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Recovery of ciliated protozoan communities in response to environmental change in a shrimp-farming pond in southern China

  • Qian Liu (a1), Borong Lu (a2), Xue Song (a1), Yan Li (a1), Yu Gao (a1), Huifang Li (a1), Min Wang (a1), Hongbing Shao (a1), Alan Warren (a3), Xiangrui Chen (a2), Yong Jiang (a1) and Zhihua Lin (a4)...


The temporal dynamics of ciliate community structure in a southern Chinese shrimp aquaculture facility were investigated during the period June–September 2012. A total of 53 species belonging to 37 genera and 17 orders were recorded based on analyses of eight samples. Ciliate abundance peaked between 16 August and 14 September 2012, while the maximum number of species occurred on 26 June 2012. Clear temporal patterns were observed in the ciliate community structure. The patterns of succession of the 10 most abundant species were consistent with the results of a Canonical Analysis of Principal coordinates (CAP) analysis. Correlation analyses showed that these patterns of succession were related to temporal changes in environmental variables. In summary, the results demonstrate that the ciliate community responds predictably to environmental variations and recovers from shrimp cultivation.


Corresponding author

Correspondence should be addressed to: Y. Jiang and X. Chen College of Marine Life, Ocean University of China, Qingdao 266003, P.R. China; School of Marine Sciences, Ningbo University, Ningbo 315211, P.R. China Emails: and


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Anderson, M.J., Gorley, R.N. and Clarke, K.R. (2008) PERMANOVA+ for PRIMER guide to software and statistical methods. Plymouth: PRIMER-E.
APHA (1992) Standard methods for examination of water and waste water. 18th edition. Washington, DC: American Public Health Association.
Bratvold, D., Lu, J. and Browdy, C.L. (1999) Disinfection, microbial community establishment and shrimp production in a prototype biosecure pond. Journal of the World Aquaculture Society 30, 422432.
Cao, L., Wang, W., Yang, Y., Yang, C., Yuan, Z., Xiong, S. and Diana, J. (2007) Environmental impact of aquaculture and countermeasures to aquaculture pollution in China. Environmental Science and Pollution Research 14, 452462.
Cardozo, A.P., Britto, V.O. and Odebrecht, C. (2011) Temporal variability of plankton and nutrients in shrimp culture ponds vs. adjacent estuarine water. Pan-American Journal of Aquatic Sciences 6, 2843.
Caron, D.A. and Goldmann, J.C. (1990) Protozoan nutrient regeneration. In Capriulo, G.M. (ed.) Ecology of marine protozoa. New York, NY: Oxford University Press, pp. 283306
Casé, M., Leça, E.E., Leitão, S.N., Sant, E.E., Schwamborn, R. and de Moraes Junior, A.T. (2008) Plankton community as an indicator of water quality in tropical shrimp culture ponds. Marine Pollution Bulletin 56, 13431352.
Clarke, K.R. and Gorley, R.N. (2006) PRIMER 6 user manual/tutorial. Plymouth: PRIMER-E.
Elloumi, J., Carrias, J.F., Ayadi, H., Sime-Ngando, T., Boukhris, M. and Bouain, A. (2006) Composition and distribution of planktonic ciliates from ponds of different salinity in the solar saltwork of Sfax, Tunisia. Estuarine Coastal and Shelf Science 67, 2129.
Endo, Y., Hasumoto, H. and Taniguchi, A. (1983) Microzooplankton standing crop in the western subtropical Pacific off the Bonin Islands in winter. Journal of the Oceanographical Society of Japan 39, 185191.
Finlay, B.J., Bannister, P. and Stewart, J. (1979) Temporal variation in benthic ciliates and the application of association analysis. Freshwater Biology 9, 4553.
Finlay, B.J., Berninger, U.G., Clarke, K.J., Cowling, A.J., Hindle, R.M. and Rogerson, A. (1988) On the abundance and distribution of protozoa and their food in a productive fresh water pond. European Journal of Protistology 23, 205217.
Gong, J., Song, W. and Warren, A. (2005) Periphytic ciliate colonization: annual cycle and responses to environmental conditions. Aquatic Microbial Ecology 39, 159179.
Ismael, A.A. and Dorgham, M.M. (2003) Ecological indices as a tool for assessing pollution in El-Dekhaila Harbour (Alexandria, Egypt). Oceanologia 45, 121131.
Jiang, Y., Xu, H., Hu, X., Song, W., Alrasheid, K.A.S. and Warren, A. (2011 b) Planktonic ciliate communities in a semi-enclosed bay of Yellow Sea, northern China: annual cycle. Journal of the Marine Biological Association of the United Kingdom 91, 97105.
Jiang, Y., Xu, H., Hu, X., Zhu, M., Al-Rasheid, K.A.S. and Warren, A. (2011 a) An approach to analyzing spatial patterns of planktonic ciliate communities for monitoring water quality in Jiaozhou Bay, northern China. Marine Pollution Bulletin 62, 227235.
Jiang, Y., Yang, E.J., Kim, S.Y., Kim, Y.N. and Lee, S. (2014) Spatial patterns in pelagic ciliate community responses to various habitats in the Amundsen Sea (Antarctica). Progress in Oceanography 128, 4959.
Jiang, Y., Yang, E.J., Min, J.O., Kang, S.H. and Lee, S.H. (2013) Using pelagic ciliated microzooplankton communities as an indicator for monitoring environmental condition under impact of summer sea-ice reduction in western arctic ocean. Ecological Indicators 34, 380390.
Kankaala, P. and Eloranta, P. (1987) Epizooic ciliates (Vorticella sp.) compete for food with their host Daphnia longispina in a small polyhumic lake. Oecologia 73, 203206.
Kchaou, N., Elloumi, J., Drira, Z., Hamza, A., Ayadi, H., Bouain, A. and Aleya, L. (2009) Distribution of ciliates in relation to environmental factors along the coastline of the Gulf of Gabes, Tunisia. Coastal and Shelf Science 83, 414424.
Kim, Y.O., Chae, J., Hong, J.S. and Jang, P.G. (2007) Comparing the distribution of ciliate plankton in inner and outer areas of a harbor divided by an artificial breakwater. Marine Environmental Research 64, 3853.
Kofoid, C.A. and Campbell, A.S. (1929) A conspectus of the marine and freshwater Ciliata belonging to the suborder Tintinnoinea, with descriptions of new species principally from the Agassiz expedition to the eastern tropical Pacific 1904–1905. University of California Publications in Zoology 34, 1403.
Kofoid, C.A. and Campbell, A.S. (1939) The Tintinnoinea of the eastern tropical Pacific. Bulletin of the Museum of Comparative Zoology at Harvard College 84, 1473.
Lynn, D.H. (2008) The ciliated protozoa. Characterization, classification and guide to the literature. 3rd edition. Berlin: Springer.
Martin, J.H., Coale, K.H., Johnson, K.S., Fitzwater, S.E., Gordon, R.M., Tanner, S.J., Hunter, C.N., Elord, V.A., Nowicki, J.L., Coley, T.L., Barber, R.T., Lindly, S., Watson, A.J., Van Scoy, K., Law, C.S., Liddicoat, M.I., Ling, R., Ondrusek, M., Latasa, M., Millero, F.J., Lee, J., Yao, W., Zhang, J.Z., Friedrich, G., Sakamoto, C., Anderson, A., Bidigare, R., Ondrusek, M., Latasa, M., Millero, F.J., Lee, J., Yao, W., Zhang, J.Z., Friederich, G., Sakamoto, C., Chavez, F., Buck, K., Kolber, Z., Greene, R., Falkowski, P., Chishohn, S.W., Hoge, F., Swift, R., Yungel, J., Turner, S., Nightingale, P., Hatton, A., Liss, P. and Tindale, N.W. (1994) Testing the iron hypothesis in ecosystem of the equatorial Pacific Ocean. Nature 371, 123129.
Montagnes, D. and Humphrey, E. (1998) A description of occurrence and morphology of a new species of red-water forming Strombidium (Spirotrichea, Oligotrichia). Journal of Eukaryotic Microbiology 45, 502506.
Naylor, R.L., Goldburg, R.J., Primavera, J.H., Kautsky, N., Beveridge, M.C., Clay, J., Folke, C., Lubchenco, J., Mooney, H. and Troell, M. (2000) Effect of aquaculture on world fish supplies. Nature 405, 10171024.
Pierce, R.W. and Turner, J.T. (1992) Ecology of planktonic ciliates in marine food webs. Reviews in Aquatic Science 6, 139181.
Pitta, P., Giannakourou, A. and Christaki, U. (2001) Planktonic ciliates in the oligotrophic Mediterranean Sea: longitudinal trends of standing stocks, distributions and analysis of food vacuole contents. Aquatic Microbial Ecology 24, 297311.
Rahman Al Muftah, A. (2015) The status of harmful algae in the Arabian Gulf. Science Proceedings 5, 12.
Rekik, A., Denis, M., Dugenne, M., Maalej, S. and Ayadi, H. (2015) Planktonic ciliates in relation to abiotic variables on the north coast of Sfax after environmental restoration: species composition, and abundance-biomass seasonal variation. Journal of Oceanography, Research and Data 8, 116.
Robertson, A.I. and Phillips, M.J. (1995) Mangroves as filters of shrimp pond effluent: predictions and biogeochemical research needs. Hydrobiologia 295, 311321.
Selbach, M. and Kuhlmann, H.W. (1999) Structure, fluorescent properties and proposed function in phototaxis of the stigma apparatus in the ciliate Chlamydodon mnemosyne. Journal of Experimental Biology 202, 919927.
Shao, C., Gao, F., Hu, X., AL-Rasheid, K.A.S. and Warren, A. (2011) Ontogenesis and molecular phylogeny of a new marine urostylid ciliate, Anteholosticha petzi n. sp. (Ciliophora, Urostylida). Journal of Eukaryotic Microbiology 58, 254265.
Sherr, E.B. and Sherr, B.F. (1987) High rates of consumption of bacteria by pelagic ciliates. Nature 325, 710711.
Song, W., Warren, A. and Hu, X. (2009) Free-living ciliates in the Bohai and Yellow Seas, China. Beijing: Science Press [In Chinese]
Song, W., Zhao, Y., Xu, K., Hu, X. and Gong, J. (2003) Pathogenic protozoa in mariculture. Beijing: Science Press. [In Chinese]
Song, X., Xu, Z., Liu, Q., Li, Y., Ma, Y., Wang, J., Sun, M., Shao, H., Sun, H., Gill, M., Jiang, Y. and Wang, M. (2016) Comparative study of the composition and genetic diversity of the picoeukaryote community in a Chinese aquaculture area and an open sea area. Journal of the Marine Biological Association of the United Kingdom 97, 151159. doi: 10.1017/S0025315416000205.
Stoecker, D.K., Sieracki, M.R., Verity, P.G., Michaels, A.E., Haugen, E., Burkill, P.H. and Edwards, E.S. (1994) Nanoplankton and protozoan microzooplankton during the JGOFS North Atlantic bloom experiment. Journal of the Marine Biological Association of the United Kingdom 74, 427443.
Tovar, A., Moreno, C., Mánuel-Vez, M.P. and García-Vargas, M. (2000) Environmental impacts of intensive aquaculture in marine waters. Water Research 34, 334342.
Utermöhl, H. (1958) Zurvervolkommungder quantitativen phytoplankton Methodik. Mitteilungen der InernationaleVereinigung fur Theoretische und Angewandte. Limnologie 9, 138.
Wickham, S.A., Steinmair, U. and Kamennaya, N. (2011) Ciliate distributions and forcing factors in the Amundsen and Bellingshausen Seas (Antarctic). Aquatic Microbial Ecology 62, 215230.
Xu, H., Jiang, Y., Zhang, W., Zhu, M. and Al-Rasheid, K.S.A. (2011a) An approach to determining potential surrogates for analyzing ecological patterns of planktonic ciliate communities in marine bioassessments. Environmental Science and Pollution Research 18, 14331441.
Xu, H., Song, W., Warren, A., Al-Rasheid, K.A.S., Al-Farraj, S.A., Gong, J. and Hu, X. (2008) Planktonic protist communities in a semi-enclosed mariculture pond: structural variation and correlation with environmental conditions. Journal of the Marine Biological Association of the United Kingdom 88, 13531362.
Xu, H., Zhang, W., Jiang, Y., Zhu, M., Al-Rasheid, K.S.A., Warren, A. and Song, W. (2011b) An approach to determining sampling effort for analyzing biofilm-dwelling ciliate colonization using an artificial substrate in coastal waters. Biofouling 27, 357366.
Yang, E.J., Choi, J.K. and Hyun, J.H. (2004) Distribution and structure of heterotrophic protist communities in the northeast equatorial Pacific Ocean. Marine Biology 146, 115.
Zhu, M., Jiang, Y., Zhang, W., Al-Rasheid, K.A.S. and Xu, H. (2012) Can nonloricate ciliate assemblages be a surrogate to analyze taxonomic relatedness pattern of ciliated protozoan communities for marine bioassessment? A case study in Jiaozhou Bay, northern China. Water Environment Research 84, 20452053.



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