Effects of daily nitrogen and phosphorus input on planktonic community metabolism in a semi-enclosed bay by mesocosm experiment

Chenhui Xiang Yao Li Zhixin Ke Gang Li Yadong Huang Xinying Su Liangmin Huang Xinyu Song

Chenhui Xiang, Yao Li, Zhixin Ke, Gang Li, Yadong Huang, Xinying Su, Liangmin Huang, Xinyu Song. Effects of daily nitrogen and phosphorus input on planktonic community metabolism in a semi-enclosed bay by mesocosm experiment[J]. Acta Oceanologica Sinica, 2022, 41(8): 99-110. doi: 10.1007/s13131-022-1986-4
Citation: Chenhui Xiang, Yao Li, Zhixin Ke, Gang Li, Yadong Huang, Xinying Su, Liangmin Huang, Xinyu Song. Effects of daily nitrogen and phosphorus input on planktonic community metabolism in a semi-enclosed bay by mesocosm experiment[J]. Acta Oceanologica Sinica, 2022, 41(8): 99-110. doi: 10.1007/s13131-022-1986-4

doi: 10.1007/s13131-022-1986-4

Effects of daily nitrogen and phosphorus input on planktonic community metabolism in a semi-enclosed bay by mesocosm experiment

Funds: the National Natural Science Foundation of China under contract No. 41890853; the Fund of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) under contract No. GML2019ZD0404; the Science & Technology Basic Resources Investigation Program of China under contract No. 2018FY100105; the Fund of Innovation Academy of South China Sea Ecology and Environmental Engineering, Chinese Academy of Sciences under contract No. ISEE2018ZD02; the National Key Basic Research Program of China (973 Program) under contract No. 2015CB452904; the Development Project of China under contract Nos 2017YFC0506302 and 2016YFC0502805.
More Information
    • 关键词:
    •  / 
    •  / 
    •  / 
    •  / 
    •  / 
    •  
  • Figure  1.  Location of the Daya Bay and mesocosms site (▲).

    Figure  2.  Changes of environmental conditions in the mesocosms (vertical bars indicate the standard deviations from triplicate pools of each mesocosms, n=3). The implications of the figure legends are listed in Table 1.

    Figure  3.  Changes of planktonic metabolism of gross primary production (GPP, a), community respiration (CR, b) and net community production (NCP, c) in the mesocosms (vertical bars indicate the standard deviations from triplicate pools of each mesocosms, n=3). The implications of the figure legends are listed in Table 1.

    Figure  4.  Changes of total chlorophyll a (Chl a) concentration (a), micro-phytoplankton total abundance (b), Shannon-Wiener diversity index (c), and relative abundance of Rhizosolenia sinensis (d) in the mesocosms (vertical bars indicate the standard deviations from triplicate pools of each mesocosms, n=3). The implications of the figure legends are listed in Table 1.

    Figure  5.  Changes of Euk (a), Syn (b) and HBA (c) abundance in the mesocosms (vertical bars indicate the standard deviations from triplicate pools of each mesocosms, n=3). The implications of the figure legends are listed in Table 1.

    Figure  6.  Comparison of the ecological responses to nutrient input of different concentrations (different lowercase, a to e, indicate statistically significant differences between treatments at p<0.05; vertical bars indicate the standard deviations from triplicate pools of each mesocosms; data from the D0−D5 period). The implications of the subscripts are listed in Table 1.

    Table  1.   Concentrations of nutrient enrichments of each treatment

    TreatmentsKNO3-N/(μmol·L−1·d−1)NaH2PO4-P/(μmol·L−1·d−1)
    Control00.000
    N1+P1/3010.033
    N2+P2/3020.066
    N4+P4/3040.132
    N8+P8/3080.264
    N16+P16/30160.528
    Note: Subscript represents preset molar concentration of KNO3 and NaH2PO4.
    下载: 导出CSV

    Table  2.   Chlorophyll a size structure in the mesocosms after the 10 d incubation

    TreatmentsMicro/%Nano/%Pico/%<20 μm/%
    Control12.72±8.0329.04±7.8458.24±14.7587.28±8.03
    N1+P1/3017.18±8.8141.16±4.0641.66±7.6382.82±8.81
    N2+P2/305.47±1.9547.55±13.8646.98±12.3794.53±1.95
    N4+P4/302.65±1.6630.33±12.6767.02±14.2997.35±1.66
    N8+P8/308.89±4.5147.82±3.3543.28±1.9891.11±4.51
    N16+P16/3010.15±3.4543.25±9.5846.6±9.0589.85±3.45
    Note: The implications of the subscripts are listed in Table 1.
    下载: 导出CSV

    Table  3.   Pearson’s correlations between the net community production (NCP), the gross primary production (GPP) and the community respiration (CR)

    TreatmentGPP and NCPCR and NCP
    Control0.898**0.011
    N1+P1/300.707*−0.474
    N2+P2/30−0.092−0.801*
    N4+P4/300.263−0.666*
    N8+P8/300.464−0.694*
    N16+P16/300.525−0.358
    Note: Asterisks represent the level of significance: *p<0.05, **p<0.01.The implications of the subscripts are listed in Table 1.
    下载: 导出CSV

    Table  4.   Dissolved nitrogen (N) and phosphorus (P) fluxes from major rivers and sewage outlets in the Daya Bay

    Water regionPeriodDaily input/
    μmol·(L·d)−1
    Reference
    NP
    Aotou Coveyearly2.8450.051Huang et al. (2019)
    wet season4.450.080 Huang et al. (2019)
    Whole Daya Bayyearly0.1090.002 Huang et al. (2019)
    Note: The water volume of the Daya Bay is 6.6 km3 (600 km2×11 m), and that of Aotou Cove is 0.195 km3 (39 km2×5 m).
    下载: 导出CSV
  • [1] Adolf J E, Stoecker D K, Harding L W Jr. 2006. The balance of autotrophy and heterotrophy during mixotrophic growth of Karlodinium micrum (Dinophyceae). Journal of Plankton Research, 28(8): 737–751. doi: 10.1093/plankt/fbl007
    [2] Agustí S, Satta M P, Mura M P. 2004. Summer community respiration and pelagic metabolism in upper surface Antarctic waters. Aquatic Microbial Ecology, 35(2): 197–205. doi: 10.3354/ame035197
    [3] Agusti S, Vigoya L, Duarte C M. 2018. Annual plankton community metabolism in estuarine and coastal waters in Perth (Western Australia). PeerJ, 6: e5081. doi: 10.7717/peerj.5081
    [4] Arbones B, Castro C G, Alonso-Pérez F, et al. 2008. Phytoplankton size structure and water column metabolic balance in a coastal upwelling system: the Ría de Vigo, NW Iberia. Aquatic Microbial Ecology, 50(2): 169–179. doi: 10.3354/ame01160
    [5] Boesch D F. 2002. Challenges and opportunities for science in reducing nutrient over-enrichment of coastal ecosystems. Estuaries, 25(4): 886–900. doi: 10.1007/BF02804914
    [6] Brussaard C P D, Mari X, Van Bleijswijk J D L, et al. 2005. A mesocosm study of Phaeocystis globosa (Prymnesiophyceae) population dynamics: II. Significance for the microbial community. Harmful Algae, 4(5): 875–893. doi: 10.1016/j.hal.2004.12.012
    [7] Caffrey J M, Murrell M C, Amacker K S, et al. 2014. Seasonal and inter-annual patterns in primary production, respiration, and net ecosystem metabolism in three estuaries in the northeast gulf of Mexico. Estuaries and Coasts, 37(S1): S222–S241. doi: 10.1007/s12237-013-9701-5
    [8] Cai Weijun. 2011. Estuarine and coastal ocean carbon paradox: CO2 sinks or sites of terrestrial carbon incineration?. Annual Review of Marine Science, 3: 123–145,
    [9] Chen Chen-Tung Arthur, Borges A V. 2009. Reconciling opposing views on carbon cycling in the coastal ocean: continental shelves as sinks and near-shore ecosystems as sources of atmospheric CO2. Deep-Sea Research Part II: Topical Studies in Oceanography, 56(8−10): 578–590. doi: 10.1016/j.dsr2.2009.01.001
    [10] Conley D J, Markager S, Andersen J, et al. 2002. Coastal eutrophication and the Danish national aquatic monitoring and assessment program. Estuaries, 25(4): 848–861. doi: 10.1007/BF02804910
    [11] Cotovicz Jr L C, Knoppers B A, Brandini N, et al. 2015. A strong CO2 sink enhanced by eutrophication in a tropical coastal embayment (Guanabara Bay, Rio de Janeiro, Brazil). Biogeosciences, 12(20): 6125–6146. doi: 10.5194/bg-12-6125-2015
    [12] Davis J C. 1975. Minimal dissolved oxygen requirements of aquatic life with emphasis on Canadian species: a review. Journal of the Fisheries Research Board of Canada, 32(12): 2295–2332. doi: 10.1139/f75-268
    [13] del Giorgio P A, Duarte C M. 2002. Respiration in the open ocean. Nature, 420(6914): 379–384. doi: 10.1038/nature01165
    [14] del Giorgio P A, Peters R H. 1994. Patterns in planktonic P: R ratios in lakes: Influence of lake trophy and dissolved organic carbon. Limnology and Oceanography, 39: 772–87. doi: 10.4319/lo.1994.39.4.0772
    [15] del Giorgio P A, Williams P J L B. 2005. Respiration in Aquatic Ecosystems. New York: Oxford University Press
    [16] Dodds W K, Cole J J. 2007. Expanding the concept of trophic state in aquatic ecosystems: it’s not just the autotrophs. Aquatic Sciences, 69(4): 427–439. doi: 10.1007/s00027-007-0922-1
    [17] Dodds W K, Johnson K R, Priscu J C. 1989. Simultaneous nitrogen and phosphorus deficiency in natural phytoplankton assemblages: theory, empirical evidence, and implications for lake management. Lake and Reservoir Management, 5(1): 21–26. doi: 10.1080/07438148909354677
    [18] Duarte C M, Agustí S, Vaqué D. 2004. Controls on planktonic metabolism in the Bay of Blanes, northwestern Mediterranean littoral. Limnology and Oceanography, 49(6): 2162–2170. doi: 10.4319/lo.2004.49.6.2162
    [19] Duarte C M, Regaudie-de-Gioux A. 2009. Thresholds of gross primary production for the metabolic balance of marine planktonic communities. Limnology and Oceanography, 54(3): 1015–1022. doi: 10.4319/lo.2009.54.3.1015
    [20] Duarte C M, Regaudie-de-Gioux A, Arrieta J M, et al. 2013. The oligotrophic ocean is heterotrophic. Annual Review of Marine Science, 5: 551–569. doi: 10.1146/annurev-marine-121211-172337
    [21] Ducklow H W, Doney S C. 2013. What is the metabolic state of the oligotrophic ocean? A debate. The Annual Review of Marine Science, 5: 525–533. doi: 10.1146/annurev-marine-121211-172331
    [22] Ferreira V, Elosegi A, Tiegs S D, et al. 2020. Organic matter decomposition and ecosystem metabolism as tools to assess the functional integrity of streams and rivers—a systematic review. Water, 12(12): 3523. doi: 10.3390/w12123523
    [23] Finkel Z V, Irwin A J, Schofield O. 2004. Resource limitation alters the 3/4 size scaling of metabolic rates in phytoplankton. Marine Ecology Progress Series, 273: 269–279. doi: 10.3354/meps273269
    [24] Ganf G G, Viner A B. 1973. Ecological stability in a shallow equatorial lake (Lake George, Uganda). Proceedings of the Royal Society B: Biological Sciences, 184(1076): 321–346. doi: 10.1098/rspb.1973.0051
    [25] Grasshoff K, Ehrhardt M, Kremling K, 1983. Methods of Seawater Analysis. 2nd ed. Weinheim: Verlag Chemie
    [26] Huang Xiaoping, Huang Liangmin, Song Jinming, et al. 2019. Process and Mechanism of Nutrient Inputs on Bay Ecological Environment (in Chinese). Beijing: Science Press
    [27] Huang Bangqin, Lan Wenlu, Cao Zhenrui, et al. 2008. Spatial and temporal distribution of nanoflagellates in the northern South China Sea. Hydrobiologia, 605(1): 143–157. doi: 10.1007/s10750-008-9330-3
    [28] Huete-Stauffer T M, Morán X A G. 2012. Dynamics of heterotrophic bacteria in temperate coastal waters: similar net growth but different controls in low and high nucleic acid cells. Aquatic Microbial Ecology, 67(3): 211–223. doi: 10.3354/ame01590
    [29] Jiang Tao, Chen Feiyu, Yu Zonghe, et al. 2016. Size-dependent depletion and community disturbance of phytoplankton under intensive oyster mariculture based on HPLC pigment analysis in Daya Bay, South China Sea. Environmental Pollution, 219: 804–814. doi: 10.1016/j.envpol.2016.07.058
    [30] Jiang Xin, Li Jiajun, Ke Zhixin, et al. 2017. Characteristics of picoplankton abundances during a Thalassiosira diporocyclus bloom in the Taiwan Bank in late winter. Marine Pollution Bulletin, 117(1−2): 66–74. doi: 10.1016/j.marpolbul.2017.01.042
    [31] Joint I, Henriksen P, Fonnes G A, et al. 2002. Competition for inorganic nutrients between phytoplankton and bacterioplankton in nutrient manipulated mesocosms. Aquatic Microbial Ecology, 29(2): 145–159. doi: 10.3354/ame029145
    [32] Ke Zhixin, Tan Yehui, Huang Liangmin, et al. 2019. Significantly depleted 15N in suspended particulate organic matter indicating a strong influence of sewage loading in Daya Bay, China. Science of the Total Environment, 650: 759–768. doi: 10.1016/j.scitotenv.2018.09.076
    [33] Kemp W M, Smith E M, Marvin-DiPasquale M, et al. 1997. Organic carbon balance and net ecosystem metabolism in Chesapeake Bay. Marine Ecology Progress Series, 150: 229–248. doi: 10.3354/meps150229
    [34] Krause-Jensen D, Markager S, Dalsgaard T. 2012. Benthic and pelagic primary production in different nutrient regimes. Estuaries and Coasts, 35(2): 527–545. doi: 10.1007/s12237-011-9443-1
    [35] Lagaria A, Psarra S, Lefèvre D, et al. 2011. The effects of nutrient additions on particulate and dissolved primary production and metabolic state in surface waters of three Mediterranean eddies. Biogeosciences, 8(9): 2595–2607. doi: 10.5194/bg-8-2595-2011
    [36] Li Yao, Xiang Chenhui, Jiang Zhijian, et al. 2021. Production and metabolism characteristics of planktonic community and their influencing factors in Daya Bay during summer. Journal of Tropical Oceanography, 40(6): 83–92
    [37] Liu Huaxue, Hu Zifeng, Huang Liangmin, et al. 2013. Biological response to typhoon in northern South China Sea: A case study of “Koppu”. Continental Shelf Research, 68: 123–132. doi: 10.1016/j.csr.2013.08.009
    [38] López-Sandoval D C, Rowe K, Carillo-de-Albonoz P, et al. 2019. Rates and drivers of Red Sea plankton community metabolism. Biogeosciences, 16(15): 2983–2995. doi: 10.5194/bg-16-2983-2019
    [39] Malone T C. 1991. River flow, phytoplankton production and oxygen depletion in Chesapeake Bay. Geological Society, London, Special Publications, 58(1): 83–93
    [40] Malone T, Azzaro M, Bode A, et al. 2015. Chapter 6: primary production, cycling of nutrients, surface layer and plankton. In: Nations U, ed. First Global Integrated Marine Assessment, Also Known as the First World Ocean Assessment: World Ocean Assessment I. Cambridge: Cambridge University Press, 119–148
    [41] Marañón E. 2015. Cell size as a key determinant of phytoplankton metabolism and community structure. Annual Review of Marine Science, 7(1): 241–264. doi: 10.1146/annurev-marine-010814-015955
    [42] Morel F M M. 1987. Kinetics of nutrient uptake and growth in phytoplankton. Journal of Phycology, 23(2): 137–150. doi: 10.1111/j.1529-8817.1987.tb04436.x
    [43] Nixon S W, Buckley B A, Granger S L, et al. 2008. Nitrogen and phosphorus inputs to narragansett bay: past, present, and future. In: Desbonnet A, Costa-Pierce B A, eds. Science for Ecosystem-Based Management. New York: Springer, 101–175
    [44] Parsons T R, Maita Y, Lalli C M. 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Oxford: Pergamon Press
    [45] Qiu Dajun, Huang Liangmin, Zhang Jianlin, et al. 2010. Phytoplankton dynamics in and near the highly eutrophic Pearl River Estuary, South China Sea. Continental Shelf Research, 30(2): 177–186. doi: 10.1016/j.csr.2009.10.015
    [46] Rochelle-Newall E J, Winter C, Barrón C, et al. 2007. Artificial neural network analysis of factors controlling ecosystem metabolism in coastal systems. Ecological Applications, 17(S5): S185–S196. doi: 10.1890/05-1769.1
    [47] Scheffer M, Carpenter S, Foley J A, et al. 2001. Catastrophic shifts in ecosystems. Nature, 413(6856): 591–596. doi: 10.1038/35098000
    [48] Serret P, Fernández E, Sostres J A, et al. 1999. Seasonal compensation of microbial production and respiration in a temperate sea. Marine Ecology Progress Series, 187: 43–57. doi: 10.3354/meps187043
    [49] Serret P, Robinson C, Aranguren-Gassis M, et al. 2015. Both respiration and photosynthesis determine the scaling of plankton metabolism in the oligotrophic ocean. Nature Communications, 6: 6961. doi: 10.1038/ncomms7961
    [50] Smith E M, Kemp W M. 2003. Planktonic and bacterial respiration along an estuarine gradient: responses to carbon and nutrient enrichment. Aquatic Microbial Ecology, 30(3): 251–261. doi: 10.3354/ame030251
    [51] Smith S V, Mackenzie F T. 1987. The ocean as a net heterotrophic system: implications From the carbon biogeochemical cycle. Global Biogeochemical Cycles, 1(3): 187–198. doi: 10.1029/GB001i003p00187
    [52] Sommer U, Lewandowska A. 2011. Climate change and the phytoplankton spring bloom: warming and overwintering zooplankton have similar effects on phytoplankton. Global Change Biology, 17(1): 154–162. doi: 10.1111/j.1365-2486.2010.02182.x
    [53] Song Xingyu, Huang Liangmin, Zhang Jianlin, et al. 2004. Variation of phytoplankton biomass and primary production in Daya Bay during spring and summer. Marine Pollution Bulletin, 49(11−12): 1036–1044. doi: 10.1016/j.marpolbul.2004.07.008
    [54] Song Xingyu, Huang Liangmin, Zhang Jianlin, et al. 2009. Harmful algal blooms (HABs) in Daya Bay, China: an in situ study of primary production and environmental impacts. Marine Pollution Bulletin, 58(9): 1310–1318. doi: 10.1016/j.marpolbul.2009.04.030
    [55] Song Xingyu, Liu Huaxue, Zhong Yu, et al. 2015. Bacterial growth efficiency in a partly eutrophicated bay of South China Sea: implication for anthropogenic impacts and potential hypoxia events. Ecotoxicology, 24(7−8): 1529–1539. doi: 10.1007/s10646-015-1497-6
    [56] Song Xingyu, Tan Meiting, Xu Ge, et al. 2019. Is phosphorus a limiting factor to regulate the growth of phytoplankton in Daya Bay, northern South China Sea: a mesocosm experiment. Ecotoxicology, 28(5): 559–568. doi: 10.1007/s10646-019-02049-7
    [57] Stange P, Bach L T, Le Moigne F A C, et al. 2017. Quantifying the time lag between organic matter production and export in the surface ocean: implications for estimates of export efficiency. Geophysical Research Letters, 44(1): 268–276. doi: 10.1002/2016GL070875
    [58] Strayer D. 1988. On the limits to secondary production. Limnology and Oceanography, 33(5): 1217–1220. doi: 10.4319/lo.1988.33.5.1217
    [59] Sun Cuici, Wang Youshao, Sun Song, et al. 2006. Dynamic analysis of phytoplankton community characteristics in Daya Bay, China. Acta Ecologica Sinica, 26(12): 3948–3958. doi: 10.1016/S1872-2032(07)60005-5
    [60] Sun Cuici, Wang Youshao, Wu Meilin, et al. 2011. Seasonal variation of water quality and phytoplankton response patterns in Daya Bay, China. International Journal of Environmental Research and Public Health, 8(7): 2951–2966. doi: 10.3390/ijerph8072951
    [61] USEPA. 2000. Ambient Water Quality Criteria for Dissolved Oxygen (Saltwater): Cape Cod to Cape Hatteras. Washington: United States Environmental Protection Agency, 44
    [62] Utermöhl H. 1958. Methods of collecting plankton for various purposes are discussed. SIL Communications, 9(1): 1–38
    [63] Vázquez-Domínguez E, Vaqué D, Gasol J M. 2007. Ocean warming enhances respiration and carbon demand of coastal microbial plankton. Global Change Biology, 13(7): 1327–1334. doi: 10.1111/j.1365-2486.2007.01377.x
    [64] Vidussi F, Mostajir B, Fouilland E, et al. 2011. Effects of experimental warming and increased ultraviolet B radiation on the Mediterranean plankton food web. Limnology and Oceanography, 56(1): 206–218. doi: 10.4319/lo.2011.56.1.0206
    [65] Wang Youshao, Lou Zhiping, Sun Cuici, et al. 2008. Ecological environment changes in Daya Bay, China, from 1982 to 2004. Marine Pollution Bulletin, 56(11): 1871–1879. doi: 10.1016/j.marpolbul.2008.07.017
    [66] Wang Zhaohui, Zhao Jiangang, Zhang Yujuan, et al. 2009. Phytoplankton community structure and environmental parameters in aquaculture areas of Daya Bay, South China Sea. Journal of Environmental Sciences, 21(9): 1268–1275. doi: 10.1016/S1001-0742(08)62414-6
    [67] Watson S B, Zastepa A, Boyer G L, et al. 2017. Algal bloom response and risk management: on-site response tools. Toxicon, 129: 144–152. doi: 10.1016/j.toxicon.2017.02.005
    [68] Williams P J L B, Quay P D, Westberry T K, et al. 2013. The oligotrophic ocean is autotrophic. Annual Review of Marine Science, 5: 535–549. doi: 10.1146/annurev-marine-121211-172335
    [69] Wilson J, Abboud S, Beman J M. 2017. Primary production, community respiration, and net community production along oxygen and nutrient gradients: environmental controls and biogeochemical feedbacks within and across “marine lakes”. Frontiers in Marine Science, 4: 12. doi: 10.3389/fmars.2017.00012
    [70] Wiltshire K H, Malzahn A M, Wirtz K, et al. 2008. Resilience of North Sea phytoplankton spring bloom dynamics: an analysis of long-term data at Helgoland Roads. Limnology and Oceanography, 53(4): 1294–1302. doi: 10.4319/lo.2008.53.4.1294
    [71] Wu Meilin, Wang Youshao. 2007. Using chemometrics to evaluate anthropogenic effects in Daya Bay, China. Estuarine, Coastal and Shelf Science, 72(4): 732–742,
    [72] Wu Meilin, Wang Yutu, Cheng Hao, et al. 2020. Phytoplankton community, structure and succession delineated by partial least square regression in Daya Bay, South China Sea. Ecotoxicology, 29(6): 751–761. doi: 10.1007/s10646-020-02188-2
    [73] Wu Meilin, Wang Youshao, Wang Yutu, et al. 2017. Scenarios of nutrient alterations and responses of phytoplankton in a changing Daya Bay, South China Sea. Journal of Marine Systems, 165: 1–12. doi: 10.1016/j.jmarsys.2016.09.004
    [74] Xiang Chenhui, Tan Yehui, Zhang Huangchen, et al. 2019. The key to dinoflagellate (Noctiluca scintillans) blooming and outcompeting diatoms in winter off Pakistan, northern Arabian Sea. Science of the Total Environment, 694: 133396. doi: 10.1016/j.scitotenv.2019.07.202
    [75] Xie Fuwu, Song Xingyu, Tan Yehui, et al. 2019. Impact of simulated warming and nutrients input on plankton community metabolism in Daya Bay. Journal of Tropical Oceanography, 38(2): 48–57
    [76] Yang Xi, Tan Yehui, Li Kaizhi, et al. 2020. Long-term changes in summer phytoplankton communities and their influencing factors in Daya Bay, China (1991−2017). Marine Pollution Bulletin, 161: 111694. doi: 10.1016/j.marpolbul.2020.111694
    [77] Yin Kedong, Song Xiuxian, Liu Sheng, et al. 2008. Is inorganic nutrient enrichment a driving force for the formation of red tides? A case study of the dinoflagellate Scrippsiella trochoidea in an embayment. Harmful Algae, 8(1): 54–59. doi: 10.1016/j.hal.2008.08.004
    [78] Yu Jing, Tang Danling, Oh I S, et al. 2007. Response of harmful algal blooms to environmental changes in Daya Bay, China. Terrestrial Atmospheric and Oceanic Sciences, 18(5): 1011–1027. doi: 10.3319/TAO.2007.18.5.1011(Oc
    [79] Zhang Xia, Shi Zhen, Huang Xiaoping, et al. 2017. Abiotic and biotic factors influencing nanoflagellate abundance and distribution in three different seasons in PRE, South China Sea. Continental Shelf Research, 143: 1–8. doi: 10.1016/j.csr.2017.05.012
    [80] Zhao Xiufeng, Yang Weifeng, Ma Haoyang, et al. 2019. Seasonal variations in the abundance and sinking flux of biogenic silica in Daya Bay, northern South China Sea. Oceanologia, 61(2): 239–251. doi: 10.1016/j.oceano.2018.11.003
    [81] Zhu Aijia, Huang Liangmin, Xu Zhanzhou. 2008. Impacts of nitrogen and phosphorus on phytoplankton community structure in Dapeng’ao area of Daya Bay I. Chlorophyll a and primary productivity. Journal of Tropical Oceanography, 27(1): 38–45
    [82] Zwart J A, Solomon C T, Jones S E. 2015. Phytoplankton traits predict ecosystem function in a global set of lakes. Ecology, 96(8): 2257–2264. doi: 10.1890/14-2102.1
  • 加载中
图(6) / 表(4)
计量
  • 文章访问数:  288
  • HTML全文浏览量:  92
  • PDF下载量:  8
  • 被引次数: 0
出版历程
  • 收稿日期:  2021-10-11
  • 录用日期:  2022-01-13
  • 网络出版日期:  2022-04-22
  • 刊出日期:  2022-08-15

目录

    /

    返回文章
    返回