Skip to main content
SpringerLink
Log in

Effects of the allelopathically active macrophyte Myriophyllum spicatum on a natural phytoplankton community: a mesocosm study

  • PLANTS IN HYDROSYSTEMS
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

We investigated the effects of Eurasian watermilfoil (Myriophyllum spicatum) on a natural phytoplankton community in 85 l mesocosms. Changes in phytoplankton community composition, biomass, primary productivity, nitrogenase activity and the abundance of toxic and non-toxic Microcystis aeruginosa subpopulations were investigated during 13 days of exposure. We aimed to test whether the known allelopathic activity of M. spicatum towards certain algae and cyanobacteria could be proven under field-like conditions with potential interference of resource competition and zooplankton grazing. The presence of M. spicatum had only short-term inhibitory patterns on total phytoplankton and green algae, whereas consistent negative effects were observed on cyanobacteria biomass. Quantitative PCR analyses revealed that toxic and non-toxic M. aeruginosa were equally inhibited. Total phytoplankton gross primary production was significantly suppressed by the presence of M. spicatum. Despite the partial interference by nutrient limitation, there are indications for a significant impact of macrophyte-excreted allelochemicals on phytoplankton. We argue that more mesocosm experiments with complex natural phytoplankton communities are needed to unravel the ecological relevance of macrophyte allelopathy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Barko, J. W. & W. F. James, 1998. Effects of Submerged Aquatic Macrophytes on Nutrient Dynamics, Sedimentation, and Resuspension. In Jeppesen, E., M. Søndergaard & K. Christoffersen (eds), The Structuring Role of Submerged Macrophytes in Lakes. Springer, New York: 197–217.

    Chapter  Google Scholar 

  • Best, M. D. & K. E. Mantai, 1978. Growth of Myriophyllum: sediment or lake water as the source of nitrogen and phosphorus. Ecology 59: 1075–1080.

    Article  CAS  Google Scholar 

  • Beutler, M., K. H. Wiltshire, B. Meyer, C. Moldaenke, C. Lüring, M. Meyerhöfer, U. P. Hansen & H. Dau, 2002. A fluorometric method for the differentiation of algal populations in vivo and in situ. Photosynthesis Research 72: 39–53.

    Article  CAS  PubMed  Google Scholar 

  • Blindow, I., A. Hargeby, M. A. Bálint, A. Wagner & G. Andersson, 2000. How important is the crustacean plankton for the maintenance of water clarity in shallow lakes with abundant submerged vegetation? Freshwater Biology 44: 185–197.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Brownlee, B. G. & T. P. Murphy, 1983. Nitrogen fixation and phosphorus turnover in a hypertrophic Prairie Lake. Canadian Journal of Fisheries and Aquatic Sciences 40: 1853–1860.

    Article  CAS  Google Scholar 

  • Burks, R. L., E. Jeppesen & D. M. Lodge, 2000. Macrophyte and fish chemicals suppress Daphnia growth and alter life-history traits. Oikos 88: 139–148.

    Article  CAS  Google Scholar 

  • Capone, D. G., 1993. Determination of Nitrogenase Activity in Aquatic Samples Using the Acetylene Reduction Procedure. In Kemp, P. F., B. F. Sherr, E. B. Sherr & J. J. Cole (eds), Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton: 621–632.

    Google Scholar 

  • Chang, X., F. Eigemann & S. Hilt, 2012. Do macrophytes support harmful cyanobacteria? Interactions with a green alga reverse the inhibiting effects of macrophyte allelochemicals on Microcystis aeruginosa. Harmful Algae 19: 76–84.

    Article  CAS  Google Scholar 

  • Declerck, S., M. Vanderstukken, A. Pals, K. Muylaert & L. De Meester, 2007. Plankton biodiversity along a gradient of productivity and its mediation by macrophytes. Ecology 88: 2199–2210.

    Article  CAS  PubMed  Google Scholar 

  • Demarty, M. & Y. T. Prairie, 2009. In situ dissolved organic carbon (DOC) release by submerged macrophyte-epiphyte communities in southern Quebec lakes. Canadian Journal of Fisheries and Aquatic Sciences 66: 1522–1531.

    Article  CAS  Google Scholar 

  • Eigemann, F., S. Hilt & M. Schmitt-Jansen, 2013. Flow cytometry as a diagnostic tool for the effects of polyphenolic allelochemicals on phytoplankton. Aquatic Botany 104: 5–14.

    Article  CAS  Google Scholar 

  • Grace, J. B. & R. G. Wetzel, 1978. The production biology of Eurasian watermilfoil (Myriophyllum spicatum L.): a review. Journal of Aquatic Plant Management 16: 1–11.

    Google Scholar 

  • Grasshoff, K., 1983. Determination of Oxygen. In: Grasshoff, K., M. Ehrhardt & K. Kremling (eds), Methods of Seawater Analysis. Verlag Chemie, Weinheim: 61–72.

  • Gregg, W. W. & F. Rose, 1985. Influences of aquatic macrophytes on invertebrate community structure, guild structure, and microdistribution in streams. Hydrobiologia 128: 45–56.

    Article  Google Scholar 

  • Gross, E. M., H. Meyer & G. Schilling, 1996. Release and ecological impact of algicidal hydrolysable polyphenols in Myriophyllum spicatum. Phytochemistry 41: 133–138.

    Article  CAS  Google Scholar 

  • Häggqvist, K. & T. Lindholm, 2012. Phytoplankton dynamics in a shallow lake dominated by common water milfoil. Inland Waters 2: 137–146.

    Article  Google Scholar 

  • Hilt, S., 2006. Allelopathic inhibition of epiphytes by submerged macrophytes. Aquatic Botany 85: 252–256.

    Article  Google Scholar 

  • Hilt, S. & E. M. Gross, 2008. Can allelopathically active submerged macrophytes stabilise clear-water states in shallow lakes? Basic and Applied Ecology 9: 422–432.

    Article  Google Scholar 

  • Howard-Williams, C. & B. R. Allanson, 1981. Phosphorus cycling in a dense Potamogeton pectinatus. L. bed. Oecologia 49: 56–66.

    Article  Google Scholar 

  • Huss, A. A. & J. D. Wehr, 2004. Strong indirect effects of a submersed aquatic macrophyte, Vallisneria americana, on bacterioplankton densities in a mesotrophic lake. Microbial Ecology 45: 305–315.

    Google Scholar 

  • Ibelings, B. W. & S. C. Maberly, 1998. Photoinhibition and the availability of inorganic carbon restrict photosynthesis by surface blooms of cyanobacteria. Limnology & Oceanography 43: 408–419.

    Article  CAS  Google Scholar 

  • Jasser, I., 1995. The influence of macrophytes on a phytoplankton community in experimental conditions. Hydrobiologia 306: 21–32.

    Article  CAS  Google Scholar 

  • John, D. M., B. A. Whitton & A. J. Brook, 2002. The Freshwater Algal Flora of the British Isles. Cambridge University Press, Cambridge.

    Google Scholar 

  • Jorgensen, S. E., S. N. Nielsen & L. A. Jorgensen, 1995. Handbook of Ecological Parameters and Ecotoxicology. Elsevier, Amsterdam.

    Google Scholar 

  • Komárek, J. & K. Anagnostidis, 1999. Cyanoprokaryota: Chroococcales. In: Ettl, H., G. Gärtner, H. Heynig & D. Mollenhauer (eds), Süßwasserflora von Mitteleuropa, 19/1. Gustav Fischer, Jena-Stuttgart-Lübeck-Ulm. (In German).

  • Körner, S., 1999. Nitrifying and denitrifying bacteria in epiphytic communities of submerged macrophytes in a treated sewage channel. Acta Hydrochimica et Hydrobiologica 27: 27–31.

    Article  Google Scholar 

  • Körner, S. & A. Nicklisch, 2002. Allelopathic growth inhibition of selected phytoplankton species by submerged macrophytes. Journal of Phycology 38: 862–871.

    Article  Google Scholar 

  • Kurmayer, R. & T. Kutzenberger, 2003. Application of real-time PCR for quantification of microcystin genotypes in a population of the toxic cyanobacterium Microcystis sp. Applied and Environmental Microbiology 69: 6723–6730.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kutikova, L. A., 1970. The Rotifer Fauna of USSR. NAUKA Publishing, Leningrad. (in Russian).

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, B. Y., P. Jiang, A. E. Zhou, J. R. Tian & S. Y. Jiang, 2007. Effect of pyrogallol on the growth and pigment content of cyanobacteria-blooming toxic and nontoxic Microcystis aeruginosa. Bulletin of Environmental Contamination and Toxicology 78: 499–502.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Mulderij, G., W. M. Mooij, A. J. P. Smolders & E. Van Donk, 2005. Allelopathic inhibition of phytoplankton by exudates from Stratiotes aloides. Aquatic Botany 82: 284–296.

    Article  Google Scholar 

  • Muylaert, K., S. Declerck, J. Van Wichelen, L. De Meester & W. Vyverman, 2006. An evaluation of the role of daphnids in controlling phytoplankton biomass in clear water versus turbid shallow lakes. Limnologica 36: 69–78.

    Article  Google Scholar 

  • Nakai, S., Y. Inoue, M. Hosomi & A. Murakami, 2000. Myriophyllum spicatum-released allelopathic polyphenols inhibiting growth of blue-green algae Microcystis aeruginosa. Water Research 34: 3026–3032.

    Article  CAS  Google Scholar 

  • Nam, S., S. Joo, S. Kim, N. I. Baek, H. K. Choi & S. Park, 2008. Induced metabolite changes in Myriophyllum spicatum during co-existence experiment with the cyanobacterium Microcystis aeruginosa. Journal of Plant Biology 51: 373–378.

    Article  CAS  Google Scholar 

  • Pilkaitytė, R. & A. Razinkovas, 2007. Seasonal changes in phytoplankton composition and nutrient limitation in a shallow Baltic lagoon. Boreal Environmental Research 12: 551–559.

    Google Scholar 

  • Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar & the R Development Core Team, 2013. nlme: Linear and Nonlinear Mixed Effects Models. R Package Version 3.1-108.

  • R Core Team, 2013. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/.

  • Reynolds, C. S., R. L. Oliver & A. E. Walsby, 1987. Cyanobacterial dominance: the role of buoyancy regulation in dynamic lake environments. New Zealand Journal of Marine and Freshwater Research 21: 379–390.

    Article  Google Scholar 

  • Rybak, J. I. & L. A. Błędzki, 2010. Freshwater Planktonic Crustaceans. Guide to Species Identification. Warsaw University Press, Warsaw. (in Polish).

  • Salazkin, A. A., M. B. Ivanova & V. A. Ogorodnikova, 1984. Methodical Recommendations for Data Collecting and Analysis in Hydrobiological Studies of Fresh Waters: Productivity of Zooplankton. State Research Institute of Lake and River Fisheries, Leningrad. (in Russian).

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Scheffer, M., S. Rinaldi, A. Gragnani, L. R. Mur & E. H. van Nes, 1997. On the dominance of filamentous cyanobacteria in shallow turbid lakes. Ecology 78: 272–282.

    Article  Google Scholar 

  • Smith, V. H. & D. W. Schindler, 2009. Eutrophication science: where do we go from here? Trends in Ecology & Evolution 24: 201–207.

    Article  Google Scholar 

  • Søndergaard, M. & B. Moss, 1998. Impact of Submerged Macrophytes on Phytoplankton in Shallow Freshwater Lakes. In Jeppesen, E., Ma. Søndergaard, Mo. Søndergaard & K. Christoffersen (eds), The Structuring Role of Submerged Macrophytes in Lakes. Springer, New York: 115–132.

  • Starmach, K., 1989. The Freshwater Phytoplankton. Research Methods and Keys to Identification of Species from Central European Waters. PWN, Warszawa-Kraków. (in Polish).

  • Talling, J. I., 1976. The depletion of carbon dioxide from lake water by phytoplankton. The Journal of Ecology 64: 79–121.

    Article  CAS  Google Scholar 

  • Timms, R. M. & B. Moss, 1984. Prevention of growth of potentially dense phytoplankton populations by zooplankton grazing in the presence of zooplanktivorous fish in a shallow wetland ecosystem. Limnology & Oceanography 29: 472–486.

    Article  Google Scholar 

  • Tukey, J. W., 1962. The future of data analysis. Annals of Mathematical Statistics 33: 1–67.

    Article  Google Scholar 

  • Van den Berg, M. S., H. Coops, M. L. Meijer, M. Scheffer & J. Simons, 1998. Clear Water Associated with a Dense Chara Vegetation in the Shallow and Turbid Lake Veluwemeer, The Netherlands. In Jeppesen, E., Ma. Søndergaard, Mo. Søndergaard & K. Christoffersen (eds), The Structuring Role of Submerged Macrophytes in Lakes. Springer, New York: 339–352.

  • Vanderstukken, M., S. Declerck, A. Pals, L. De Meester & K. Muylaert, 2010. The influence of plant-associated filter feeders on phytoplankton biomass: a mesocosm study. Hydrobiologia 646: 199–208.

    Article  CAS  Google Scholar 

  • Vanderstukken, M., N. Mazzeo, W. Van Colen, S. A. J. Declerck & K. Muylaert, 2011. Biological control of phytoplankton by the subtropical submerged macrophytes Egeria densa and Potamogeton illinoensis: a mesocosm study. Freshwater Biology 56: 1837–1849.

    Article  CAS  Google Scholar 

  • Wang, J., J. Zhu, S. Liu, B. Liu, Y. Gao & Z. Wu, 2011. Generation of reactive oxygen species in cyanobacteria and green algae induced by allelochemicals of submerged macrophytes. Chemosphere 85: 977–982.

    Article  CAS  PubMed  Google Scholar 

  • Weisner, S., G. Eriksson, W. Graneli & L. Leonardson, 1994. Influence of macrophytes on nitrate removal in wetlands. Ambio 23: 363–366.

    Google Scholar 

  • Wium-Andersen, S., U. Anthoni, C. Christophersen & G. Houen, 1982. Allelopathic effects on phytoplankton by substances isolated from aquatic macrophytes (Charales). Oikos 39: 187–190.

    Article  Google Scholar 

  • Zhang, T. T., M. He, A. P. Wu & L. W. Nie, 2009. Allelopathic effects of submerged macrophyte Chara vulgaris on toxic Microcystis aeruginosa. Allelopathy Journal 23: 391–402.

    CAS  Google Scholar 

  • Zhang, M., T. Cao, L. Ni, P. Xie, G. Zhu, A. Zhong, J. Xu & H. Fu, 2011. Light-dependent phosphate uptake of a submersed macrophyte Myriophyllum spicatum L. Aquatic Botany 94: 151–157.

    Article  CAS  Google Scholar 

  • Zhou, J., M. Bruns & J. Tiedje, 1996. DNA recovery from soils of diverse composition. Applied and Environmental Microbiology 62: 316–322.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zuur, A. F., E. N. Ieno, N. J. Walker, A. A. Saveliev & G. M. Smith, 2009. Mixed-Effects Models and Extensions in Ecology with R. Springer, New York.

    Book  Google Scholar 

Download references

Acknowledgments

We thank M. Riaukaitė, D. Švanytė for their assistance, A. Razinkovas-Baziukas, S. Šulčius and J. Lesutienė for very helpful discussions, S. Mažeikaitė for zooplankton counting, J. Karosienė for phytoplankton identification, K. Pohlmann and B. Hidding for advices on statistical analyses and S. Brothers for linguistic improvements. H. P. Grossart kindly provided access to his laboratory for quantitative PCR analyses and F. Eigemann and I. Salka supported laboratory measurements. This study was partially supported by European Social Fund Agency (Project VP1-3.1-ŠMM-08-K-01-019). A. Švanys was supported by Deutsche Bundesstiftung Umwelt (No. 86011/009) and Research Council of Lithuania (Project VP1-3.1-ŠMM-01-V-02-003). We acknowledge constructive comments and suggestions from three anonymous reviewers.

Author information

Authors and Affiliations

  1. Marine Science and Technology Centre, Klaipėda University, H. Manto 84, 92294, Klaipėda, Lithuania

    Algirdas Švanys & Ričardas Paškauskas

  2. Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Müggelseedamm 301, 12587, Berlin, Germany

    Algirdas Švanys & Sabine Hilt

  3. Institute of Botany of Nature Research Centre, Žaliųjų ežerų 49, 08406, Vilnius, Lithuania

    Ričardas Paškauskas

Authors
  1. Algirdas Švanys
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ričardas Paškauskas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sabine Hilt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Algirdas Švanys.

Additional information

Guest editors: M. T. Ferreira, M. O’Hare, K. Szoszkiewicz & S. Hellsten / Plants in Hydrosystems: From Functional Ecology to Weed Research

Rights and permissions

Reprints and permissions

About this article

Cite this article

Švanys, A., Paškauskas, R. & Hilt, S. Effects of the allelopathically active macrophyte Myriophyllum spicatum on a natural phytoplankton community: a mesocosm study. Hydrobiologia 737, 57–66 (2014). https://doi.org/10.1007/s10750-013-1782-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-013-1782-4

Keywords

Search

Navigation