, 2006. In situ allelopathic potential of Myriophyllum verticillatum (Haloragaceae) against selected phytoplankton species. Journal of Phycology: 42:1189–1198.
Inderjit & R. del Moral, 1997. Is separating resource competition from allelopathy realistic? Botanical Review 63: 221–230.
Jacobsen, N. & L. E. K. Pedersen, 1983. Synthesis and insecticidal properties of derivatives of propane-1,3-dithiol (analogs of the insecticidal derivatives of dithiolane and trithiane from the alga Chara globularis (Thuillier). Pesticide Science 14: 90–97.
Jasser, I., 1995. The influence of macrophytes on a phytoplankton community in experimental conditions. Hydrobiologia 306: 21–32.
Keating, K. I., 1977. Allelopathic influence on blue-green bloom sequence in a eutrophic lake. Science 196: 885–887.
Kogan, S. I. & G. A. Chinnova, 1972. Relations between Ceratophyllum demersum (L.) and some blue-green algae. Hydrobiological Journal (Ghidrobiol. Zh.) 8: 14–19 (21–27).
Koricheva, J., 2002. The Carbon-Nutrient Balance Hypothesis is dead: long live the Carbon-Nutrient Balance Hypothesis? Oikos 98: 537–539.
Körner, S. & A. Nicklisch, 2002. Allelopathic growth inhibition of selected phytoplankton species by submerged macrophytes. Journal of Phycology 38: 862–871.
Leu, E., A. Krieger-Liszkay, C. Goussias, E. M. Gross, 2002. Polyphenolic allelochemicals from the aquatic angiosperm Myriophyllum spicatum L. inhibit photosystem II. Plant Physiology 130: 2011–2018.
Lewis, W. M. Jr., 1986. Evolutionary interpretation of allelochemical interactions in phytoplanktonic algae. American Naturalist 127: 184–194.
Lombardo, P. & G. D. Cooke, 2001. Effects of freshwater gastropods on epiphyton, macrophytes, and water transparency under meso- to eutrophic conditions. Chapter from PhD Dissertation. Kent State University, Kent, OH, USA.
Lombardo, P. & G. D. Cooke, 2003. Ceratophyllum demersum: phosphorus interactions in nutrient enriched aquaria. Hydrobiologia 497: 79–90.
Lombardo, P., 2005. Applicability of littoral food-web biomanipulation for lake management purposes: snails: macrophytes, and water transparency in northeast Ohio shallow lakes. Lake and Reservoir Management 21: 186–202.
Lürling, M., G. van Geest & M. Scheffer, 2006. Importance of nutrient competition and allelopathic effects in suppression of the green alga Scenedesmus obliquus by the macrophytes Chara, Elodea and Myriophyllum. Hydrobiologia 556: 209–220.
McCollum, E. W., L. B. Crowder & S. A. McCollum, 1998. Complex interactions of fish, snails, and littoral zone periphyton. Ecology 79: 1980–1994.
Mjelde, M. & B. A. Faafeng, 1997. Ceratophyllum demersum hampers phytoplankton development in some small Norwegian lakes over a wide range of phosphorus concentrations and geographical latitude. Freshwater Biology 37: 355–365.
Molisch, H., 1937. Der Einfluss einer Pflanze auf die andere—Allelopathie. Fischer, Jena.
Mulderij, G., B. Mau, E. van Donk & E. M. Gross, 2007. Allelopathic activity of Stratiotes aloides on phytoplankton—towards identification of allelopathic substances. Hydrobiologia 584: 89–100.
Mulderij, G., W. M. Mooij, A. J. P. Smolders & E. van Donk, 2005a. Inhibition of phytoplankton by allelopathic substances from Stratiotes aloides. Aquatic Botany 82: 284–296.
Mulderij, G., W. M. Mooij & E. van Donk, 2005b. Allelopathic growth inhibition and colony formation of the green alga Scenedesmus obliquus by the aquatic macrophyte Stratiotes aloides. Aquatic Ecology 39: 11–21.
Mulderij, G., A. J. P. Smolders & E. van Donk, 2006. The allelopathic effect of Stratiotes aloides on phytoplankton under natural conditions. Freshwater Biology 51: 554–562.
Mulderij, G., E. van Donk & J. G. M. Roelofs, 2003. Differential sensitivity of green algae to allelopathic substances from Chara. Hydrobiologia 491: 261–271.
Nakai, S., Y. Inoue, M. Hosomi & A. Murakami, 1999. Growth inhibition of blue–green algae by allelopathic effects of macrophytes. Water Science & Technology 39: 47–53.
Pelton, D. K., S. N. Levine & M. Braner, 1998. Measurements of phosphorus uptake by macrophytes and epiphytes from the LaPlatte River (VT) using 32P in stream microcosms. Freshwater Biology 39: 285–299.
Perez, E. & D. F. Martin, 2001. Critical micelle concentrations of allelopathic substances produced by Nannochloris oculata which affect a red tide organism, Gymnodinium breve. Cytobios 106: 163–170.
Phillips, G. L., D. Eminson, & B. Moss, 1978. A mechanism to account for macrophyte decline in progressively eutrophicated freshwaters. Aquatic Botany 4: 103–126.
Pratt, R., R. C. Daniels, J. J. Eiler, J. B. Gunnison, W. D. Kumler, J. F. Oneto, L. A. Strait, H. A. Spoehr, G. J. Hardin, H. W. Milner, J. H. C. Smith & H. H. Strain, 1944. Chlorellin, an antibacterial substance from Chlorella. Science 99: 351–352.
Pringsheim, E. G. & O. Pringsheim, 1962. Axenic culture of Utricularia. American Journal of Botany 49: 898–901.
Reigosa, M. J., A. Sanchez-Moreiras & L. Gonzalez, 1999. Ecophysiological approach in allelopathy. Critical Reviews in Plant Sciences 18: 577–608.
Scheffer, M., S. H. Hosper, M. L. Meijer, B. Moss & E. Jeppesen, 1993. Alternative equilibria in shallow lakes. Trends in Ecology and Evolution 8: 275–279.
Søndergaard, M., 1981. Kinetics of extracellular release of 14C-labelled organic carbon by submersed macrophytes. Oikos 36: 331–347.
Sukenik, A., R. Eshkol, A. Livne, O. Hadas, M. Rom, D. Tchernov, A. Vardi & A. Kaplan, 2002. Inhibition of growth and photosynthesis of the dinoflagellate Peridinium gatunense by Microcystis sp. (cyanobacteria): a novel allelopathic mechanism. Limnology and Oceanography 47: 1656–1663.
Underwood, G. J. C., 1991. Growth enhancement of the macrophyte Ceratophyllum demersum in the presence of the snail Planorbis planorbis: the effect of grazing and chemical conditioning. Freshwater Biology 26: 325–334.
van, Donk E. & W. J. van de Bund, 2002. Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquatic Botany 72: 261–274.
Vance, H. D. & D. A. Francko, 1997. Allelopathic potential of Nelumbo lutea (Willd.) Pers. to alter growth of Myriophyllum spicatum L. and Potamogeton pectinatus L. Journal of Freshwater Ecology 12: 405–409.
Walenciak, O., W. Zwisler, E. M. Gross, 2002. Influence of Myriophyllum spicatum-derived tannins on gut microbiota of its herbivore Acentria ephemerella. Journal of Chemical Ecology 28: 2045–2056.
Wetzel, R. G. & D. L. McGregor, 1968. Axenic culture and nutritional studies of aquatic macrophytes. American Midland Naturalist 80: 52–64.
Wetzel R. G., 2001. Limnology—Lake and River Ecosystems, 3rd ed. Academic Press, San Diego, 1006 pp.
Willis, R. J., 1985. The historical bases of the concept of allelopathy. Journal of the History of Biology 18: 71–102.
Wooten, J. W. & S. D. Elakovich, 1991. Comparisons of potential allelopathy of seven freshwater species of spikerushes (Eleocharis). Journal of Aquatic Plant Management 29: 12–15.
Acknowledgments
We greatly appreciate helpful discussion with Marit Mjelde during the Shallow Lakes 2005 meeting. We very much acknowledge constructive comments by Miquel Lürling and an anonymous reviewer on a previous version of this manuscript. This project was in part supported by the German Science Foundation (DFG) in Project SFB454-A2 to EMG and by a grant by the Berliner Programm zur Förderung von Frauen in Forschung und Lehre to SH.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gross, E.M., Hilt (nee Körner), S., Lombardo, P. et al. Searching for allelopathic effects of submerged macrophytes on phytoplankton—state of the art and open questions. Hydrobiologia 584, 77–88 (2007). https://doi.org/10.1007/s10750-007-0591-z
Issue Date:
DOI: https://doi.org/10.1007/s10750-007-0591-z