Skip to main content
SpringerLink
Log in

Influence of Daphnia infochemicals on functional traits of Microcystis strains (Cyanobacteria)

  • Primary research paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

We conducted a laboratory experiment to investigate the influence of Daphnia infochemicals on growth rate, microcystin production, colony formation and cell size of eight Microcystis strains isolated from two lakes. The strains were characterized genetically by their 16S-23S rDNA ITS sequence. The experiment was composed of four treatments: (1) a control using filtered WC medium, (2) addition of Scenedesmus obliquus culture medium filtrate, (3) addition of Daphnia magna culture medium filtrate and (4) addition of sodium octyl sulphate, a commercially available Daphnia infochemical. Our results showed that sympatric strains differed strongly for the measured functional traits, while no correlations between traits were found. Between-strain differences in growth rate, microcystin production, colony formation and cell size were generally larger than the differences in phenotypes observed between treatments. Despite this, several strains reacted to the infochemicals by changing functional trait values. Daphnia culture medium filtrate and, to a lesser extent, sodium octyl sulphate had a negative influence on the growth rate of half of the strains and stimulated microcystin production in one strain, but the latter effect was not Daphnia-specific as Scenedesmus culture medium filtrate had the same effect. Daphnia culture medium filtrate also induced colony formation in one strain. Our data suggest that Daphnia infochemicals generally have a weak influence on growth rate, microcystin production and colony formation of Microcystis strains as compared to the inter-strain variability, while existing inducible effects are highly strain-specific.

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

  • Bañares-España, E., V. Lopez-Rodas, C. Salgado, E. Costas & A. Flores-Moya, 2006. Inter-strain variability in the photosynthetic use of inorganic carbon, exemplified by the pH compensation point, in the cyanobacterium Microcystis aeruginosa. Aquatic Botany 85: 159–162.

    Article  CAS  Google Scholar 

  • Bañares-España, E., V. Lopez-Rodas, E. Costas, C. Salgado & A. Flores-Moya, 2007. Genetic variability associated with photosynthetic pigment concentration, and photochemical and nonphotochemical quenching, in strains of the cyanobacterium Microcystis aeruginosa. Fems Microbiology Ecology 60: 449–455.

    Article  PubMed  CAS  Google Scholar 

  • Bonnet, E. & Y. Van de Peer, 2002. Zt: a software tool for simple and partial Mantel tests. Journal of Statistical software 7: 1–12.

    Google Scholar 

  • Carrillo, E., L. M. Ferrero, C. Alonso-Andicoberry, A. Basanta, A. Martin, V. Lopez-Rodas & E. Costas, 2003. Interstrain variability in toxin production in populations of the cyanobacterium Microcystis aeruginosa from water-supply reservoirs of Andalusia and lagoons of Doñana National Park (southern Spain). Phycologia 42: 269–274.

    Google Scholar 

  • Chorus, I. & J. Bartram, 1999. WHO. Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. E and FN Spon, London, UK.

    Google Scholar 

  • Christoffersen, K., B. Riemann, A. Klysner & M. Sondergaard, 1993. Potential role of fish predation and natural populations of zooplankton in structuring a plankton community in eutrophic lake water. Limnology and Oceanography 38: 561–573.

    Google Scholar 

  • Czarnecki, O., M. Henning, I. Lippert & M. Welker, 2006. Identification of peptide metabolites of Microcystis (Cyanobacteria) that inhibit trypsin-like activity in planktonic herbivorous Daphnia (Cladocera). Environmental Microbiology 8: 77–87.

    Article  PubMed  CAS  Google Scholar 

  • Ghadouani, A., B. Pinel-Alloul & E. E. Prepas, 2003. Effects of experimentally induced cyanobacterial blooms on crustacean zooplankton communities. Freshwater Biology 48: 363–381.

    Article  Google Scholar 

  • Guillard, R. R. & C. J. Lorenzen, 1972. Yellow-green algae with chlorophyllide c. Journal of Phycology 8: 10–14.

    CAS  Google Scholar 

  • Ha, K., M. H. Jang & N. Takamura, 2004. Colony formation in planktonic algae induced by zooplankton culture media filtrate. Journal of Freshwater Ecology 19: 9–16.

    Google Scholar 

  • Hansson, L. A., 1996. Behavioural response in plants: adjustment in algal recruitment induced by herbivores. Proceedings of the Royal Society of London Series B-Biological Sciences 263: 1241–1244.

    Article  Google Scholar 

  • Hansson, L. A., 2000. Synergistic effects of food chain dynamics and induced behavioral responses in aquatic ecosystems. Ecology 81: 842–851.

    Article  Google Scholar 

  • Hessen, D. O. & E. van Donk, 1993. Morphological changes in Scenedesmus induced by substances released from Daphnia. Archiv Fur Hydrobiologie 127: 129–140.

    Google Scholar 

  • Hisbergues, M., G. Christiansen, L. Rouhiainen, K. Sivonen & T. Borner, 2003. PCR-based identification of microcystin-producing genotypes of different cyanobacterial genera. Archives of Microbiology 180: 402–410.

    Article  PubMed  CAS  Google Scholar 

  • Huisman, J., H. C. P. Matthijs & P. M. Visser, 2005. Harmful Cyanobacteria. Springer, Dordrecht, The Netherlands: 243 pp.

    Book  Google Scholar 

  • Jang, M. H., K. Ha, G. J. Joo & N. Takamura, 2003. Toxin production of cyanobacteria is increased by exposure to zooplankton. Freshwater Biology 48: 1540–1550.

    Article  Google Scholar 

  • Jang, M. H., J. M. Jung & N. Takamura, 2007. Changes in microcystin production in cyanobacteria exposed to zooplankton at different population densities and infochemical concentrations. Limnology and Oceanography 52: 1454–1466.

    CAS  Google Scholar 

  • Jang, M. H., K. Ha & N. Takamura, 2008. Microcystin production by Microcystis aeruginosa exposed to different stages of herbivorous zooplankton. Toxicon 51: 882–889.

    Article  PubMed  CAS  Google Scholar 

  • Janse, I., W. E. A. Kardinaal, M. Meima, J. Fastner, P. M. Visser & G. Zwart, 2004. Toxic and nontoxic Microcystis colonies in natural populations can be differentiated on the basis of rRNA gene internal transcribed spacer diversity. Applied and Environmental Microbiology 70: 3979–3987.

    Article  PubMed  CAS  Google Scholar 

  • Joung, S. H., C. J. Kim, C. Y. Ahn, K. Y. Jang, S. M. Boo & H. M. Oh, 2006. Simple method for a cell count of the colonial cyanobacterium, Microcystis sp. Journal of Microbiology 44: 562–565.

    Google Scholar 

  • Kardinaal, W. E. A., I. Janse, M. Kamst-Van Agterveld, M. Meima, J. Snoek, L. R. Mur, J. Huisman, G. Zwart & P. M. Visser, 2007. Microcystis genotype succession in relation to microcystin concentrations in freshwater lakes. Aquatic Microbial Ecology 48: 1–12.

    Article  Google Scholar 

  • Lukač, M. & R. Aegerter, 1993. Influence of trace-metals on growth and toxin production of Microcystis aeruginosa. Toxicon 31: 293–305.

    Article  PubMed  Google Scholar 

  • Luo, W., S. Pflugmacher, T. Proschold, N. Walz & L. Krienitz, 2006. Genotype versus phenotype variability in Chlorella and Micractinium (Chlorophyta, Trebouxiophyceae). Protist 157: 315–333.

    Article  PubMed  CAS  Google Scholar 

  • Lürling, M., 1999. Grazer-induced coenobial formation in clonal cultures of Scenendesmus obliquus (Chlorococcales, Chlorophyceae). Journal of Phycology 35: 19–23.

    Article  Google Scholar 

  • Lürling, M. & E. van Donk, 1997. Morphological changes in Scenedesmus induced by infochemicals released in situ from zooplankton grazers. Limnology and Oceanography 42: 783–788.

    Google Scholar 

  • Lürling, M. & E. van Donk, 1999. Grazer-induced colony formation in Scenedesmus acutus (Chlorophyceae): ecomorph expression at different temperatures. Journal of Phycology 35: 1120–1126.

    Article  Google Scholar 

  • Lürling, M., H. J. De Lange & E. van Donk, 1997. Changes in food quality of the green alga Scenedesmus induced by Daphnia infochemicals: biochemical composition and morphology. Freshwater Biology 38: 619–628.

    Article  Google Scholar 

  • Menden-Deuer, S. & E. J. Lessard, 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnology and Oceanography 45: 569–579.

    Article  CAS  Google Scholar 

  • Otsuka, S., S. Suda, S. Shibata, H. Oyaizu, S. Matsumoto & M. M. Watanabe, 2001. A proposal for the unification of five species of the cyanobacterial genus Microcystis Kutzing ex Lemmermann 1907 under the rules of the Bacteriological Code. International Journal of Systematic and Evolutionary Microbiology 51: 873–879.

    PubMed  CAS  Google Scholar 

  • Rohrlack, T., K. Christoffersen, M. Kaebernick & B. A. Neilan, 2004. Cyanobacterial protease inhibitor microviridin J causes a lethal molting disruption in Daphnia pulicaria. Applied and Environmental Microbiology 70: 5047–5050.

    Article  PubMed  CAS  Google Scholar 

  • Sarnelle, O., 2007. Initial conditions mediate the interaction between Daphnia and bloom-forming cyanobacteria. Limnology and Oceanography 52: 2120–2127.

    CAS  Google Scholar 

  • Selinummi, J., J. Seppala, O. Yli-Harja & J. A. Puhakka, 2005. Software for quantification of labeled bacteria from digital microscope images by automated image analysis. Biotechniques 39: 859–863.

    Article  PubMed  CAS  Google Scholar 

  • Sivonen, K. & G. Jones, 1999. Cyanobacterial toxins. In Chorus, I. & J. Bartram (eds), Toxic Cyanobacteria in Water—A Guide To Their Public Health Consequences Monitoring And Management. E and FN Spon, London, England: pp. 41–111.

    Google Scholar 

  • Vaitomaa, J., A. Rantala, K. Halinen, L. Rouhiainen, P. Tallberg, L. Mokelke & K. Sivonen, 2003. Quantitative real-time PCR for determination of microcystin synthetase E copy numbers for Microcystis and Anabaena in lakes. Applied and Environmental Microbiology 69: 7289–7297.

    Article  PubMed  CAS  Google Scholar 

  • van der Oost, R., 2007. Cyanotoxine monitoring: standaardisering en validatie van methoden voor de Nederlandse Waterkwaliteitsbeheerders. Rapport STOWA onderzoek 2005 and 2006. Waternet/Waterproef, Amsterdam.

    Google Scholar 

  • van Donk, E., 2007. Chemical information transfer in freshwater plankton. Ecological Informatics 2: 112–120.

    Article  Google Scholar 

  • van Donk, E., M. Lürling & W. Lampert, 1999. Consumer-induced changes in phytoplankton: inducibility, costs, benefits, and the impact on grazers. In Tollrian, R. & C. D. Harvell (eds), The Ecology and Evolution of Inducible Defenses. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • van Gremberghe, I., P. Vanormelingen, B. Vanelslander, K. Van der Gucht, S. D’hondt, L. De Meester & W. Vyverman, 2009. Genotype-dependent interactions among sympatric Microcystis strains mediated by Daphnia grazing. Oikos. doi: 10.1111/j.1600-0706.2009.17538.x.

  • Verschoor, A. M., I. Van Der Stap, N. R. Helmsing, M. Lürling & E. van Donk, 2004. Inducible colony formation within the Scenedesmaceae: adaptive responses to infochemicals from two different herbivore taxa. Journal of Phycology 40: 808–814.

    Article  Google Scholar 

  • Visser, P. M., B. W. Ibelings, L. R. Mur & A. E. Walsby, 2005. The ecophysiology of the harmful cyanobacterium Microcystis. Features explaining its success and measures for its control. In Huisman, J., H. C. P. Matthijs & P. M. Visser (eds), Harmful Cyanobacteria. Springer, Dordrecht, The Netherlands: pp. 109–142.

    Chapter  Google Scholar 

  • Wiedner, C., P. M. Visser, J. Fastner, J. S. Metcalf, G. A. Codd & L. R. Mur, 2003. Effects of light on the microcystin content of Microcystis strain PCC 7806. Applied and Environmental Microbiology 69: 1475–1481.

    Article  PubMed  CAS  Google Scholar 

  • Wilson, A. E., O. Sarnelle, B. A. Neilan, T. P. Salmon, M. M. Gehringer & M. E. Hay, 2005. Genetic variation of the bloom-forming cyanobacterium Microcystis aeruginosa within and among lakes: implications for harmful algal blooms. Applied and Environmental Microbiology 71: 6126–6133.

    Article  PubMed  CAS  Google Scholar 

  • Wilson, A. E., W. A. Wilson & M. E. Hay, 2006. Intraspecific variation in growth and morphology of the bloom-forming cyanobacterium Microcystis aeruginosa. Applied and Environmental Microbiology 72: 7386–7389.

    Article  PubMed  CAS  Google Scholar 

  • Yang, Z. & J. J. Li, 2007. Effects of Daphnia-associated infochemicals on the morphology and growth of Scenedesmus obliquus and Microcystis aeruginosa. Journal of Freshwater Ecology 22: 249–253.

    Google Scholar 

  • Yang, Z., F. X. Kong, X. L. Shi & H. S. Cao, 2006a. Differences in response to rotifer Brachionus urceus culture media filtrate between Scenedesmus obliquus and Microcystis aeruginosa. Journal of Freshwater Ecology 21: 209–214.

    Google Scholar 

  • Yang, Z., F. X. Kong, X. L. Shi & H. S. Cao, 2006b. Morphological response of Microcystis aeruginosa to grazing by different sorts of zooplankton. Hydrobiologia 563: 225–230.

    Article  Google Scholar 

  • Yasumoto, K., A. Nishigami, M. Yasumoto, F. Kasai, Y. Okada, T. Kusumi & T. Ooi, 2005. Aliphatic sulfates released from Daphnia induce morphological defense of phytoplankton: isolation and synthesis of kairomones. Tetrahedron Letters 46: 4765–4767.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Jeroen Van Wichelen and Renaat Dasseville for sampling lake Leeuwenhof, Victor Chepurnov for isolating the Microcystis strains and Caroline Souffreau for helping with the sampling during the experiment. This research was financially supported by ESF EURODIVERSITY project BIOPOOL (nationally supported by BELSPO—Belgian Science Policy and FWO—Fonds Wetenschappelijk Onderzoek Vlaanderen) and Belgian project B-BLOOMS2 (nationally supported by BELSPO).

Author information

Authors and Affiliations

  1. Laboratory of Protistology and Aquatic Ecology, Ghent University, Krijgslaan 281-S8, 9000, Ghent, Belgium

    Ineke van Gremberghe, Pieter Vanormelingen, Katleen Van der Gucht, Antoniya Mancheva, Sofie D’hondt & Wim Vyverman

  2. Laboratory of Aquatic Ecology and Evolutionary Biology, Katholieke Universiteit Leuven, Charles Debériotstraat 32, 3000, Leuven, Belgium

    Luc De Meester

Authors
  1. Ineke van Gremberghe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pieter Vanormelingen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Katleen Van der Gucht
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Antoniya Mancheva
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sofie D’hondt
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Luc De Meester
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Wim Vyverman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ineke van Gremberghe.

Additional information

Handling editor: D. P. Hamilton

Rights and permissions

Reprints and permissions

About this article

Cite this article

van Gremberghe, I., Vanormelingen, P., Van der Gucht, K. et al. Influence of Daphnia infochemicals on functional traits of Microcystis strains (Cyanobacteria). Hydrobiologia 635, 147–155 (2009). https://doi.org/10.1007/s10750-009-9907-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-009-9907-5

Keywords

Search

Navigation