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Grazing impact on the cyanobacterium Microcystis aeruginosa by the heterotrophic flagellate Collodictyon triciliatum in an experimental pond

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Abstract

We estimated the grazing impact of the heterotrophic flagellate Collodictyon triciliatum on the harmful, bloom-forming cyanobacterium Microcystis aeruginosa in an experimental pond during a Microcystis bloom from summer to winter in 2010. For these experiments, we calculated the grazing rates from the digestion rate of C. triciliatum and its food vacuole contents. During the study period, M. aeruginosa exhibited one bloom event with a maximum density of 1.1 × 105 cells ml−1. The cell density of C. triciliatum fluctuated from below the detection limit to 291 cells ml−1. The number of M. aeruginosa cells ingested by C. triciliatum food vacuoles ranged between 0.4 and 10.8 cells flagellate−1, and the digestion rate of C. triciliatum at 25 °C was 0.73 % cell contents min−1. The grazing rate of C. triciliatum on the M. aeruginosa prey was 0.2–6.9 cells flagellate−1 h−1, and its grazing impact was 0.0–25.3 % standing stock day−1. The functional response of C. triciliatum to the M. aeruginosa prey followed the Michaelis–Menten model of significance (r 2 = 0.873, p < 0.001) in our experimental systems, in which the prey concentration varied from 1.0 × 104 to 2.1 × 106 cells ml−1. The maximum grazing rate was 6.2 prey cells grazer−1 h−1, and the half-saturation constant was 1.2 × 105 cells ml−1. We present evidence that C. triciliatum grazing explained the remarkable decrease in M. aeruginosa cell density in the pond. The present study is the first demonstration of the high potential of protistan grazing on M. aeruginosa to reduce cyanobacterial blooms.

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References

  • Baek SH, Hong SS, Song SY, Lee HO, Nakano S, Han MS (2009) Grazing effects on toxic and non-toxic Microcystis aeruginosa by the mixotrophic flagellate Ochromonas sp. J Freshw Ecol 24:367–373

    Article  Google Scholar 

  • Burkert U, Hyenstrand P, Drakare S, Blomqvist P (2001) Effects of the mixotrophic flagellate Ochromonas sp. on colony formation in Microcystis aeruginosa. Aquat Ecol 35:9–17

    Article  Google Scholar 

  • Carmichael WW (1992) Cyanobacterial secondary metabolites—the cyanotoxins. J Appl Microbiol 72:445–459

    Google Scholar 

  • Cole GT, Wynne MJ (1974) Endocytosis of Microcystis aeruginosa by Ochromonas danica. J Phycol 10:397–410

    Google Scholar 

  • Dokulil MT, Teubner K (2000) Cyanobacterial dominance in lakes. Hydrobiologia 438:1–12

    Article  CAS  Google Scholar 

  • Dolan JR, Šimek K (1998) Ingestion and digestion of an autotrophic picoplankter, Synechococcus, by a heterotrophic nanoflagellate, Bodo saltans. Limnol Oceanogr 43:1740–1746

    Article  Google Scholar 

  • Fulton RS, Pearl HW (1987) Toxic and inhibitory effects of the blue-green alga Microcystis aeruginosa on herbivorous zooplankton. J Plankton Res 9:837–855

    Article  Google Scholar 

  • Gobler CJ, Davis TW, Coyne KJ, Boyer GL (2007) Interactive influences of nutrient loading, zooplankton grazing, and microcystin synthetase gene expression on cyanobacterial bloom dynamics in a eutrophic New York lake. Harmful Algae 6:119–133

    Article  CAS  Google Scholar 

  • Guo S, Gan N, Zheng L, Song L (2008) Effect of Microcystis aeruginosa (Cyanobacteria) abundance on the growth and ingestion of Poterioochromonas sp. (Chrysophyceae). In: Proc 2nd Int Conf on Bioinformatics and Biomedical Engineering (ICBBE 2008), Beijing, China, 16–18 May 2008, pp 3639–3695

  • Hanazato Y, Yasuno M (1984) Growth, reproduction and assimilation of Moina macropoda fed on Microcystis and/or Chlorella. Jpn J Ecol (Otsu) 34:195–202

    Google Scholar 

  • Heinbokel JF (1978) Studies on the functional role of tintinnids in the Southern California Bight. II. Grazing rates of field populations. Mar Biol 47:191–197

    Google Scholar 

  • Hodoki Y, Ohbayashi K, Kobayashi Y, Okuda N, Nakano S (2011) Temporal variation in cyanobacteria species composition and photosynthetic activity in experimentally induced blooms. J Plankton Res 33:1410–1416

    Article  CAS  Google Scholar 

  • Imai H, Chang KH, Kusaba M, Nakano S (2009) Temperature-dependent dominance of Microcystis (Cyanophyceae) species: M. aeruginosa and M. wesenbergii. J Plankton Res 31:171–178

    Article  Google Scholar 

  • Ishikawa K, Walker RF, Tsujimura S, Nakahara H, Kumagai M (2004) Estimation of Microcystis colony size in developing water blooms via image analysis. J Jpn Soc Water Environ 27:69–72 (in Japanese with English abstract)

    Article  CAS  Google Scholar 

  • Jarvis AC, Hart RC, Combrink S (1987) Zooplankton feeding on size fractionated Microcystis colonies and Chlorella in a hypertrophic lake (Hartbeespoort Dam, South Africa): implications to resource utilization and zooplankton succession. J Plankton Res 9:1231–1249

    Article  Google Scholar 

  • Jeong HJ, Park JY, Nho JH, Park MO, Ha JH, Seong KA, Jeng C, Seong CN, Lee KY, Yih WH (2005) Feeding by red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquat Microb Ecol 41:131–143

    Article  Google Scholar 

  • Kim BR, Nakano S, Kim BH, Han MS (2006) Grazing and growth of the heterotrophic flagellate Diphylleia rotans on the cyanobacterium Microcystis aeruginosa. Aquat Microb Ecol 45:163–170

    Article  Google Scholar 

  • Latour D, Sabido O, Salencon MJ, Giraudet H (2004) Dynamics and metabolic activity of the benthic cyanobacterium Microcystis aeruginosa in the Grangent Reservoir (France). J Plankton Res 26:719–726

    Google Scholar 

  • Manage PM, Kawabata Z, Nakano S (2000) Algicidal effect of the bacterium Alcaligenes denitrificans on Microcystis spp. Aquat Microb Ecol 22:111–117

    Article  Google Scholar 

  • Mischke U (1994) Influence of food quality and quantity on ingestion and growth rates of three omnivorous heterotrophic flagellates. Mar Microbiol Food Webs 8:125–143

    Google Scholar 

  • Miura T (1990) The effects of planktivorous fishes on the plankton community in a eutrophic lake. Hydrobiologia 200(201):567–579

    Article  Google Scholar 

  • Nishibe Y, Kawabata Z, Nakano S (2002) Grazing on Microcystis aeruginosa by the heterotrophic flagellate Collodictyon triciliatum in a hypertrophic pond. Aquat Microb Ecol 29:173–179

    Article  Google Scholar 

  • Nishibe Y, Manage PM, Kawabata Z, Nakano S (2004) Trophic coupling of a testate amoeba and Microcystis species in a hypertrophic pond. Limnology 5:71–76

    Article  Google Scholar 

  • Park HD, Iwami C, Watanabe MF, Harada K, Okino T, Hayashi H (1998) Temporal variabilities of the concentration of inter- and extracellular microcystin and toxic Microcystis species in a hypertrophic lake, Lake Suwa, Japan (1991–1994). Environ Toxicol Water Qual 13:61–72

    Article  CAS  Google Scholar 

  • Reynolds CS, Walsby AE (1975) Water blooms. Biol Rev 50:437–481

    Article  CAS  Google Scholar 

  • Sherr BF, Sherr EB, Fallon RD (1987) Use of monodispersed, fluorescently labeled bacteria to estimate in situ protozoan bacterivory. Appl Environ Microbiol 53:958–965

    PubMed  CAS  Google Scholar 

  • Snell TW (1980) Blue-green algae and selection in rotifer populations. Oecologia 46:343–346

    Google Scholar 

  • Sugiura N, Inamori Y, Ouchiyama T, Sudo R (1992) Degradation of cyanobacteria, Microcystis by microflagellate, Monas guttula. Water Sci Technol 26:2173–2176

    Google Scholar 

  • Van Donk E, Cerbin S, Wilken S, Helmsing NR, Ptacnik R, Verschoor AM (2009) The effect of a mixotrophic chrysophyte on toxic and colony-forming cyanobacteria. Freshw Biol 54:1843–1855

    Article  Google Scholar 

  • Watanabe MM, Ichimura T (1997) Fresh- and salt-water forms of Spirulina platensis in axenic cultures. Bull Jpn Soc Phycol 25 Suppl (Mem Iss Yamada):371–377

  • Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39:1985–1992

    Article  CAS  Google Scholar 

  • Wilken S, Wiezer S, Huisman J, van Donk E (2010) Microcystins do not provide anti-herbivore defense against mixotrophic flagellates. Aquat Microb Ecol 59:207–216

    Article  Google Scholar 

  • Yamamoto Y, Nakahara H (2009) Seasonal variations in the morphology of bloom-forming cyanobacteria in a eutrophic pond. Limnology 10:185–193

    Article  Google Scholar 

  • Yamamoto Y, Suzuki K (1984) Light and electron microscope observations and prey specificities of an algophorous amoeba from Japanese freshwater. J Gen Appl Microbiol 30:411–417

    Article  Google Scholar 

  • Yang Z, Kong F, Shi X, Zhang M, Xing P, Cao H (2008) Changes in the morphology and polysaccharide content of Microcystis aeruginosa (Cyanobacteria) during flagellate grazing. J Phycol 44:716–720

    Article  Google Scholar 

  • Yang Z, Kong F, Yang Z, Zhang M, Yu Y, Qian S (2009) Benefits and costs of the grazer-induced colony formation in Microcystis aeruginosa. Ann Limnol Int J Lim 45:203–208

    Article  Google Scholar 

  • Yoshida T, Takashima Y, Tomaru Y, Shirai Y, Takao Y, Hiroishi S, Nagasaki K (2006) Isolation and characterization of a cyanophage infecting the toxic Cyanobacterium Microcystis aeruginosa. Appl Environ Microb 72:1239–1247

    Article  CAS  Google Scholar 

  • Zhang X, Watanabe MM, Inouye I (1996) Light and electron microscopy of grazing by Poterioochromonas malhamensis (Chrysophyceae) on a range of phytoplankton taxa. J Phycol 32:37–46

    Article  CAS  Google Scholar 

  • Zhang X, Hu HY, Men YJ, Yang J, Christoffersen K (2009) Feeding characteristics of a golden alga (Poterioochromonas sp.) grazing on toxic cyanobacterium Microcystis aeruginosa. Water Res 43:2953–2960

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This research was supported by the Environment Research and Technology Development Fund (D-0905) of the Ministry of the Environment, Japan.

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Correspondence to Shin-ichi Nakano.

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Handling Editor: Takehito Yoshida.

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Kobayashi, Y., Hodoki, Y., Ohbayashi, K. et al. Grazing impact on the cyanobacterium Microcystis aeruginosa by the heterotrophic flagellate Collodictyon triciliatum in an experimental pond. Limnology 14, 43–49 (2013). https://doi.org/10.1007/s10201-012-0384-6

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