Abstract
Phytoplankton diversity and abundance in estuarine systems are controlled by many factors. Salinity, turbidity, and inorganic nutrient concentrations and their respective ratios have all been proposed as principal factors that structure phytoplankton diversity and influence the emergence of potentially toxic species. Although much work has been conducted on temperate estuaries, less is known about how phytoplankton diversity is controlled in tropical, monsoonal systems that are subject to large, seasonal shifts in hydrology and to rapidly changing land use. Here, we present the results of an investigation into the factors controlling phytoplankton species composition and distribution in a tropical, monsoonal estuary (Bach Dang estuary, North Vietnam). A total of 245 taxa, 89 genera from six algal divisions were observed. Bacillariophyceae were the most diverse group contributing to 51.4 % of the microalgal assemblage, followed by Dinophyceae (29.8 %), Chlorophyceae (10.2 %), Cyanophyceae (3.7 %), Euglenophyceae (3.7 %) and Dictyochophyceae (1.2 %). The phytoplankton community was structured by inorganic nutrient ratios (DSi:DIP and DIN:DIP) as well as by salinity and turbidity. Evidence of a decrease in phytoplankton diversity concomitant with an increase in abundance and dominance of certain species (e.g., Skeletonema costatum) and the appearance of some potentially toxic species over the last two decades was also found. These changes in phytoplankton diversity are probably due to a combination of land use change resulting in changes in nutrient ratios and concentrations and global change as both rainfall and temperature have increased over the last two decades. It is therefore probable in the future that phytoplankton diversity will continue to change, potentially favoring the emergence of toxic species in this system.
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References
Aminot, A., & Kerouel, R. (1998). Pasteurization as an alternative method for preservation of nitrate and nitrite in seawater samples. Marine Chemistry, 61(3–4), 203–208.
Anderson, D. M., Glibert, P. M., & Burkholder, J. M. (2002). Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries, 25(4), 704–726. doi:10.1007/bf02804901.
Balech, E. (1995). The genus Alexandrium Halim (Dinoflagellata) (Vol. 1). Sherkin Island, Co. Cork, Ireland: Sherkin Island Marine Station.
Benschneider, K., & Robinson, R. J. (1952). A new spectrophotometric method for the determination of nitrite in sea water. Journal of Marine Research, 11, 87–96.
Berger, W. H., & Parker, F. L. (1970). Diversity of planktonic Foraminifera in deep-sea sediments. Science, 168, 1345–1347.
Bettarel, Y., Bouvier, T., Agis, M., Bouvier, C., Chu, V. T., Combe, M., et al. (2011). Viral distribution and life strategies in the Bach Dang estuary, Vietnam. Microbial Ecology, 62, 142–154.
Borges, A. V. (2005). Do we have enough pieces of the jigsaw to integrate CO2 fluxes in the coastal ocean? Estuaries, 28(1), 3–27.
Canini, N. D., Metillo, E. B., & Azanza, R. V. (2013). Monsoon-influenced phytoplankton community structure in a Philippine mangrove estuary. Tropical Ecology, 54(3), 331–343.
Chao, A., Chazdon, R. L., Colwell, R. K., & Shen, T.-J. (2005). A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecology Letters, 8(2), 148–159. doi:10.1111/j.1461-0248.2004.00707.x.
Chapman, D. (1996). Water Quality Assessments - A Guide to Use of Biota, Sediments and Water in Environmental Monitoring: UNESCO/WHO/UNEP
Chu, V. T. (1996). Phytoplankton in the three rivermouths: Tien Yen, Bach Dang and Red river. In Collection of Marine Environment and Resources (Vol. III, pp. 223–242): Science and Technics Publishing House, Hanoi, Vietnam.
Chu, V. T., & Tran, V. D. (2003). An overview of current activities relating to phytoplankton monitoring in coastal waters of North Vietnam. Paper presented at the Workshop on Red Tide Monitoring in Asian Coastal Waters, March 10–12, 2003, University of Tokyo, Japan
Chu, V. T., Nguyen, T. M. H., Pham, T. T., & Le, T. T. (2012). Some new data on phytoplankton in the western of Tonkin Gulf. Vietnam Journal of Marine Science and Technology, 12, 32–46.
Combe, M., Bouvier, T., Pringault, O., Rochelle-Newall, E., Bouvier, C., Agis, M., et al. (2013). Freshwater prokaryote and virus communities can adapt to a controlled increase in salinity through changes in their structure and interactions. Estuarine, Coastal and Shelf Science, 133, 58–66. doi:10.1016/j.ecss.2013.08.013.
Cronberg, G., & Annadotter, H. (2006). Manual on aquatic cyanobacteria—a photo guide and a synopsis of their toxicology. Denmark: ISSHA.
Dollhopf, S. L., Hashsham, S. A., & Tiedje, J. M. (2001). Interpreting 16S rDNA T-RFLP data: application of self-organizing maps and principal component analysis to describe community dynamics and convergence. Microbial Ecology, 42(4), 495–505.
Duong, D. T., & Vo, H. (1997). Vietnam freshwater algae—taxonomy of order Chlorococcales. Hanoi: Agriculture Publishing House.
Duong, T. T., Coste, M., Feurtet-Mazel, A., Dang, D. K., Gold, C., Park, Y. S., et al. (2006). Impact of urban pollution from the Hanoi area on benthic diatom communities collected from the red, Nhue and Tolich rivers (Vietnam). Hydrobiologia, 563, 201–216.
Duong, T. T., Le, T. P. Q., Dao, T.-S., Pflugmacher, S., Rochelle-Newall, E., Hoang, T., et al. (2013). Seasonal variation of cyanobacteria and microcystins in the Nui Coc Reservoir, Northern Vietnam. Journal of Applied Phycology, 25(4), 1065–1075. doi:10.1007/s10811-012-9919-9.
Eaton, A. D., Clesceri, L. S., & Greenberg, A. E. (1995). Standard methods for the examination of water and wastewater (19 ed.). Washington, DC.
Elliott, M., & McLusky, D. S. (2002). The need for definitions in understanding estuaries. Estuarine, Coastal and Shelf Science, 55(6), 815–827. doi:10.1006/ecss.2002.1031.
Fanning, G. O., & Pilson, M. E. Q. (1973). On the spectrophotometric determination of dissolved silica in natural waters. Analytical Chemistry Symposia Series, 45, 136–140.
Fisher, T. R., Harding, L. W., Stanley, D. W., & Ward, L. G. (1988). Phytoplankton, nutrients and turbidity in the Chesapeake, Delaware and Hudson estuaries. Estuarine and Coastal Shelf Science, 27, 61–93.
Fisher, T. R., Hagy, J. D., & Rochelle-Newall, E. (1998). Dissolved and particulate organic carbon in Chesapeake Bay. Estuaries, 21(2), 215–229.
Fisher, T. R., Gustafson, A. B., Sellner, K., Lacouture, R., Haas, L. W., Wetzel, R. L., et al. (1999). Spatial and temporal variation of resource limitation in Chesapeake Bay. Marine Biology, 133(4), 763–778.
Fonge, B. A., Tening, A. S., Egbe, E. A., Yinda, G. S., Fongod, A. N., & Achu, R. M. (2012). Phytoplankton diversity and abundance in Ndop wetland plain, Cameroon. African Journal of Environmental Science and Technology, 523(6), 247–257.
Fukuyo, Y., Takano, H., Chihara, M., & Matsuoka, K. (1990). Red tide organisms in Japan—an illustrated taxonomic guide. Tokyo, Japan: Uchida Rokakuho.
Halpern, B. S., Walbridge, S., Selkoe, K. A., Kappel, C. V., Micheli, F., D'Agrosa, C., et al. (2008). A global map of human impact on marine ecosystems. Science, 319(5865), 948–952. doi:10.1126/science.1149345.
He, D., Ren, J., Fu, K., & Li, Y. (2007). Sediment change under climate changes and human activities in the Yuanjiang-Red River Basin. Chinese Science Bulletin, 52(2), 164–171. doi:10.1007/s11434-007-7010-8.
HIO. (1995). Assessment of water quality in the Haiphong harbour and the coastal waters of Haiphong city (Project database). Haiphong, Vietnam: Institute of Marine Environment and Resources.
Holm-Hansen, O., Lorenzen, C. J., Holmes, R. W., & Strickland, J. D. H. (1965). Fluorimetric determination of chlorophyll. [Rapp P-V Reun Cons Int Explor Mer]. Journal of Construct International Exploration Mer., 30, 3–15.
Howarth, R., & Paerl, H. W. (2008). Coastal marine eutrophication: control of both nitrogen and phosphorus is necessary. Proceedings of the National Academy of Sciences of the United States of America, 105(49), E103–E103. doi:10.1073/pnas.0807266106.
Howarth, R., Swaney, D., Billen, G., Garnier, J., Hong, B. G., Humborg, C., et al. (2012). Nitrogen fluxes from the landscape are controlled by net anthropogenic nitrogen inputs and by climate. Frontiers in Ecology and the Environment, 10(1), 37–43. doi:10.1890/100178.
Huang, L., Jian, W., Song, X., Huang, X., Liu, S., Qian, P., et al. (2004). Species diversity and distribution for phytoplankton of the Pearl River estuary during rainy and dry seasons. Marine Pollution Bulletin, 49(7–8), 588–596. doi:10.1016/j.marpolbul.2004.03.015.
Huang, W., Zhu, X., Chen, Q., He, Q., Liao, Y., Du, P., et al. (2013). Seasonal variability of phytoplankton community structure in relation to different nitrogen-phosphorus ratios in the southern coastal waters of Zhejiang, China. Journal of Ocean University of China, 12(4), 577–588. doi:10.1007/s11802-013-2192-y.
Jaanus, A., Toming, K., Hällfors, S., Kaljurand, K., & Lips, I. (2009). Potential phytoplankton indicator species for monitoring Baltic coastal waters in the summer period. In J. H. Andersen, & D. J. Conley (Eds.), Eutrophication in Coastal Ecosystems (Vol. 207, pp. 157–168, Developments in Hydrobiology): Springer Netherlands.
Justić, D., Rabalais, N. N., & Turner, R. E. (1995a). Stoichiometric nutrient balance and origin of coastal eutrophication. Marine Pollution Bulletin, 30(1), 41–46. doi:10.1016/0025-326X(94)00105-I.
Justić, D., Rabalais, N. N., Turner, R. E., & Dortch, Q. (1995b). Changes in nutrient structure of river-dominated coastal waters: stoichiometric nutrient balance and its consequences. Estuarine, Coastal and Shelf Science, 40(3), 339–356. doi:10.1016/S0272-7714(05)80014-9.
Karlsson, J., Bystrom, P., Ask, J., Ask, P., Persson, L., & Jansson, M. (2009). Light limitation of nutrient-poor lake ecosystems. Nature, 460(7254), 506–509.
Le, T. P. Q., Billen, G., Garnier, J., Thery, S., Ruelland, D., Nghiem, X. A., et al. (2010). Nutrient (N, P, Si) transfers in the subtropical Red River system (China and Vietnam): Modelling and budget of nutrient sources and sinks. Journal of Asian Earth Sciences, 37(3), 259–274. doi:10.1016/j.jseaes.2009.08.010.
Lee, K. Y., Fisher, T. R., & Rochelle-Newall, E. (2001). Modeling the hydrochemistry of the Choptank river basin using GWLF and Arc/Info: 2. Model validation and application. Biogeochemistry, 56(3), 311–348.
Lefebvre, J.-P., Ouillon, S., Vinh, V., Arfi, R., Panché, J.-Y., Mari, X., et al. (2012). Seasonal variability of cohesive sediment aggregation in the Bach Dang–Cam Estuary, Haiphong (Vietnam). Geo-Marine Letters, 32(2), 103–121. doi:10.1007/s00367-011-0273-8.
Legendre, P., & Legendre, L. (1998). Numerical ecology. Amsterdam: Elsevier.
Li, R. H., Liu, S. M., Li, Y. W., Zhang, G. L., Ren, J. L., & Zhang, J. (2014). Nutrient dynamics in tropical rivers, lagoons, and coastal ecosystems of eastern Hainan Island, South China Sea. Biogeosciences, 11(2), 481–506. doi:10.5194/bg-11-481-2014.
Lie, A. A. Y., Wong, C. K., Lam, J. Y. C., Liu, J. H., & Yung, Y. K. (2011). Changes in the nutrient ratios and phytoplankton community after declines in nutrient concentrations in a semi-enclosed bay in Hong Kong. Marine Environmental Research, 71(3), 178–188. doi:10.1016/j.marenvres.2011.01.001.
Lueangthuwapranit, C., Sampantarak, U., & Wongsai, S. (2011). Distribution and abundance of phytoplankton: influence of salinity and turbidity gradients in the Na Thap River, Songkhla Province, Thailand. Journal of Coastal Research, 27(3), 585–594. doi:10.2112/jcoastres-d-10-00123.1.
Lui, H. K., & Chen, C. T. A. (2011). Shifts in limiting nutrients in an estuary caused by mixing and biological activity. Limnology and Oceanography, 56(3), 989–998. doi:10.4319/lo.2011.56.3.0989.
Mette, E. M., Vanni, M. J., Newell, J. M., & Gonzalez, M. J. (2011). Phytoplankton communities and stoichiometry are interactively affected by light, nutrients, and fish. Limnology and Oceanography, 56(6), 1959–1975. doi:10.4319/lo.2011.56.6.1959.
Mullin, J. B., & Riley, J. P. (1955). The spectrophotometric determination of silicate-silicon in natural waters with special reference to sea water. Analytica Chimica Acta, 12, 162–170.
Murphy, J., & Riley, J. P. (1962). A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta, 27, 31–36. doi:10.1016/S0003-2670(00)88444-5.
Muylaert, K., Sabbe, K., & Vyverman, W. (2009). Changes in phytoplankton diversity and community composition along the salinity gradient of the Schelde estuary (Belgium/The Netherlands). Estuarine, Coastal and Shelf Science, 82(2), 335–340.
Navarro, P., Amouroux, D., Thanh, N. D., Rochelle-Newall, E., Ouillon, S., Arfi, R., et al. (2012). Fate and tidal transport of butyltin and mercury compounds in the waters of the tropical Bach Dang Estuary (Haiphong, Vietnam). Marine Pollution Bulletin, 64(9), 1789–1798. doi:10.1016/j.marpolbul.2012.05.036.
Nayar, S., Goh, B. P. L., & Chou, L. M. (2005a). Dynamics in the size structure of Skeletonema costatum (Greville) Cleve under conditions of reduced photosynthetically available radiation in a dredged tropical estuary. Journal of Experimental Marine Biology and Ecology, 318(2), 163–182. doi:10.1016/j.jembe.2004.12.013.
Nayar, S., Goh, B. P. L., & Chou, L. M. (2005b). Environmental impacts of diesel fuel on bacteria and phytoplankton in a tropical estuary assessed using in situ mesocosms. Ecotoxicology, 14(3), 397–412.
Nguyen, V. N., Le, T. T., Luu, X. H., Nguyen, V. T., Nguyen, C. T., & Fukuyo, Y. (2012). Recent HAB events in Halong Bay: increase in frequency and harmful effects. Paper presented at the XV International Conference on Harmful Algae Changwon, Korea, 28 October—2 November 2012
Nguyen, D.-Q., Renwick, J., & McGregor, J. (2014). Variations of surface temperature and rainfall in Vietnam from 1971 to 2010. International Journal of Climatology, 34(1), 249–264. doi:10.1002/joc.3684.
Officer, C. B., & Ryther, J. H. (1980). The possible importance of silicon in marine eutrophication. Marine Ecology: Progress Series, 3(1), 83–91. doi:10.3354/meps003083.
Ou, L. J., Wang, D., Huang, B. Q., Hong, H. S., Qi, Y. Z., & Lu, S. H. (2008). Comparative study of phosphorus strategies of three typical harmful algae in Chinese coastal waters. Journal of Plankton Research, 30(9), 1007–1017.
Paerl, H. W. (2009). Controlling eutrophication along the freshwater-marine continuum: dual nutrient (N and P) reductions are essential. Estuaries and Coasts, 32(4), 593–601. doi:10.1007/s12237-009-9158-8.
Palleyi, S., Kar, R. N., & Panda, C. R. (2008). Seasonal variability of phytoplankton population in the Brahmani Estuary of Orissa, India. Journal of Applied Science and Environmental Management, 12(3), 19–23.
Patil, J. S., & Anil, A. C. (2008). Temporal variation of diatom benthic propagules in a monsoon-influenced tropical estuary. Continental Shelf Research, 28(17), 2404–2416. doi:10.1016/j.csr.2008.06.001.
Pielou, P. C. (1975). Ecological diversity. New York: Wiley.
Redfield, A. C., Ketchum, B. H., & Richards, F. A. (1963). The influence of organisms on the composition of sea-water. In M. N. Hill (Ed.), The sea (Vol. 2, pp. 26–77). New York: Wiley.
Ricard, M. (1987). Atlas du phytoplankton marin, Diatomophycées (Vol. 2. (1–297, Paris Editions)). Paris: CNRS.
Rochelle-Newall, E. J., & Fisher, T. R. (2002). Chromophoric dissolved organic matter and dissolved organic carbon in Chesapeake Bay. Marine Chemistry, 77, 23–41.
Rochelle-Newall, E. J., Delesalle, B., Mari, X., Rouchon, C., Torréton, J. P., & Pringault, O. (2008). Zinc induces shifts in microbial carbon flux in tropical coastal environments. Aquatic Microbial Ecology, 52(1), 57–68.
Rochelle-Newall, E. J., Chu, V. T., Pringault, O., Amouroux, D., Arfi, R., Bettarel, Y., et al. (2011). Phytoplankton diversity and productivity in a highly turbid, tropical coastal system (Bach Dang Estuary, Vietnam). Marine Pollution Bulletin, 62, 2317–2329.
Rochelle-Newall, E., Hulot, F. D., Janeau, J. L., & Merroune, A. (2014). CDOM fluorescence as a proxy of DOC concentration in natural waters: a comparison of four contrasting tropical systems. Environmental Monitoring and Assessment, 186, 589–596. doi:10.1007/s10661-013-3401-2.
Shannon, C., & Weaver, W. (1963). The mathematical theory of communication: Univ. of Illinois Press.
Tas, S., Yilmaz, I. N., & Okus, E. (2009). Phytoplankton as an indicator of improving water quality in the Golden Horn Estuary. Estuaries and Coasts, 32(6), 1205–1224. doi:10.1007/s12237-009-9207-3.
Taylor, F. (1976). Dinoflagellates from the International Indian Ocean Expedition—A report on material collected by the R.V."Anton Bruun 1963–1964". Stuttgart: Schweizerbart'sche Verlagsbuchhandlung (Nägele u. Obermiller).
Tomas, C. R. (1997). Identifying marine phytoplankton. San Diego: Academic Press Harcourt Brace & Company.
Tran, D. T., & Dinh, V. H. (2004). Assessment of potentiality, utilization and management of wetland in the coastal area of Haiphong city (Project report). Haiphong, Vietnam: Institute of Marine Environment and Resources.
Tran, D. T., & Dinh, V. H. (2005). Zoning and planning for alluvial soil utilization in the coastal area of Haiphong city (Project database). Haiphong, Vietnam: Institute of Marine Environment and Resources.
Trinh, A. D., Meysman, F., Rochelle-Newall, E. J., & Bonnet, M.-P. (2012). Quantification of sediment water interactions in a polluted tropical river through biogeochemical modeling. Global Biogeochemical Cycles, 26, GB3010. doi:10.1029/2010GB003963.
Truong, N. A. (1993). Taxonomy of marine diatoms in Vietnam. Hanoi, Vietnam: Science and Technics Publishing House.
Truong, N. A., & Do, T. B. L. (1983). The occurrence of diatom Skeletonema costatum (Grev.) Cleve in the coastal waters of Haiphong. (Project Report). Haiphong, Vietnam: Institute of Marine Environment and Resources.
Vörösmarty, C. J., & Loder, T. C. (1994). Spring-neap tidal contrasts and nutrient dynamics in a marsh-dominated estuary. Estuaries, 17(3), 537–551. doi:10.2307/1352402.
Vu, T. T. (1994). Estuarine ecosystems of Vietnam. Hanoi, Vietnam: Science and Technics Publishing House.
Vu, D. V., Ouillon, S., Tran, D. T., & La, V. C. (2014). Impact of the Hoa Binh Dam (Vietnam) on water and sediment budgets in the Red River basin and delta. Hydrology and Earth System Sciences Discussions, 11(1), 333–370. doi:10.5194/hessd-11-333-2014.
Wood, E., Armstrong, F., & Richards, F. (1967). Determination of nitrate in seawater by cadmium copper reduction to nitrite. Journal of the Marine Biological Association of the United Kingdom, 47, 23–31.
Xu, S. S., Song, J. M., Li, X. G., Yuan, H. M., Li, N., Duan, L. Q., et al. (2010). Changes in nitrogen and phosphorus and their effects on phytoplankton in the Bohai Sea. Chinese Journal of Oceanology and Limnology, 28(4), 945–952. doi:10.1007/s00343-010-0005-3.
Yamagishi, T. (1992). Plankton algae in Taiwan (Formosa). Tokyo, Japan.: Uchida Rokakuho.
Acknowledgements
This work was financed by the Vietnam Academy of Science and Technology and the EC2CO project ‘HAIPHONG’, the French Institute of Research for Development (IRD), the Centre National de la Recherche Scientifique (CNRS) and the Ministry of Science and Technology of Vietnam (the MOST project on ‘Black Carbon’). We thank to the colleagues from the IMAGO Service Unit, IRD for their help with the chemical analyses. The National Hydro-Meteorological Service of Vietnam is thanked for the rainfall data. This article is dedicated to the memory of Dr. Do Trong Binh who passed away during the project.
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Chu, T.V., Torréton, JP., Mari, X. et al. Nutrient ratios and the complex structure of phytoplankton communities in a highly turbid estuary of Southeast Asia. Environ Monit Assess 186, 8555–8572 (2014). https://doi.org/10.1007/s10661-014-4024-y
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DOI: https://doi.org/10.1007/s10661-014-4024-y