Skip to main content

Advertisement

SpringerLink
Log in

Microcystins derived from lysing Microcystis cells do not cause negative effects on crustacean zooplankton in Lake Taihu, China

  • Published:
Aquatic Ecology Aims and scope Submit manuscript

Abstract

Microcystins (MCs) have a toxic effect on crustacean zooplankton in the laboratory, but there is little or no unequivocal evidence in the literature of their lethal effects on crustacean zooplankton in the field. We used the natural microcystins extracted from Microcystis spp. to test if they could cause any negative effects on crustacean zooplankton. We conducted three experiments in enclosures with water from Lake Taihu, China, and microcystins derived by extraction from Microcystis spp. collected from the lake when the species was in bloom conditions. Initial concentrations of extracellular microcystins (EMCs = MC-RR + MC-LR + MC-YR) ranged from 9.7 to 44.9 μg/L in treatments with microcystin addition. Microcystin concentrations sharply decreased on second day in all the three experiments. EMCs at the end of the experiments varied from only 2.7 to 14.2 % of the levels at the start of the experiments. The dominant species of crustacean zooplankton in the lake were Bosmina longirotris, Ceriodaphnia cornuta, Mesocyclops spp., Limnoithona sinensis, Sinocalanus dorrii and Schmackeria inopinus. ANOVA analysis showed that the density and biomass of cladoceran and copepod did not significantly differ between treatments with microcystin addition and controls. Our results indicate that microcystins derived from lysing Microcystis do not cause any negative effects on crustacean zooplankton.

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

Similar content being viewed by others

References

  • Alava-Martinez AF, Sarma SSS, Nandini S (2007) Effect of mixed diets (cyanobacteria and green algae) on the population growth of the cladocerans Ceriodaphnia dubia and Moina macrocopa. Aquat Ecol 41:79–585

    Google Scholar 

  • Ballot A, Pflugmacher S, Wiegand C (2003) Cyanobacterial toxins in Lake Baringo, Kenya. Limnologica 33:2–9

    Article  CAS  Google Scholar 

  • Baumann HI, Jüttner F (2008) Inter-annual stability of oligopeptide patterns of Planktothrix rubescens blooms and mass mortality of Daphnia in Lake Hallwilersee. Limnologica 38:350–359

    Article  CAS  Google Scholar 

  • Bottrell HH, Duncan A, Gliwicz ZM, Grygierek E, Herzig A, Hillbricht-Ilkowska A, Kurasawa H, Larsson P, Weglenska T (1976) A review of some problems in zooplankton production studies. Norw J Zool 24:419–456

    Google Scholar 

  • Briand JF, Robillot C, Quiblier-Lloberas C (2002) A perennial bloom of Planktothrix agardhii (Cyanobacteria) in a shallow eutrophic French lake: limnological and microcystin production studies. Arch Hydrobiol 153:605–622

    CAS  Google Scholar 

  • Carmichael WW (1992) A review: cyanobacteria secondary metabolites—the cyanotoxins. J Appl Bacteriol 72:445–459

    Article  CAS  Google Scholar 

  • Carmichael WW (1994) The toxins of cyanobacteria. Sci Am 270:64–72

    Article  Google Scholar 

  • Chen FZ, Xie P (2004) The toxicities of single-celled Microcystis aeruginosa PCC7820 and liberated M. aeruginosa to Daphnia carinata in the absence and presence of the green alga Scenedesmus obliquus. J Freshw Ecol 19:539–545

    Article  Google Scholar 

  • Chen YW, Qin BQ, Teubner K (2003) Long-term dynamics of phytoplankton assemblages: Microcystis-domination in Lake Taihu, a large shallow lake in China. J Plankton Res 25:445–453

    Article  Google Scholar 

  • Chen YM, Lee TH, Lee SJ, Huang HB, Huang R, Chou HN (2006) Comparison of protein phosphatase inhibition activities and mouse toxicities of microcystins. Toxicon 47:742–746

    Article  PubMed  CAS  Google Scholar 

  • Chiang SC, Du NS (1979) Fauna Sinica, Crustacea, freshwater Cladocera Science Press. Academia Sinica, Beijing (in Chinese)

    Google Scholar 

  • Chislock MF, Sarnelle O, Jernigan LM, Wilson AE (2013) Do high concentrations of microcystin prevent Daphnia control of phytoplankton? Water Res 47:1961–1970

    Article  PubMed  CAS  Google Scholar 

  • Dai X, Chen FZ (2012) Effect of colonial Microcystis spp. on the growth and reproduction of large-sized cladoceran Daphnia similis in Lake Taihu. J Lake Sci 24:149–155 (in Chinese)

    CAS  Google Scholar 

  • Dao TS, Do-Hong LC, Wiegand C (2010) Chronic effects of cyanobacterial toxins on Daphnia magna and their offspring. Toxicon 55:1244–1254

    Article  PubMed  CAS  Google Scholar 

  • DeMott WR, Zhang QX, Carmichael WW (1991) Effects of toxic cyanobacteria and purified toxins on the survival and feeding of a copepod and three species of Daphnia. Limnol Oceanogr 36:1346–1357

    Article  CAS  Google Scholar 

  • Ebina J, Tsutsui T, Shirai T (1983) Simultaneous determination of total nitrogen and total phosphorus in water using peroxodisulfate oxidation. Water Res 17:1721–1726

    Article  CAS  Google Scholar 

  • Ernst B, Hitzfeld B, Dietrich D (2001) Presence of Planktothrix sp. and cyanobacterial toxins in Lake Ammersee, Germany and their impact on whitefish (Coregonus lavaretus L.). Environ Toxicol 16:483–488

    Article  PubMed  CAS  Google Scholar 

  • Ferrão-Filho AS, Azevedo SMFO (2003) Effects of unicellular and colonial forms of toxic Microcystis aeruginosa from laboratory cultures and natural populations on tropical cladocerans. Aquat Ecol 37:23–35

    Article  Google Scholar 

  • Ferrão-Filho AS, Kozlowsky-Suzuki B (2011) Cyanotoxins: bioaccumulation and effects on aquatic animals. Mar Drugs 9:2729–2772

    Article  Google Scholar 

  • Ferrão-Filho AS, Azevedo SMFO, DeMott WR (2000) Effects of toxic and non-toxic cyanobacteria on the life-history of tropical and temperate cladocerans. Freshw Biol 45:1–19

    Article  Google Scholar 

  • Ferrão-Filho AS, Kozlowsky-Suzuki B, Azevedo SMFO (2002) Accumulation of microcystins by a tropical zooplankton community. Aquat Toxicol 59:201–208

    Article  Google Scholar 

  • Fromme H, Kohler A, Krause R (2000) Occurrence of cyanobacterial toxins: microcystins and anatoxin-a in Berlin water bodies with implications to human health and regulations. Environ Toxicol 15:120–130

    Article  CAS  Google Scholar 

  • Gao ZM, Zhao ZH, Zhang B, Zhang L (2011) Seasonal variation of microcystins concentration and influencing factors in M eiliang Bay, Lake Taihu. Ecol Environ Sci 20:1063–1067

    Google Scholar 

  • Ger KA, Teh SJ, Goldman CR (2009) Microcystin-LR toxicity on dominant copepods Eurytemora affinis and Pseudodiaptomus forbesi of the upper San Francisco Estuary. Sci Total Environ 407:4852–4857

    Article  PubMed  CAS  Google Scholar 

  • Ger KA, Teh SJ, Baxa DV (2010) The effects of dietary Microcystis aeruginosa and microcystin on the copepods of the upper San Francisco Estuary. Freshw Biol 55:1548–1559

    Article  Google Scholar 

  • Ghadouani A, Pinel-Alloul B, Plath K (2004) Effects of Microcystis aeruginosa and purified microcystin-LR on the feeding behavior of Daphnia pulicaria. Limnol Oceanogr 49:666–679

    Article  Google Scholar 

  • Haney JF (1987) Field studies on zooplankton-cyanobacteria interactions. NZ J Mar Freshw Res 21:467–475

    Article  Google Scholar 

  • Hirooka EY, Pinotti MHP, Tsutsumi T (1999) Survey of microcystins in water between 1995 and 1996 in Parana, Brazil using ELISA. Nat Tox 7:103–109

    Article  CAS  Google Scholar 

  • Ho L, Meyn T, Keegan A (2006) Bacterial degradation of microcystin toxins within a biologically active sand filter. Water Res 40:768–774

    Article  PubMed  CAS  Google Scholar 

  • Huang XF (1999) Survey observation and analysis of lake ecology. Chinese Standards Press, Beijing

    Google Scholar 

  • Jin XC, Tu QY (1990) The standard methods for observation and analysis in lake eutrophication. Chinese Environmental Science Press, Beijing, pp 138–272 (in Chinese)

    Google Scholar 

  • Jungmann D (1992) Toxic compounds isolated from Microcystis PCC7806 that are more active against Daphnia than two microcystins. Limnol Oceanogr 37:1777–1783

    Article  CAS  Google Scholar 

  • Landsberg JH (2002) The effects of harmful algal blooms on aquatic organisms. Rev Fish Sci 10:113–390

    Article  Google Scholar 

  • Lürling M (2003) Daphnia growth on microcystin-producing and microcystin-free Microcystis aeruginosa in different mixture with the green alga Scenedesmus obliquus. Limnol Oceanogr 48:2214–2220

    Article  Google Scholar 

  • Lürling M, Faassen EJ, Van Eenennaam JS (2011) Effects of the cyanobacterial neurotoxin β-N-methylamino-l-alanine (BMAA) on the survival, mobility and reproduction of Daphnia magna. J Plankton Res 33:333–342

    Article  Google Scholar 

  • McMahon JW (1965) Some physical factors influencing the feeding behavior of Daphnia magna Straus. Can J Zoo 43:603–611

    Article  Google Scholar 

  • Oberhaus L, Gélinas M, Pinel-Alloul B, Ghadouani A, Humbert JF (2007) Grazing of two toxic Planktothrixi species by Daphnia pulicaria: potential for bloom control and transfer of microcystins. J Plankton Res 29:827–838

    Article  CAS  Google Scholar 

  • Oudra B, Loudiki M, Sbiyyaa B (2001) Isolation, characterization and quantification of microcystins (heptapeptides hepatotoxins) in Microcystis aeruginosa dominated bloom of Lalla Takerkoust lake-reservoir (Morocco). Toxicon 39:1375–1381

    Article  PubMed  CAS  Google Scholar 

  • Paerl HW, Huisman J (2008) Blooms like it hot. Science 320:57–58

    Article  PubMed  CAS  Google Scholar 

  • Park HD, Lwami C, Watanabe MF (1998) Temporal variabilities of the concentrations of intra- and extracellular microcystin and toxic microcystis species in a hypertrophic lake, Lake Suwa, Japan (1991–1994). Environ Tox Water Qual 13:61–72

    Article  CAS  Google Scholar 

  • Reinikainen M, Meriluoto JAO, Spoof L (2001) The toxicities of a polyunsaturated fatty acid and a microcystin to Daphnia magna. Environ Tox 16:444–448

    Article  CAS  Google Scholar 

  • Rohrlack T, Christoffersen K, Dittmann E, Nogueira I, Vasconcelos V, Borner T (2005) Ingestion of microcystins by Daphnia: intestinal uptake and toxic effects. Limnol Oceanogr 50:440–448

    Article  CAS  Google Scholar 

  • Seekhao I, Peerapornpisal Y, Chantara S (2007) Intra- and extracellular microcystins concentrations in Mae Kuang Udomtara Reservoir, Chiang Mai, Thailand in 2004–2005. J Sci Fac Chiang Mai Uni 34:309–318

    CAS  Google Scholar 

  • Sheng JR (1979) Fauna Sinica, Crustacea, freshwater Copepoda Science Press. Academia Sinica, Beijing (in Chinese)

    Google Scholar 

  • Song LR, Chen W, Peng L (2007) Distribution and bioaccumulation of microcystins in water column: a systematic investigation into the environmental fate and the risk associated with microcystins in Meiliang Bay, Lake Taihu. Water Res 41:2853–2864

    Article  PubMed  CAS  Google Scholar 

  • Stangenberg M (1968) Toxic effects of Microcystis aeruginosa Kg. extracts on Daphnia longispina O.F. Müller and Eucypris virens Jurine. Hydrobiologia 32:81–87

    Article  Google Scholar 

  • Wörmer L, Huerta-Fontela M, Cirés S (2010) Natural photodegradation of the cyanobacterial toxins microcystin and cylindrospermopsin. Environ Sci Technol 44:3002–3007

    Article  PubMed  Google Scholar 

  • Zheng L, Xie P, Li YL (2004) Variation of intracellular and extracellular microcystins in a shallow, hypereutrophic subtropical Chinese lake with dense cyanobacterial blooms. B Environ Contam Tox 73:698–706

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Xubo Liu, Sipeng Yao, Ke Li and Deyong Zhou for their help in the field experiments. This study was supported by the National Natural Science Foundation of China (No. 31170440 and 41271523).

Author information

Authors and Affiliations

  1. State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing, 210008, China

    Feizhou Chen, Xi Dai, Tingting Shu & Zhengwen Liu

  2. Netherlands Institute of Ecology, Droevendaalsesteeg 10, 6708 PB, Wageningen, The Netherlands

    Ramesh D. Gulati

Authors
  1. Feizhou Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xi Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tingting Shu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ramesh D. Gulati
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhengwen Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Feizhou Chen.

Additional information

Handling Editor: Bas W. Ibelings.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chen, F., Dai, X., Shu, T. et al. Microcystins derived from lysing Microcystis cells do not cause negative effects on crustacean zooplankton in Lake Taihu, China. Aquat Ecol 47, 379–387 (2013). https://doi.org/10.1007/s10452-013-9451-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10452-013-9451-2

Keywords

Search

Navigation