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.
Similar content being viewed by others
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
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
Carmichael WW (1992) Cyanobacterial secondary metabolites—the cyanotoxins. J Appl Microbiol 72:445–459
Cole GT, Wynne MJ (1974) Endocytosis of Microcystis aeruginosa by Ochromonas danica. J Phycol 10:397–410
Dokulil MT, Teubner K (2000) Cyanobacterial dominance in lakes. Hydrobiologia 438:1–12
Dolan JR, Šimek K (1998) Ingestion and digestion of an autotrophic picoplankter, Synechococcus, by a heterotrophic nanoflagellate, Bodo saltans. Limnol Oceanogr 43:1740–1746
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
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
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
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
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
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
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)
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
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
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
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
Manage PM, Kawabata Z, Nakano S (2000) Algicidal effect of the bacterium Alcaligenes denitrificans on Microcystis spp. Aquat Microb Ecol 22:111–117
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
Miura T (1990) The effects of planktivorous fishes on the plankton community in a eutrophic lake. Hydrobiologia 200(201):567–579
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
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
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
Reynolds CS, Walsby AE (1975) Water blooms. Biol Rev 50:437–481
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
Snell TW (1980) Blue-green algae and selection in rotifer populations. Oecologia 46:343–346
Sugiura N, Inamori Y, Ouchiyama T, Sudo R (1992) Degradation of cyanobacteria, Microcystis by microflagellate, Monas guttula. Water Sci Technol 26:2173–2176
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
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
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
Yamamoto Y, Nakahara H (2009) Seasonal variations in the morphology of bloom-forming cyanobacteria in a eutrophic pond. Limnology 10:185–193
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
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
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
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
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
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
Acknowledgments
This research was supported by the Environment Research and Technology Development Fund (D-0905) of the Ministry of the Environment, Japan.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Takehito Yoshida.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10201-012-0384-6