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

Limnology - Tập 14 - Trang 43-49 - 2012
Yuki Kobayashi1, Yoshikuni Hodoki1, Kako Ohbayashi1, Noboru Okuda1, Shin-ichi Nakano1
1Center for Ecological Research, Kyoto University, Otsu, Japan

Tóm tắt

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.

Tài liệu tham khảo

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