Home > 2019, 38(8) > Fast acclimation of phytoplankton assemblies to acute salinity stress in the Jiulong River Estuary

Citation: Gang Li. Fast acclimation of phytoplankton assemblies to acute salinity stress in the Jiulong River Estuary. ACTA OCEANOLOGICA SINICA, 2019, 38(8): 78-85. doi: 10.1007/s13131-019-1389-3

2019, 38(8): 78-85. doi: 10.1007/s13131-019-1389-3

Fast acclimation of phytoplankton assemblies to acute salinity stress in the Jiulong River Estuary

1.  Key Laboratory of Tropical Marine Bio-resources and Ecology & Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China

Corresponding author: Gang Li, ligang@scsio.ac.cn

Received Date: 2018-05-18
Web Publishing Date: 2019-08-01

Fund Project: The National Natural Science Foundation of China under contract Nos 41890853 and 41676156; the National Basic Research Program of China (973 Program) under contract No. 2015CB452903; the Strategic Priority Research Program of Chinese Academy of Sciences under contract Nos XDA13020103 and XDA11020305; the Natural Science Foundation of Guangdong Province under contract Nos 2015A030313826 and 2017A030313216; the Special Fund for Agro-scientific Research in the Public Interest under contract No. 201403008; the Science and Technology Planning Project of Guangdong Province under contract No. 2017B030314052.

Mixing of freshwater and seawater creates the well-known salinity gradients along the estuaries. In order to investigate how phytoplankton respond to the acute salinity changes, we exposed natural phytoplankton assemblies from the Jiulong River Estuary to differential saline field water while continuously monitoring their photosynthetic performances under both indoor- and outdoor-growth conditions. When the natural cell assemblies from salinity 30 field water were exposed to series low saline field water (salinity 25, 17, 13 and 7.5), the effective Photosystem II quantum yield (ΔF/Fm′) decreased sharply, e.g., to one-fifth of its initials after 5 min exposure to salinity 7.5 field water, and then increased fast during the following 40 min and almost completely recovered after 320 min. During such an exposure process, non-photochemical quenching (NPQ) sharply increased from 0 to 0.85 within 5 min, and then decreased to nearly 0 within the following 70 min. When these cells re-acclimated to salinity 7.5 field water were exposed to series high saline field water (salinity 13, 17, 25 and 30), a similar response pattern was observed, with the decreased ΔF/Fm′ accompanied with increased NPQ, and followed by the recovery-induced increase in ΔF/Fm′ and decrease in NPQ. A similar response pattern as ΔF/Fm′ to the acute osmotic stress was also observed in the photosynthetic carbon fixation capacity according to radiocarbon (14C) incorporation. Our results indicate that estuarine phytoplankton assemblies could rapidly recover from the acute osmotic stress, implying a potential cause for their frequent blooms in coastal-estuarine waters where despite drastically varying salinity, available nutrients are abundant due to the land-derived runoffs or mixing-caused relaxations from sediments.

Key words: PSII quantum yield , carbon fixation , salinity gradients , phytoplankton assemblies , Jiulong River Estuary


Allakhverdiev S I, Nishiyama Y, Miyairi S, et al. 2002. Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis. Plant Physiology, 130(3): 1443–1453.


Armstrong F A J, Stearns C R, Strickland J D H. 1967. The measurement of upwelling and subsequent biological process by means of the Technicon Autoanalyzer? and associated equipment. Deep Sea Research and Oceanographic Abstracts, 14(3): 381–389.


Brand L E. 1984. The salinity tolerance of forty-six marine phytoplankton isolates. Estuarine, Coastal and Shelf Science, 18(5): 543–556.


Cai Aizhi, Cai Yuee, Zhu Xiaoning, et al. 1991. Diffusion and modern sedimentation of seaward-transporting discharges in the estuary of Jiulongjiang River, Fujian Province. Marine Geology & Quaternary Geology (in Chinese), 11(1): 57–67


Cao Zhenrui, Huang Bangqin, Liu Yuan, et al. 2005. Distribution characteristics of size-fractionated chlorophyll a in Xiamen waters. Journal of Oceanography in Taiwan Strait (in Chinese), 24(4): 493–501


Cao Wenzhi, Huang Zheng, Zhai Weidong, et al. 2015. Isotopic evidence on multiple sources of nitrogen in the northern Jiulong River, Southeast China. Estuarine, Coastal and Shelf Science, 163: 37–43.


Chen Baohong, Chen Changping, Chen Jinmin, et al. 2012. Variations of nutrient content and ratios and their impact on phytoplankton community in Xiamen waters. Journal of Oceanography in Taiwan Strait (in Chinese), 31(2): 246–253


Chen Baohong, Ji Weidong, Chen Jinmin, et al. 2013a. Characteristics of nutrients in the Jiulong River and its impact on Xiamen Water, China. Chinese Journal of Oceanology and Limnology, 31(5): 1055–1063.


Chen Nengwang, Peng Benrong, Hong Huasheng, et al. 2013b. Nutrient enrichment and N:P ratio decline in a coastal bay-river system in southeast China: The need for a dual nutrient (N and P) management strategy. Ocean & Coastal Management, 81: 7–13


Cloern J E. 1999. The relative importance of light and nutrient limitation of phytoplankton growth: a simple index of coastal ecosystem sensitivity to nutrient enrichment. Aquatic Ecology, 33(1): 3–15.


Domingues R B, Anselmo T P, Barbosa A B, et al. 2010. Tidal variability of phytoplankton and environmental drivers in the freshwater reaches of the Guadiana Estuary (SW Iberia). International Review of Hydrobiology, 95(4–5): 352–369.


D'ors A, Bartolomé M C, Sánchez-Fortún S. 2016. Repercussions of salinity changes and osmotic stress in marine phytoplankton species. Estuarine, Coastal and Shelf Science, 175: 169–175.


Doucette G J, King K L, Thessen A E, et al. 2008. The effect of salinity on domoic acid production by the diatom Pseudo-Nitzschia multiseries. Nova Hedwigia Beiheft, 133: 31–46


Finkel Z V, Beardall J, Flynn K J, et al. 2010. Phytoplankton in a changing world: cell size and elemental stoichiometry. Journal of Plankton Research, 32(1): 119–137.


Gao Guang, Xia Jianrong, Yu Jinlan, et al. 2018. Physiological response of a red tide alga (Skeletonema costatum) to nitrate enrichment, with special reference to inorganic carbon acquisition. Marine Environmental Research, 133: 15–23.


Genty B, Briantais J M, Baker N R. 1989. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta (BBA)-General Subjects, 990(1): 87–92.


Giacobbe M G, Oliva F D, Maimone G. 1996. Environmental factors and seasonal occurrence of the dinoflagellate Alexandrium minutum, a PSP potential producer, in a Mediterranean lagoon. Estuarine, Coastal and Shelf Science, 42(5): 539–549.


Häubner N, Sylvander P, Vuori K, et al. 2014. Abiotic stress modifies the synthesis of alpha-tocopherol and beta-carotene in phytoplankton species. Journal of Phycology, 50(4): 753–759.


Hernando M, Schloss I R, Malanga G, et al. 2015. Effects of salinity changes on coastal Antarctic phytoplankton physiology and assemblage composition. Journal of Experimental Marine Biology and Ecology, 466: 110–119.


Holm-Hansen O, Helbling E W. 1995. Técnicas para la medición de la productividad primaria en el fitoplancton. In: Alveal K, Ferrario M E, Oliveira E C, et al, eds. Manual de Métodos Ficoló-gicos. Concepción: Universidad de Concepción, 329–350


Huang Xuguang, Guo Donghui, Xiao Wupeng, et al. 2012. The relationship between quantitative changes of microplankton and population dynamics of small medusa in the Jiulong River estuary in spring of 2011. Oceanologia et Limnologia Sinica (in Chinese), 43(3): 579–583


Huang Liangmin, Jian Weijun, Song Xingyu, 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.


Li Ying, Cao Wenzhi, Su Caixia, et al. 2011a. Nutrient sources and composition of recent algal blooms and eutrophication in the northern Jiulong River, Southeast China. Marine Pollution Bulletin, 63(5–12): 249–254.


Li Gang, Gao Kunshan, Yuan Dongxing, et al. 2011b. Relationship of photosynthetic carbon fixation with environmental changes in the Jiulong River estuary of the South China Sea, with special reference to the effects of solar UV radiation. Marine Pollution Bulletin, 62(8): 1852–1858.


Li Gang, Lin Qiang, Lin Junda, et al. 2014. Environmental gradients regulate the spatial variations of phytoplankton biomass and community structure in surface water of the Pearl River estuary. Acta Ecologica Sinica, 34(2): 129–133.


Licursi M, Sierra M V, Gómez N. 2006. Diatom assemblages from a turbid coastal plain estuary: Río de la Plata (South America). Journal of Marine Systems, 62(1–2): 35–45.


Lim P T, Ogata T. 2005. Salinity effect on growth and toxin production of four tropical Alexandrium species (Dinophyceae). Toxicon, 45(6): 699–710.


Liu Guangping, Hu Jianyu, Chen Zhaozhang, et al. 2008. Distribution characteristics of sea surface salinity and its relations to tide in Jiulongjiang estuary-Xiamen Bay. Journal of Xiamen University (Natural Science) (in Chinese), 47(5): 710–713


Liu Lemian, Yang Jun, Yu Xiaoqing, et al. 2013. Patterns in the composition of microbial communities from a subtropical river: effects of environmental, spatial and temporal factors. PLoS One, 8(11): e81232.


Lu Chongming, Zhang Jianhua. 1999. Effects of salt stress on PSII function and photoinhibition in the cyanobacterium Spirulina platensis. Journal of Plant Physiology, 155(6): 740–745.


Mo Yu, Lin Lizhen, Zheng Liping, et al. 2013. Phytoplankton phosphorus stress of Jiulongjiang River-Estuary and adjacent waters system in summer. Oceanologia et Limnologia Sinica (in Chinese), 44(1): 241–248


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.


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.


Nche-Fambo F A, Scharler U M, Tirok K. 2015. Resilience of estuarine phytoplankton and their temporal variability along salinity gradients during drought and hypersalinity. Estuarine, Coastal and Shelf Science, 158: 40–52.


Pai Sucheng, Tsau Y J, Yang T I. 2001. pH and buffering capacity problems involved in the determination of ammonia in saline water using the indophenol blue spectrophotometric method. Analytica Chimica Acta, 434(2): 209–216.


Porra R J. 2002. The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynthesis Research, 73(1–3): 149–156


Radchenko I G, Il’iash L V. 2006. Growth and photosynthetic activity of diatom Thalassiosira weissflogii at decreasing salinity. Izvestiia Akademii Nauk. Seriia Biologicheskaia, (3): 306–313


Raven J A. 1998. The twelfth tansley lecture, small is beautiful: the picophytoplankton. Functional Ecology, 12(4): 503–513.


Rijstenbil J W, Mur L R, Wijnholds J J, et al. 1989a. Impact of a temporal salinity decrease on growth and nitrogen metabolism of the marine diatom Skeletonema costatum in continuous cultures. Marine Biology, 101(1): 121–129.


Rijstenbil J W, Wijnholds J A, Sinke J J. 1989b. Implications of salinity fluctuation for growth and nitrogen metabolism of the marine diatom Ditylum brightwellii in comparison with Skeletonema costatum. Marine Biology, 101(1): 131–141.


Tang Rongkun, He Qing, Ji Weidong, et al. 2010. Characteristics of temporal and spatial variations in chlorophyll contents of waters around Xiamen Island in 2005~2007. Journal of Oceanography in Taiwan Strait (in Chinese), 29(3): 342–351


Thessen A E, Dortch Q, Parsons M L, et al. 2005. Effect of salinity on Pseudo-Nitzschia species (Bacillariophyceae) growth and distribution. Journal of Phycology, 41(1): 21–49.


Tian Yongqiang, Huang Bangqin, Yu Chaochao, et al. 2014. Dynamics of phytoplankton communities in the Jiangdong Reservoir of Jiulong River, Fujian, South China. Chinese Journal of Oceanology and Limnology, 32(2): 255–265.


Van Kooten O, Snel J F H. 1990. The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynthesis Research, 25(3): 147–150.


Villafañe V, Reid F. 1995. Métodos de microscopía para la cuanti-ficación del fitoplancton. In: Alveal K, Ferrario M E, Oliveira E C, et al., eds. Manual de Métodos Ficológicos. Concepción: Universidad de Concepción, 169–185


Wang Jia, Hong Huasheng, Zhou Lumin, et al. 2013. Numerical modeling of hydrodynamic changes due to coastal reclamation projects in Xiamen Bay, China. Chinese Journal of Oceanology and Limnology, 31(2): 334–344.


Wang Weiqiang, Huang Shanggao, Gu Deyu, et al. 1986. Mixing characters of fresh water with sea water in the Jiulong Jiang estuary, Fujian. Journal of Oceanography in Taiwan Strait (in Chinese), 5(1): 10–17


Wang Yongming, Liu Lemian, Chen Huihuang, et al. 2015b. Spatiotemporal dynamics and determinants of planktonic bacterial and microeukaryotic communities in a Chinese subtropical river. Applied Microbiology and Biotechnology, 99(21): 9255–9266.


Wang Guizhi, Wang Zhangyong, Zhai Weidong, et al. 2015a. Net subterranean estuarine export fluxes of dissolved inorganic C, N, P, Si, and total alkalinity into the Jiulong River estuary, China. Geochimica et Cosmochimica Acta, 149: 103–114.


Wood E D, Armstrong F A J, Richards F A. 1967. Determination of nitrate in sea water by cadmium-copper reduction to nitrite. Journal of the Marine Biological Association of the United Kingdom, 47(1): 23–31.


Wu Gaojie, Cao Wenzhi, Huang Zheng, et al. 2017. Decadal changes in nutrient fluxes and environmental effects in the Jiulong River Estuary. Marine Pollution Bulletin, 124(2): 871–877.


Yan Xiuli, Zhai Weidong, Hong Huasheng, et al. 2012. Distribution, fluxes and decadal changes of nutrients in the Jiulong River Estuary, Southwest Taiwan Strait. Chinese Science Bulletin, 57(18): 2307–2318.


Yi Rong, Tan Yehui, Wang Shengfu, et al. 2014. Cell size dependent responses of phytoplankton assemblages to nitrate and phosphate additions in surface waters of the northern South China Sea. Open Journal of Marine Science, 4(2): 44564


Yin Kedong, Qian Peiyuan, Wu M C S, et al. 2001. Shift from P to N limitation of phytoplankton growth across the Pearl River estuarine plume during summer. Marine Ecology Progress Series, 221: 17–28.


Zhang Shuting, Lv Lu, Zhang Yongli, et al. 2013. Occurrence and variations of five classes of antibiotic resistance genes along the Jiulong River in southeast China. Journal of Environmental Biology, 34: 345–351


Hin Lee LEE, Fredolin TANGANG, Jacqueline Isabella GISEN, Saim SURATMAN. Prediction of salinity intrusion in the sheltered estuary of Terengganu River in Malaysia using 1-D empirical intrusion model. ACTA OCEANOLOGICA SINICA, 2017, 36(5): 57-66. doi: 10.1007/s13131-017-1060-9


Shuqun SONG, Zhao LI, Caiwen LI, Zhiming YU. The response of spring phytoplankton assemblage to diluted water and upwelling in the eutrophic Changjiang (Yangtze River) Estuary. ACTA OCEANOLOGICA SINICA, 2017, 36(12): 101-110. doi: 10.1007/s13131-017-1094-z


Lei WANG, Hao HUANG, Lina AN, Hikmah THOHA, Chuiwei BONG, Wupeng XIAO, Haifeng GU. Comparison of photosynthetic pigments and phytoplankton assemblages in two types of coastal regions in Southeast Asia-Indonesian Throughflow and river estuary. ACTA OCEANOLOGICA SINICA, 2018, 37(12): 18-27. doi: 10.1007/s13131-018-1284-3


Zengjie JIANG, Meirong DU, Jinghui FANG, Yaping GAO, Jiaqi LI, Li ZHAO, Jianguang FANG. Size fraction of phytoplankton and the contribution of natural plankton to the carbon source of Zhikong scallop Chlamysfarreri in mariculture ecosystem of the Sanggou Bay. ACTA OCEANOLOGICA SINICA, 2017, 36(10): 97-105. doi: 10.1007/s13131-017-0970-x


Li LI, Jingyi CEN, Lei CUI, Songhui LU. Response of size-fractionated phytoplankton to environmental factors near the Changjiang Estuary. ACTA OCEANOLOGICA SINICA, 2019, 38(1): 151-159. doi: 10.1007/s13131-018-1259-4


Tao Jiang, Hongbo Liu, Honghui Huang, Jian Yang. Migration patterns and habitat use of the tapertail anchovy Coilia mystus in the Oujiang River Estuary and the Zhujiang River Estuary, China. ACTA OCEANOLOGICA SINICA, 2019, 38(8): 35-40. doi: 10.1007/s13131-019-1436-0


Chenglong WANG, Yifei ZHAO, Xinqing ZOU, Xinwanghao XU, Chendong GE. Recent changing patterns of the Changjiang (Yangtze River) Estuary caused by human activities. ACTA OCEANOLOGICA SINICA, 2017, 36(4): 87-96. doi: 10.1007/s13131-017-1017-z


Shengle YIN, Peng TAN, Chao YUAN, Jin HU, Xiaoshou LIU. Seasonal dynamics of meiofaunal distribution in the Dagu River Estuary, Jiaozhou Bay, China. ACTA OCEANOLOGICA SINICA, 2017, 36(12): 79-86. doi: 10.1007/s13131-017-1093-0


Xirong Chen, Zhenyu Sun, Hongyang Lin, Jia Zhu, Jianyu Hu. Analysis of temperature inversion in the Zhujiang River Estuary in July 2015. ACTA OCEANOLOGICA SINICA, 2019, 38(4): 167-174. doi: 10.1007/s13131-019-1420-8


Yong SHI, Zhishuai LIU, Jianhua GAO, Yang YANG, Yaping WANG. The response of sedimentary record to catchment changesinduced by human activities in the western intertidal flat ofYalu River Estuary, China. ACTA OCEANOLOGICA SINICA, 2017, 36(4): 54-63. doi: 10.1007/s13131-016-0941-7


Tao LIU, Yancheng TAO, Ying LIU. Mangrove swamp expansion controlled by climate since 1988: a case study in the Nanliu River Estuary, Guangxi, Southwest China. ACTA OCEANOLOGICA SINICA, 2017, 36(12): 11-17. doi: 10.1007/s13131-017-1097-9


Dong LIU, Yan BAI, Xianqiang HE, Delu PAN, Difeng WANG, Ji'an WEI, Lin ZHANG. The dynamic observation of dissolved organic matter in the Zhujiang (Pearl River) Estuary in China from space. ACTA OCEANOLOGICA SINICA, 2018, 37(7): 91-103. doi: 10.1007/s13131-017-1248-7


Suying OU, Qingshu YANG, Xiangxin LUO, Fan ZHU, Kaiwen LUO, Hao YANG. The influence of runoff and wind on the dispersion patterns of suspended sediment in the Zhujiang (Pearl) River Estuary based on MODIS data. ACTA OCEANOLOGICA SINICA, 2019, 38(3): 26-35. doi: 10.1007/s13131-019-1396-4


Guangping LIU, Shuqun CAI. Modeling of suspended sediment by coupled wave-current model in the Zhujiang (Pearl) River Estuary. ACTA OCEANOLOGICA SINICA, 2019, 38(7): 22-35. doi: 10.1007/s13131-019-1455-3


Yabin HU, Jie ZHANG, Yi Ma, Xiaomin LI, Qinpei SUN, Jubai AN. Deep learning classification of coastal wetland hyperspectral image combined spectra and texture features: A case study of Huanghe (Yellow) River Estuary wetland. ACTA OCEANOLOGICA SINICA, 2019, 38(5): 142-150. doi: 10.1007/s13131-019-1445-z


Ping ZHU, Hui WU. Origins and transports of the low-salinity coastal water in the southwestern Yellow Sea. ACTA OCEANOLOGICA SINICA, 2018, 37(4): 1-11. doi: 10.1007/s13131-018-1200-x


Jian CHEN, Xiaobao YOU, Yiguo XIAO, Ren ZHANG, Gongjie WANG, Senliang BAO. A performance evaluation of remotely sensed sea surface salinity products in combination with other surface measurements in reconstructing three-dimensional salinity fields. ACTA OCEANOLOGICA SINICA, 2017, 36(7): 15-31. doi: 10.1007/s13131-017-1079-y


Zhengquan ZHOU, Xiaojing LI, Linlin CHEN, Baoquan LI, Tiantian LIU, Binghua AI, Lufei YANG, Bo LIU, Qiao CHEN. Macrobenthic assemblage characteristics under stressed waters and ecological health assessment using AMBI and M-AMBI: a case study at the Xin’an River Estuary, Yantai, China. ACTA OCEANOLOGICA SINICA, 2018, 37(5): 77-86. doi: 10.1007/s13131-018-1180-x


Xiangfu LI, Jie XU, Zhen SHI, Qian LI, Ruihuan LI. Variability in the empirical leucine-to-carbon conversion factors along an environmental gradient. ACTA OCEANOLOGICA SINICA, 2018, 37(4): 77-82. doi: 10.1007/s13131-018-1144-1


Shunyang CHEN, Bin CHEN, Pramudji SASTROSUWONDO, I Wayan Eka DHARMAWAN, Danyun OU, Xijie YIN, Weiwei YU, Guangcheng CHEN. Ecosystem carbon stock of a tropical mangrove forest in North Sulawesi, Indonesia. ACTA OCEANOLOGICA SINICA, 2018, 37(12): 85-91. doi: 10.1007/s13131-018-1290-5

  • PDF Downloads()
  • Abstract Views()
  • HTML Views()

Figures And Tables

Fast acclimation of phytoplankton assemblies to acute salinity stress in the Jiulong River Estuary

Gang Li