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Temporal distributions of microplankton populations and relationships to environmental conditions in Jiaozhou Bay, northern China

Published online by Cambridge University Press:  21 September 2012

Yong Jiang ,
Henglong Xu ,
Mingzhuang Zhu  and
Khaled A.S. Al-Rasheid
Yong Jiang
Affiliation:
Laboratory of Protozoology, Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao 266003, China
Henglong Xu*
Affiliation:
Laboratory of Protozoology, Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao 266003, China
Mingzhuang Zhu
Affiliation:
Laboratory of Protozoology, Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao 266003, China
Khaled A.S. Al-Rasheid
Affiliation:
Zoology Department, King Saud University, PO Box 2455, Riyadh 11451, Saudi Arabia
*
Correspondence should be addressed to: H. Xu, Laboratory of Protozoology, Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao 266003, China email: [email protected]
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Abstract

To analyse temporal distributions of microplankton populations and relationships to environmental conditions in marine ecosystems, a dataset of microplankton communities was investigated using a range of statistical methods. A total of 164 microplankton species comprising 100 microalgae and 64 ciliates were identified from 120 samples, respectively. Both planktonic microalga and ciliate assemblages showed temporal patterns and were significantly correlated between their temporal variations in abundance. The microplankton communities were characterized by 14 ciliates (e.g. Strombidium sulcatum, Tintinnopsis tubulosoides and Strombidium cheshiri) and 18 microalgae (e.g. Skeletonema costatum and Alexandrium tamarense). Multiple regression analyses showed that the interspecies correlations among these dominant species represented a complex network with a clear seasonal shift. Temporal pattern of microplankton communities was significantly correlated with the environmental variables such as temperature, salinity and nitrate nitrogen. The results suggest the clear species distribution and temporal dynamics of microplankton communities in response to environmental changes, and multivariate statistical approaches were a useful tool to reveal the species distribution patterns and complex microplanktonic interspecies correlations in marine ecosystems.

Keywords

microplanktonseasonal variationmicrobial food webmarine ecosystem
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 93 , Issue 1 , February 2013 , pp. 13 - 26
Copyright
Copyright © Marine Biological Association of the United Kingdom 2012

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References

REFERENCES

Admiraal, W. and Venekamp, L.A.H. (1986) Significance of tintindid grazing during blooms of Phaeocystis pouchetii (Haptophyceae) in Dutch coastal waters. Netherlands Journal of Sea Research 20, 61–66.CrossRefGoogle Scholar
Agatha, S. and Riedel-Lorjé, J. (1998) Morphology, infraciliature, and ecology of some strobilidiine ciliates (Ciliophora, Oligotrichea) from coastal brackish water basins of Germany. European Journal of Protistology 34, 10–17.CrossRefGoogle Scholar
APHA (American Public Health Association) (1992) Standard methods for examination of water and wastewater. 17th edition. Washington, DC: APHA.Google Scholar
Anderson, M.J., Gorley, R.N. and Clarke, K.R. (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. Plymouth: PRIMER-E Ltd.Google Scholar
Bernard, C. and Rassoulzadegan, F. (1990) Bacteria or microflagellates as a major food source for marine ciliates: possible implications for the microzooplankton. Marine Ecology Progress Series 64, 147–155.CrossRefGoogle Scholar
Bochstahler, K.R. and Coats, D.W. (1993) Grazing of the mixotrophic dinoflagellate Gymnodinium sanguineum on ciliate populations of Chesapeake Bay. Marine Biology 116, 477–487.CrossRefGoogle Scholar
Clarke, K.R. and Gorley, R.N. (2006) PRIMER v6: user manual/tutorial. Plymouth: PRIMER-E Ltd.Google Scholar
Clarke, K.R. and Warwick, R.M. (1994) Change in marine communities: an approach to statistical analysis and interpretation. Plymouth: Plymouth Marine Laboratory, Natural Environment Research Council.Google Scholar
Clough, J. and Strom, S. (2005) Effects of Heterosigma akashiwo (Raphidophyceae) on protist grazers: laboratory experiments with ciliates and heterotrophic dinoflagellates. Aquatic Microbial Ecology 39, 121–134.CrossRefGoogle Scholar
Dolan, J.R. and Simek, K. (1997) Processing of ingested matter in Strombidium sulcatum, a marine ciliate (Oligotrichida). Limnology and Oceanography 42, 393–397.CrossRefGoogle Scholar
Gomez, F. and Gorsky, G. (2003) Annual microplankton cycles in Villefranche Bay, Ligurian Sea, NW Mediterranean. Journal of Planktonic Research 25, 323–339.CrossRefGoogle Scholar
Granéli, E. and Johansson, N. (2003) Effects of the toxic haptophyte Prymnesium parvum on the survival and feeding of a ciliate: the influence of different nutrient conditions. Marine Ecology Progress Series 254, 49–56.CrossRefGoogle Scholar
Gransden, S.G. and Lewitus, A.J. (2003) Grazing of two euplotid ciliates on the heterotrophic dinoflagellates Pfiesteria piscicida and Cryptoperidiniopsis sp. Aquatic Microbial Ecology 33, 303–308.CrossRefGoogle Scholar
Hasle, G.R. and Syvertsen, E.E. (1997) Marine diatoms. In Tomas, C.R. (ed.) Identifying marine phytoplankton. San Diego, CA: Academic Press, pp. 5–386.CrossRefGoogle Scholar
Heinbokel, J.F. (1978) Studies on the functional role of tintinnids in the Southern California Bight. I. Grazing and growth rates in laboratory cultures. Marine Biology 47, 177–189.CrossRefGoogle Scholar
Jakobsen, H.H., Hyatt, C. and Buskey, E.J. (2001) Growth and grazing on the ‘Texas brown tide’ alga Aureoumbra lagunensis by the tintinnid Amphorides quadrilineata. Aquatic Microbial Ecology 23, 245–252.CrossRefGoogle Scholar
Jacobson, D.M. and Anderson, D.M. (1996) Widespread phagocytosis of ciliates and other protists by mixotrophic and heterotrophic thecate dinoflagellates. Journal of Phycology 32, 279–285.CrossRefGoogle Scholar
Jeong, H.J., Shim, J.H., Lee, C.W., Kim, J.S. and Koh, S.M. (1999) Growth and grazing rates of the marine planktonic ciliate Strombidinopsis sp. on red-tide and toxic dinoflagellates. Journal of Eukaryotic Microbiology 46, 69–76.CrossRefGoogle Scholar
Jiang, Y., Xu, H., Hu, X., Zhu, M., Al-Rasheid, K.A.S. and Warren, A. (2011a) An approach to analyzing spatial patterns of planktonic ciliate communities for monitoring water quality in Jiaozhou Bay, northern China. Marine Pollution Bulletin 62, 227–235.CrossRefGoogle ScholarPubMed
Jiang, Y., Xu, H., Al-Rasheid, K.A.S., Warren, A., Hu, X. and Song, W. (2011b) 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, 97–105.CrossRefGoogle Scholar
Jiang, Y., Xu, H., Zhang, W., Zhu, M. and Al-Rasheid, K.A.S. (2012a) Can body-size patterns of ciliated zooplankton be used for assessing marine water quality? A case study on bioassessment in Jiaozhou Bay, northern Yellow Sea. Environmental Science and Pollution Research 19, 1747–1754.CrossRefGoogle ScholarPubMed
Jiang, Y., Zhang, W., Zhu, M., Al-Rasheid, K.A.S. and Xu, H. (2012b) Are non-loricate ciliates a primary contributor to ecological pattern of planktonic ciliate communities? A case study in Jiaozhou Bay, northern China. Journal of the Marine Biological Association of the United Kingdom. DOI 10.1017/S0025315412000276.CrossRefGoogle Scholar
Kamiyama, T. and Arima, S. (2001) Feeding characteristics of two tintinnid ciliate species on phytoplankton including harmful species: effects of prey size on ingestion rates and selectivity. Journal of Experimental Marine Biology and Ecology 257, 281–196.CrossRefGoogle ScholarPubMed
Kamiyama, T. and Matsuyama, Y. (2005) Temporal changes in the ciliate assemblage and consecutive estimates of their grazing effect during the course of a Heterocapsa circularisquama bloom. Journal of Planktonic Research 27, 303–311.CrossRefGoogle Scholar
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. Estuarine, Coastal and Shelf Science 83, 414–424.CrossRefGoogle Scholar
Li, A., Stoecker, D.K., Coats, D.W. and Adam, E.J. (1996) Ingestion of fluorescently labeled and phycoerythrin-containing prey by mixotrophic dinoflagellates. Aquatic Microbial Ecology 10, 139–147.CrossRefGoogle Scholar
Maneiro, I., Frangópulos, M., Guisande, C., Fernández, M., Reguera, B. and Riveiro, I. (2000) Zooplankton as a potential vector of diarrhetic shellfish poisoning toxins through the food web. Marine Ecology Progress Series 201, 155–163.CrossRefGoogle Scholar
Montagnes, D.J.S., Berger, J.D. and Taylor, F.J.R. (1996) Growth rate of the marine planktonic ciliate Strombidinopsis cheshiri Snyder and Ohman as a function of food concentration and interclonal variability. Journal of Experimental Marine Biology and Ecology 206, 121–132.CrossRefGoogle Scholar
Montagnes, D.J.S. 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, 502–506.CrossRefGoogle Scholar
Montagnes, D.J.S. and Lessard, E.J. (1999) Population dynamics of the marine planktonic ciliate Strombidinopsis multiauris: its potential to control phytoplankton blooms. Aquatic Microbial Ecology 20, 167–181.CrossRefGoogle Scholar
Pedersen, M.F. and Hansen, P.J. (2003) Effects of high pH on the growth and survival of six marine heterotrophic protists. Marine Ecology Progress Series 33, 33–41.CrossRefGoogle Scholar
Rosetta, C.H. and McManus, G.B. (2003) Feeding by ciliates on two harmful algal bloom species, Prymnesium parvum and Prorocentrum minimum. Harmful Algae 2, 109–126.CrossRefGoogle Scholar
Sapp, M., Schwaderer, A.S., Wiltshire, K.H., Hoppe, H.G., Gerdts, G. and Wichels, A. (2007) Species-specific bacterial communities in the phycosphere of microalgae? Microbial Ecology 53, 683–699.CrossRefGoogle ScholarPubMed
Setälä, O., Autio, R. and Kuosa, H. (2005) Predator–prey interactions between a planktonic ciliate Strombidium sp. (Ciliophora, Oligotrichida) and the dinoflagellate Pfiesteria piscicida (Dinamoebiales, Pyrrophyta). Harmful Algae 4, 235–247.CrossRefGoogle Scholar
Shen, Z. (2001) Historical changes in nutrient structure and its influences on phytoplankton composition in Jiaozhou Bay. Estuarine, Coastal and Shelf Science 52, 211–224.CrossRefGoogle Scholar
Smalley, G.W., Coats, D.W. and Adams, E.J. (1999) A new method using fluorescent microspheres to determine grazing on ciliates by the mixotrophic dinoflagellate Ceratium furca. Aquatic Microbial Ecology 17, 167–179.CrossRefGoogle Scholar
Smalley, G.W. and Coats, D.W. (2002) Ecology of the red-tide dinoflagellate Ceratium furca: distribution, mixotrophy, and grazing impact on ciliate populations of Chesapeake Bay. Journal of Eukaryotic Microbiology 49, 63–73.CrossRefGoogle ScholarPubMed
Song, W., Zhao, Y., Xu, K., Hu, X. and Gong, J. (2003) Pathogenic protozoa in mariculture. Beijing: Science Press.Google Scholar
Steidinger, K. and Tangen, K. (1997) Dinoflagellates. In Tomas, C.R. (ed.) Identifying marine phytoplankton. San Diego, CA: Academic Press, pp. 387–584.CrossRefGoogle Scholar
Stoecker, D.K. and McDowell Capuzzo, J. (1990) Predation on Protozoa: its importance to zooplankton. Journal of Planktonic Research 12, 891–908.CrossRefGoogle Scholar
Stoecker, D.K. and Michaels, A.E. (1991) Respiration, photosynthesis and carbon metabolism in planktonic ciliates. Marine Biology 108, 441–447.CrossRefGoogle Scholar
Stoecker, D.K., Parrow, M.W., Burkholder, J.M. and Glasgow, H.B. Jr (2002) Pfiesteria piscicida cultures with different histories of toxicity. Aquatic Microbial Ecology 28, 79–85.CrossRefGoogle Scholar
Strom, S.L. and Morello, T.A. (1998) Comparative growth rates and yields of ciliates and heterotrophic dinoflagellates. Journal of Planktonic Research 20, 571–584.CrossRefGoogle Scholar
Tang, K.W., Jakobsen, H.H. and Visser, A.W. (2001) Phaeocystis globosa (Prymenesiophyceae) and the planktonic food web: feeding, growth, and trophic interactions among grazers. Limnology and Oceanography 46, 1860–1870.CrossRefGoogle Scholar
Tillmann, U. (1998) Phagotrophy of a plastidic haptophyte, Prymnesium patelliferum. Aquatic Microbial Ecology 14, 155–160.CrossRefGoogle Scholar
Tillmann, U. (2004) Interactions between planktonic microalgae and protozoan grazers. Journal of Eukaryotic Microbiology 51, 156–168.CrossRefGoogle ScholarPubMed
Verity, P.G. (1985) Grazing, respiration, excretion, and growth rates of tintinnids. Limnology and Oceanography 30, 1268–1282.CrossRefGoogle Scholar
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, 1353–1362.CrossRefGoogle Scholar
Xu, H., Min, G.S., Choi, J.K., Zhu, M., Jiang, Y. and Al-Rasheid, K.A.S. (2010) Temporal population dynamics of the dinoflagellate Prorocentrum minimum in a semi-enclosed mariculture pond and its relationship to environmental factors and protozoan grazers. Chinese Journal of Oceanology and Limnology 28, 75–81.CrossRefGoogle Scholar
Xu, H., Jiang, Y., Al-Rasheid, K.A.S., Song, W. and Warren, A. (2011a) Spatial variation in taxonomic distinctness of ciliated protozoan communities at genus-level resolution and relationships to marine water quality in Jiaozhou Bay, northern China. Hydrobiologia 665, 67–78.CrossRefGoogle Scholar
Xu, H., Jiang, Y., Al-Rasheid, K.A.S., Al-Farraj, S.A. and Song, W. (2011b) Application of an indicator based on taxonomic relatedness of ciliated protozoan assemblages for marine environmental assessment. Environmental Science and Pollution Research 18, 1213–1221.CrossRefGoogle ScholarPubMed
Zhang, W. and Wang, R. (2001) Abundance and biomass of copepod nauplii and ciliates in Jiaozhou Bay. Oceanologia et Limnologia Sinica 32, 280–287. [In Chinese with English summary.]Google Scholar