Picophytoplankton abundance and distribution in three contrasting periods in the Pearl River Estuary, South China
Xia Zhang A , Zhen Shi A , Feng Ye A , Yanyi Zeng A and Xiaoping Huang A B
+ Author Affiliations
- Author Affiliations
A State Key Laboratory of Tropical Oceanography, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, P. R. China.
B Corresponding author. Email: xphuang@scsio.ac.cn
Marine and Freshwater Research 64(8) 692-705 https://doi.org/10.1071/MF12303
Submitted: 22 October 2012 Accepted: 17 March 2013 Published: 21 June 2013
Abstract
Abundance and distribution characteristics of three picophytoplankton groups (Synechococcus, Prochlorococcus and picoeukaryotes), identified by flow cytometer, and two types of picocyanobacteria (phycoerythrin and phycocyanin-rich strains), determined by epifluorescence microscope, were assessed in three contrasting periods in the Pearl River Estuary, South China. The average abundance of picophytoplankon and picocyanobacteria was 104 cells mL–1 in the two summer observations and 103 cells mL–1 in winter. Low cell density in the cold season was probably due to high turbidity and low water temperature. Prochlorococcus was detected within the estuarine plume in the summer investigations and was undetectable in the winter. Higher abundance and the further upstream occurrence of Prochlorococcus in the summer of 2011 were mainly associated with extreme low river flows. We presumed that Prochlorococcus abundance and distribution range were balanced by river discharge and saline-water intrusion. Synechococcus was the dominant group in the inner estuary. Similar to Prochlorococcus, Synechococcus distribution was related with freshwater inflow. The river inflow exerted strong limitation on Synechococcus and Prochlorococcus, with this effect weakening along the salinity gradient. Picoeukaryotes were the least abundant category among picophytoplankton and showed a different distribution pattern from that of Synechococcus and Prochlorococcus. For picocyanobacteria, there was a clear spatial gradient with phycocyanin-rich strains dominant in the upper estuary, and phycocyanin-rich and phycoerythrin-rich cells dominant downstream. A significant negative correlation was observed between phycocyanin-rich cells to phycoerythrin-rich cells ratio and salinity.
Additional keywords: picocyanobacteria, picoplankton, Prochlorococcus.
References
Affronti, L. F., and Marshall, H. G. (1993). Diel abundance and productivity patterns of autotrophic picoplankton in the lower Chesapeake Bay. Journal of Plankton Research 15, 1–8.| Diel abundance and productivity patterns of autotrophic picoplankton in the lower Chesapeake Bay.Crossref | GoogleScholarGoogle Scholar |
Agawin, N. S., Duarte, C. M., and Agustí, S. (1998). Growth and abundance of Synechococcus sp. in a Mediterranean Bay: seasonality and relationship with temperature. Marine Ecology Progress Series 170, 45–53.
| Growth and abundance of Synechococcus sp. in a Mediterranean Bay: seasonality and relationship with temperature.Crossref | GoogleScholarGoogle Scholar |
Armstrong, F. A., Stearns, C. R., and Strickland, J. D. (1967). The measurement of upwelling and subsequent biological processes by means of the Technicon Auto Analyzer and associated equipment. Deep-sea Research. Part II. Topical Studies in Oceanography 14, 381–389.
| 1:CAS:528:DyaF1cXktlSgtg%3D%3D&md5=0d80fdbf9a97680b6b1cacdcc560acebCAS |
Badylak, S., and Phlips, E. J. (2004). Spatial and temporal patterns of phytoplankton composition in a subtropical coastal lagoon, the Indian River Lagoon, Florida, USA. Journal of Plankton Research 26, 1229–1247.
| Spatial and temporal patterns of phytoplankton composition in a subtropical coastal lagoon, the Indian River Lagoon, Florida, USA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVOks78%3D&md5=2bf46ec7d988849cbae888a295331d9aCAS |
Campbell, L., Landry, M. R., Constantinou, J., Nolla, H. A., Brown, S. L., Liu, H., and Caron, D. A. (1998). Response of microbial community structure to environmental forcing in the Arabian Sea. Deep-sea Research. Part II. Topical Studies in Oceanography 45, 2301–2325.
| Response of microbial community structure to environmental forcing in the Arabian Sea.Crossref | GoogleScholarGoogle Scholar |
Chisholm, S. W., Frankel, S. L., Goericke, R., Olson, R. J., Palenik, B., Waterbury, J. B., West-Johnsrud, L., and Zettler, E. R. (1992). Prochlorococcus marinus ov. gen. nov. sp.: an oxyphototrophic marine prokaryote containing Chlorophyll a and b. Archives of Microbiology 157, 297–300.
| Prochlorococcus marinus ov. gen. nov. sp.: an oxyphototrophic marine prokaryote containing Chlorophyll a and b.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhsVyisLg%3D&md5=59cc1220061b36014de637b8e42e72e2CAS |
Crosbie, N. D., and Furnas, M. J. (2001). Abundance, distribution and flow-cytometric characterization of picophytoprokaryote populations in central (17 degree S) and southern (20 degree S) shelf waters of the Great Barrier Reef. Journal of Plankton Research 23, 809–828.
| Abundance, distribution and flow-cytometric characterization of picophytoprokaryote populations in central (17 degree S) and southern (20 degree S) shelf waters of the Great Barrier Reef.Crossref | GoogleScholarGoogle Scholar |
Dortch, Q. (1998). Phytoplankton characteristics. In ‘An Observational Study of the Mississippi–Atchafalaya Coastal Plume. U.S’. (Ed. S. P. Murray.) pp. 239–268. MMS 98-00400. (Department of the Interior, Minerals Management Service. New Orleans, LA.)
Haas, L. W., and Pearl, H. W. (1988). The roles of blue-green algae. In ‘Chesapeake Bay. NOAA Estuary-of the-Month Seminar Series No. 5’. (Ed. S. E. McCoy.) p. 99–113. (National Oceanic and Atmospheric Administration, Estuarine Programs Office: Washington, DC.)
Huang, J. Y. (2012). Phylogenetic distribution of phycocyanin-rich Synechococcus spp. in the East China Sea in summers. M.Sc. Thesis, National Taiwan Ocean University, Taiwan, Republic of China.
Huang, B. Q., Lin, X. Y., Liu, M., Dai, M. H., Hong, H. S., and Li, W. (2002). Ecological study of picoplankton in northern South China Sea. Chinese Oceanology and Limnology 20, 22–32.
Huang, B. Q., Hong, H. S., Lin, X. J., Chen, J. X., and Liu, Y. (2003). Ecological study on picophytoplankton in the Taiwan Strait. I. Spatial and temporal distribution and its controlling factors. Acta Oceanologica Sinica 25, 72–82.
Huang, L. M., Jian, W. J., Song, X. Y., Huang, X. P., Liu, S., Qian, P. Y., Yin, K. D., and Wu, M. (2004). Species diversity and distribution for phytoplankton of the Pearl River Estuary during rainy and dry seasons. Marine Pollution Bulletin 49, 588–596.
| Species diversity and distribution for phytoplankton of the Pearl River Estuary during rainy and dry seasons.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXot1ykt70%3D&md5=6b70c812bffea8348f1c6686f29d0189CAS |
Iriarte, A. (1993). Size-fractionated chlorophylla biomass and picophytoplankton cell density along a longitudinal axis of a temperate estuary (Southampton Water). Journal of Plankton Research 15, 485–500.
| Size-fractionated chlorophylla biomass and picophytoplankton cell density along a longitudinal axis of a temperate estuary (Southampton Water).Crossref | GoogleScholarGoogle Scholar |
Jiao, N. Z., Yang, Y. H., Harada, S., Koshigawa, H., and Watanabe, M. (2002a). Responses of picoplankton to nutrient perturbation in the South China Sea, with special reference to the coast-ward distribution of Prochlorococcus. Acta Botanica Sinica 44, 731–739.
| 1:CAS:528:DC%2BD2cXktVSqsbo%3D&md5=b451323f065a78dceed66f804a4a2088CAS |
Jiao, N., Yang, Y., Koshigawa, H., and Watanabe, M. (2002b). Influence of hydrographic conditions on picoplankton distribution in the East China Sea. Aquatic Microbial Ecology 30, 37–48.
| Influence of hydrographic conditions on picoplankton distribution in the East China Sea.Crossref | GoogleScholarGoogle Scholar |
Jiao, N., Yang, Y., Hong, N., Ma, Y., Harada, S., Koshikawa, H., and Watanabe, M. (2005). Dynamics of autotrophic picoplankton and heterotrophic bacteria in the East China Sea. Continental Shelf Research 25, 1265–1279.
| Dynamics of autotrophic picoplankton and heterotrophic bacteria in the East China Sea.Crossref | GoogleScholarGoogle Scholar |
Jochem, F. J. (2003). Photo- and heterotrophic pico- and nanoplankton in the Mississippi River Plume: distribution and grazing activity. Journal of Plankton Research 25, 1201–1214.
| Photo- and heterotrophic pico- and nanoplankton in the Mississippi River Plume: distribution and grazing activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXosVeru7w%3D&md5=f2ec69ce4856f3bb84c735a99a9138d3CAS |
Kuparinen, J., and Kuosa, H. (1993). Autotrophic and heterotrophic picoplankton in the Baltic Sea. Advances in Marine Biology 29, 73–128.
| Autotrophic and heterotrophic picoplankton in the Baltic Sea.Crossref | GoogleScholarGoogle Scholar |
Larson, M., Bellanca, R., Jönsson, L., Chen, C. Q., and Shi, P. (2005). A model of the 3D circulation, salinity distribution, and transport pattern in the Pearl River Estuary, China. Journal of Coastal Research 21, 896–908.
Li, Y., and Li, D. J. (2012). Spatial distributions of picoplankton and viruses in the Changjiang Estuary and its adjacent sea area during summer. Journal of Marine Biology , .
| Spatial distributions of picoplankton and viruses in the Changjiang Estuary and its adjacent sea area during summer.Crossref | GoogleScholarGoogle Scholar |
Lin, D., Zhu, A., Xu, Z., Huang, L., and Fang, H. (2010). Dynamics of photosynthetic picoplankton in a subtropical estuary and adjacent shelf waters. Journal of the Marine Biological Association of the United Kingdom 90, 1319–1329.
| Dynamics of photosynthetic picoplankton in a subtropical estuary and adjacent shelf waters.Crossref | GoogleScholarGoogle Scholar |
Lindell, D., and Post, A. F. (1995). Ultraphytoplankton succession is triggered by deep winter mixing in the Gulf of Aqaba (Eilat), Red Sea. Limnology and Oceanography 40, 1130–1141.
| Ultraphytoplankton succession is triggered by deep winter mixing in the Gulf of Aqaba (Eilat), Red Sea.Crossref | GoogleScholarGoogle Scholar |
Liu, H. B., Dagg, M., Campbell, L., and Urban-Rich, J. (2004). Picophytoplankton and bacterioplankton in the Mississippi River Plume and its adjacent waters. Estuaries 27, 147–156.
| Picophytoplankton and bacterioplankton in the Mississippi River Plume and its adjacent waters.Crossref | GoogleScholarGoogle Scholar |
Lohrenz, S. E., Fahnenstiel, G. L., Redalje, D. G., Lang, G. A., Dagg, M. J., Whitledge, T. E., and Dortch, Q. (1999). Nutrients, irradiance, and mixing as factors regulating primary production in coastal waters impacted by the Mississippi River plume. Continental Shelf Research 19, 1113–1141.
| Nutrients, irradiance, and mixing as factors regulating primary production in coastal waters impacted by the Mississippi River plume.Crossref | GoogleScholarGoogle Scholar |
Mitbavkar, S., Rajaneesh, K. M., Anil, A. C., and Sundar, D. (2012). Picophytoplankton community in a tropical estuary: detection of Prochlorococcus-like populations. Estuarine, Coastal and Shelf Science 107, 159–164.
| Picophytoplankton community in a tropical estuary: detection of Prochlorococcus-like populations.Crossref | GoogleScholarGoogle Scholar |
Murrell, M. C., and Lores, E. M. (2004). Phytoplankton and zooplankton seasonal dynamics in a subtropical estuary: importance of cyanobacteria. Journal of Plankton Research 26, 371–382.
| Phytoplankton and zooplankton seasonal dynamics in a subtropical estuary: importance of cyanobacteria.Crossref | GoogleScholarGoogle Scholar |
Ning, X. R., Shi, J. X., Liu, Z. L., and Cai, Y. M. (1997). Abundance and distribution of photosynthetic picoplankton and the environmental limitation in Xiangshan Bay. Acta Oceanologica Sinica 10, 87–95.
Ning, X., Cloern, J. E., and Cole, B. E. (2000). Spatial and temporal variability of picocyanobacteria Synechococcus sp. in San Francisco Bay. Limnology and Oceanography 45, 695–702.
| Spatial and temporal variability of picocyanobacteria Synechococcus sp. in San Francisco Bay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsV2ltbk%3D&md5=390ad8d2e68d347f139ad060f971b53dCAS |
Pan, L. A., Zhang, J., and Zhang, L. H. (2007). Picophytoplankton, nanophytoplankton, heterotrophic bacteria and viruses in the Changjiang Estuary and adjacent coastal waters. Journal of Plankton Research 29, 187–197.
| Picophytoplankton, nanophytoplankton, heterotrophic bacteria and viruses in the Changjiang Estuary and adjacent coastal waters.Crossref | GoogleScholarGoogle Scholar |
Partensky, F., Hess, W. R., and Vaulot, D. (1999). Prochlorococcus, a marine photosynthetic prokaryote of global signiðcance. Microbiology and Molecular Biology Reviews 63, 106–127.
| 1:CAS:528:DyaK1MXitVert78%3D&md5=0c9ce6cc62ad9165c9a84848474e74aaCAS | 10066832PubMed |
Perkins, E., Haas, L., Phillips, D., and Webb, K. (1981). Ultrastructure of a marine Synechococcus possessing spinae. Canadian Journal of Microbiology 27, 318–329.
| 1:STN:280:DyaL3M3gvFKhtQ%3D%3D&md5=3b76c26b851667b400468ca38bf87fc4CAS |
Phlips, E. J., Badylak, S., and Lynch, T. C. (1999). Blooms of the picoplanktonic cyanobacterium Synechococcus in Florida Bay, a subtropical inner-shelf lagoon. Limnology and Oceanography 44, 1166–1175.
| Blooms of the picoplanktonic cyanobacterium Synechococcus in Florida Bay, a subtropical inner-shelf lagoon.Crossref | GoogleScholarGoogle Scholar |
Putland, J. N., and Rivkin, R. B. (1999). Influence of storage mode and duration on the microscopic enumeration of Synechococcus from a cold coastal ocean environment. Marine Ecology Progress Series 17, 191–199.
Qiu, D. J., Huang, L. M., Zhang, J. L., and Lin, S. J. (2010). Phytoplankton dynamics in and near the highly eutrophic Pearl River Estuary, South China Sea. Continental Shelf Research 30, 177–186.
| Phytoplankton dynamics in and near the highly eutrophic Pearl River Estuary, South China Sea.Crossref | GoogleScholarGoogle Scholar |
Ray, R. T., Haas, L. W., and Sieracki, M. E. (1989). Autotrophic picoplankton dynamics in a Chesapeake Bay sub-estuary. Marine Ecology Progress Series 52, 273–285.
| Autotrophic picoplankton dynamics in a Chesapeake Bay sub-estuary.Crossref | GoogleScholarGoogle Scholar |
Shimada, A., Nishijima, M., and Maruyama, T. (1995). Seasonal appearance of Prochlorococcus in Suruga Bay, Japan in 1992–1993. Journal of Oceanography 51, 289–300.
| Seasonal appearance of Prochlorococcus in Suruga Bay, Japan in 1992–1993.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmslCls7k%3D&md5=90105c6618f91fd3eae4d0885ec07869CAS |
Slawyk, G., and MacIsaac, J. J. (1972). Comparison of two automated ammonium methods in a region of coastal upwelling. Deep-Sea Research 19, 521–524.
| 1:CAS:528:DyaE3sXnsFKrsA%3D%3D&md5=60d8fd389bbb54bdd3435b4f5f48a159CAS |
Stockner, J. G., and Antia, N. J. (1986). Algal picoplankton from marine and freshwater ecosystems: a multidisciplinary perspective. Canadian Journal of Fisheries and Aquatic Sciences 43, 2472–2503.
| Algal picoplankton from marine and freshwater ecosystems: a multidisciplinary perspective.Crossref | GoogleScholarGoogle Scholar |
Stomp, M., Huisman, J., de Jongh, F., Veraart, A. J., Gerla, D., Rijkeboer, M., Ibellings, B. W., Wollenzien, U. I. A., and Stal, L. J. (2004). Adaptive divergence in pigment composition promotes phytoplankton biodiversity. Journal of General Microbiology 111, 1–61.
Stomp, M., Huisman, J., Vörös, L., Pick, F. R., Laamanen, M., Haverkamp, T., and Stal, L. J. (2007). Colorful coexistence of red and green pico-cyanobacteria in lakes and seas. Ecology Letters 10, 290–298.
| Colorful coexistence of red and green pico-cyanobacteria in lakes and seas.Crossref | GoogleScholarGoogle Scholar | 17355568PubMed |
Sun, L., Ren, F. M., Wang, Z. Y., Liu, Y. Y., Liu, Y. J., Wang, P. L., and Wang, D. Q. (2012). Analysis of anomaly and causation in August 2011. Meteorological Monographs 38, 615–622.
Tsai, A. Y., Chiang, K., Chang, P. J., and Gong, G. C. (2008). Seasonal variations in trophic dynamics of nanoflagellates and picoplankton in coastal waters of the western subtropical Pacific Ocean. Aquatic Microbial Ecology 51, 263–274.
| Seasonal variations in trophic dynamics of nanoflagellates and picoplankton in coastal waters of the western subtropical Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |
Vaulot, D., and Ning, X. (1988). Abundance and cellular characteristics of marine Synechococcus spp. in the dilution zone of the Changjiang (Yangtze) River China. Continental Shelf Research 8, 1171–1186.
| Abundance and cellular characteristics of marine Synechococcus spp. in the dilution zone of the Changjiang (Yangtze) River China.Crossref | GoogleScholarGoogle Scholar |
Vaulot, D., Partensky, F., Neveux, J., Mantoura, R. F. C., and Llewellyn, C. A. (1990). Winter presence of prochlorophytes in surface waters of the northwestern Mediterranean Sea. Limnology and Oceanography 35, 1156–1164.
| Winter presence of prochlorophytes in surface waters of the northwestern Mediterranean Sea.Crossref | GoogleScholarGoogle Scholar |
Vörös, L., Callieri, C., Balogh, K. V., and Bertoni, R. (1998). Freshwater picocyanobacteria along trophic gradient and light quality range. Hydrobiologia 369/370, 117–125.
| Freshwater picocyanobacteria along trophic gradient and light quality range.Crossref | GoogleScholarGoogle Scholar |
Wang, C. H. (2006). Numerical modeling of wave-current induced turbidity maximum in the Pearl River Estuary. Ph.D Thesis. The Hong Kong Polytechnic University, Hong Kong.
Wang, K., Wommack, K. E., and Chen, F. (2011). Abundance and distribution of Synechococcus spp. and cyanophages in the Chesapeake Bay. Applied and Environmental Microbiology 77, 7459–7468.
| Abundance and distribution of Synechococcus spp. and cyanophages in the Chesapeake Bay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Ors73L&md5=cb3ca7f19ea95c72b3a82bf240defb55CAS | 21821760PubMed |
Wood, E., Armstrong, F., and Richards, F. (1967). Determination of nitrate in sea water by cadmium-copper reduction to nitrite. Journal of the Marine Biological Association of the United Kingdom 47, 23–31.
| Determination of nitrate in sea water by cadmium-copper reduction to nitrite.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2sXktlKgsr8%3D&md5=d2571beeca70ec79c31663cddbade036CAS |
Wood, A. M., Horan, P. K., Muirhead, K., Phinney, D. A., Yentsch, C. M., and Waterbury, J. B. (1985). Discrimination between types of pigments in marine Synechococcus spp. by scanning spectroscopy, epifluorescence microscopy, and flow cytometry. Limnology and Oceanography 30, 1303–1315.
| Discrimination between types of pigments in marine Synechococcus spp. by scanning spectroscopy, epifluorescence microscopy, and flow cytometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XjtFCmug%3D%3D&md5=0fe93c3b61115afccf39e4c767a5f611CAS |
Yin, K. D., Song, X. X., Sun, J., and Wu, M. C. S. (2004). Potential P limitation leads to excess N in the pearl river estuarine coastal plume. Continental Shelf Research 24, 1895–1907.
| Potential P limitation leads to excess N in the pearl river estuarine coastal plume.Crossref | GoogleScholarGoogle Scholar |
Zhao, H. (Ed.) (1990). ‘Evolution of the Pearl River Estuary.’ (Ocean Press: Beijing.) [In Chinese].
Zubkov, M. V., Sleigh, M. A., Tarran, G. A., Burkill, P. H., and Leakey, R. J. G. (1998). Picoplanktonic community structure on an Atlantic transect from 50°N to 50°S. Deep-sea Research. Part I. Oceanographic Research Papers 45, 1339–1355.
| Picoplanktonic community structure on an Atlantic transect from 50°N to 50°S.Crossref | GoogleScholarGoogle Scholar |
