Phytoplankton and carbon biomass dynamics in the South China Sea: responses to shelf-oceanic gradients and tropical cyclone

Abstract

This study contains integrated in situ observations from three research cruises (2019–2020), one of which encountered the tropical cyclone Sinlaku. The results show that the depth-integrated phytoplankton abundance and carbon biomass in the open sea was more than eightfold and sixfold, respectively, than those in the shelf. Diatoms were the major contributors in shelf areas. In the open sea, Trichodesmium was dominant, exhibiting abundances more than sixteen times higher than shelf areas and exceeding diatom and dinoflagellate abundances by three to nine orders of magnitude near the surface. In the period affected by tropical cyclone Sinlaku, total phytoplankton abundance and carbon biomass increased markedly compared to non-cyclone conditions, with horizontal and vertical distributions showing significant fluctuations due to the patchy distribution of high-density aggregations. Dinoflagellates were the dominant carbon biomass contributor at the 25 m layer, accounting for 71.13% of total carbon biomass. Species-level analysis of carbon biomass and equivalent spherical diameter confirmed that chain-forming diatoms and large-size dinoflagellates were significant participants in the carbon pool. Statistical and modeling approaches identified salinity and vertical stratification as key environmental drivers of shelf assemblages, while cyclone-induced coupling of temperature and nutrients played a critical role in shaping open-sea phytoplankton.

Keywords

Phytoplankton / Trichodesmium / Carbon biomass / Dinoflagellate / South China Sea

References

[1] Anglès S, Jordi A, Campbell L. Responses of the coastal phytoplankton community to tropical cyclones revealed by high-frequency imaging flow cytometry. Limnol Oceanogr, 2015, 60: 1562-1576

[2] Barton AD, Finkel ZV, Ward BA, Johns DG, Follows MJ. On the roles of cell size and trophic strategy in north Atlantic diatom and dinoflagellate communities. Limnol Oceanogr, 2013, 58: 254-266

[3] Camila SP, Ward BA, Jérme P, André W, Visser KT, Andersen KH. Linking plankton size spectra and community composition to carbon export and its efficiency. Glob Biogeochem Cycles, 2022, 36: e2021GB007275

[4] Canadell JG, Seneviratne SI, Zscheischler J, Cramer W, Buchmann N, Vicca S, Beer C, Bahn M, Wattenbach M, Ibrom A, Miglietta F, Mahecha MD, Rammig A, Walz A, Frank DA, Poulter B, Frank D, Thonicke K, Smith P, Ciais P, Zavala MA, Van der Velde M, Babst F, Reichstein M. Effects of climate extremes on the terrestrial carbon cycle: concepts, processes and potential future impacts. Glob Change Biol, 2015, 21: 2861-2880

[5] Chai F, Wang Y, Xing X, Yan Y, Boss E. A limited effect of sub-tropical typhoons on phytoplankton dynamics. Biogeosciences, 2021, 18: 849-859

[6] Chang ST (2011) The distribution of Trichodesmium in the South China Sea and the ecological factors that affect it. Dissertation, National Sun Yat-Sen University

[7] Chen YLL, Chen H-Y. Seasonal dynamics of primary and new production in the northern South China Sea: the significance of river discharge and nutrient advection. Deep Sea Res Part A Oceanogr Res Pap, 2006, 53: 971-986

[8] Chen YLL, Chen H-Y, Tuo S-H, Ohki K. Seasonal dynamics of new production from Trichodesmium N₂ fixation and nitrate uptake in the upstream Kuroshio and South China Sea basin. Limnol Oceanogr, 2009, 53: 1705-1721

[9] Chen Z, Sun J, Gu T, Zhang G, Wei Y. Nutrient ratios driven by vertical stratification regulate phytoplankton community structure in the oligotrophic western Pacific Ocean. Ocean Sci, 2021, 17: 1775-1789

[10] Clarke KR, Gorley RN (2001) PRIMER v5: user manual/tutorial, PRIMER-E. Plymouth UK, 91

[11] Dang X, Chen X, Bai Y, He X, Arthur Chen C-T, Li T, Pan D, Zhang Z. Impact of ENSO events on phytoplankton over the Sulu ridge. Mar Environ Res, 2020, 157: 104934

[12] Ding X, Liu J, Zhang H, Ke Z, Li J, Liu W, Li K, Zhao C, Tan Y. Phytoplankton community patterns in the Northeastern South China Sea: implications of intensified Kuroshio Intrusion during the 2015/16 El Niño. J Geophys Res-Oceans, 2022, 127: 1-17

[13] Dippner JW, Nguyen KV, Hein H, Ohde T, Loick N. Monsoon-induced upwelling off the Vietnamese coast. Ocean Dyn, 2007, 57: 46-62

[14] Eppley RW, Reid FMH, Strickland JDH. Estimates of phytoplankton crop size, growth rate and primary production. Bull Scripps Inst Oceanogr, 1970, 17: 33-42

[15] Falor D, Gayen B, Sengupta D, Sengupta D, Chaudhuri D. Enhanced ocean mixing during the passage of Tropical Cyclone. Geophys Res Lett, 2024, 51: e2024GL111925

[16] Gui J, Wei Y, Sun J, Le F, Cai Y, Ning X. Summer phytoplankton assemblages and carbon biomass in the northern South China Sea. Cont Shelf Res, 2020, 210: 104276

[17] Hansen HP, Koroleff FGrasshoff K, Kremling K, Ehrhardt M. Determination of nutrients. Methods of seawater analysis, 1999, Weinheim. Wiley-VCH: 159-226

[18] Hu C, Muller-Karger FE. Response of sea surface properties to Hurricane Dennis in the eastern Gulf of Mexico. Geophys Res Lett, 2007, 34: 248-265

[19] Hu J, Wang XH. Progress on upwelling studies in the China seas. Rev Geophys, 2016, 54: 653-673

[20] Li L, Song X, Wang Z, Wan M, Ni G, Tan Y, Li G. Nitrogen enrichment ameliorates the stimulatory effects of reduced salinity on photosynthesis and growth of phytoplankton assemblages in the northern South China Sea. Mar Environ Res, 2023, 192: 106249

[21] Lin I, Liu WT, Wu CC, Wong GTF, Hu C, Chen Z, Liang W-D, Yang Y, Liu K-K. New evidence for enhanced ocean primary production triggered by tropical cyclone. Geophys Res Lett, 2003, 30: 1718

[22] Linacre L, Sa´nchez-Robles C, Mirabal-Go´mez U, Lara-Lara JR, Baza´n-Guzma´n C. Cell carbon content and biomass assessments of dinoflagellates and diatoms in the oceanic ecosystem of the Southern Gulf of Mexico. PLoS ONE, 2021, 16: e0247071

[23] Liu K-K, Chao S-Y, Shaw P-T, Gong G-C, Chen C-C, Tang TY. Monsoon-forced chlorophyll distribution and primary production in the South China Sea: observations and a numerical study. Deep Sea Res Part A Oceanogr Res Pap, 2002, 49: 1387-1412

[24] Liu SM, Li RH, Zhang GL, Wang DR, Du JZ. The impact of anthropogenic activities on nutrient dynamics in the tropical Wenchanghe and Wenjiaohe Estuary and Lagoon system in East Hainan, China. Mar Chem, 2011, 125: 49-68

[25] Lydia I. Size scaling patterns of species richness and carbon biomass for marine phytoplankton functional groups. Mar Ecol, 2017, 38: e12454

[26] Ma C, Zhao J, Ai B, Sun S, Zhang G, Huang W, Wang G. Assessing responses of phytoplankton to consecutive tropical cyclones by combining Argo, remote sensing and numerical simulation data. Sci Total Environ, 2021, 790: 148086

[27] Mao Y, Guo C, Yu L, Gong X, Sun J. The impact of eddies and spring warm pool on sinking rates of phytoplankton with different shapes and sizes. Mar Biol, 2024, 171: 1-22

[28] Mao Y, Li X, Zhang G, Liao Y, Qian G, Sun J. Rinking rate and community structures of autumn phytoplankton responses to mesoscale physical processes in the Western South China Sea. Front Microbiol, 2021, 12: 777473

[29] Mao Y, Sun J, Guo C, Wei Y, Wang X, Yang S, Wu C. Effects of tropical cyclone Roke and Haitang on phytoplankton community structure in northeastern South China Sea. Ecosyst Health Sust, 2019, 5: 144-154

[30] Mena C, Reglero P, Hidalgo M, Sintes E, Santiago R, Martín M, Moy`a G, Balbín R. Phytoplankton community structure is driven by stratification in the oligotrophic Mediterranean Sea. Front Microbiol, 2019, 10: 1698

[31] Mulholland MR, Bernhardt PW, Ozmon I, Procise LA, Garrett M, O'Neil JM, Heil CA, Bronk DA. Contribution of diazotrophy to nitrogen inputs supporting karenia brevis blooms in the Gulf of Mexico. Harmful Algae, 2014, 38: 20-29

[32] Ning X, Chai F, Xue H, Cai Y, Liu C, Shi J. Physical-biological oceanographic coupling influencing phytoplankton and primary production in the South China Sea. J Geophys Res, 2004, 109: C10

[33] Pabortsava K, Lampitt RS, Benson J, Crowe C, McLachlan R, Le Moigne FAC, Woodward EMS. Carbon sequestration in the deep Atlantic enhanced by Saharan dust. Nat Geosci, 2017, 10: 189-194

[34] Pan J, Huang L, Devlin AT, Lin H. Quantification of typhoon-induced phytoplankton blooms using satellite multi-sensor data. Remote Sens, 2018, 10: 318

[35] Peñaflor EL, Villanoy CL, Liu C-T, David LT. Detection of monsoonal phytoplankton blooms in Luzon Strait with MODIS data. Remote Sens Environ, 2007, 109: 443-450

[36] Roberts MJ, Camp J, Seddon J, Vidale PL, Hodges K, Vannière B, Mecking J, Haarsma R, Bellucci A, Scoccimarro E, Caron L-P, Chauvin F, Terray L, Valcke S, Moine M-P, Putrasahan D, Roberts CD, Senan R, Zarzycki C, Ullrich P, Yamada Y, Mizuta R, Kodama C, Fu D, Zhang Q, Danabasoglu G, Rosenbloom N, Wang H, Wu L. Projected future changes in tropical cyclones using the CMIP6 HighResMIP multimodel ensemble. Geophys Res Lett, 2020, 47: e2020GL088662

[37] Sun J, Liu DY. The preliminary notion on nomenclature of common phytoplankton in China Sea waters. Oceanol Limnol Sin, 2002, 33: 271-286

[38] Sun J, Liu DY. Geometric models for calculating cell biovolume and surface area for phytoplankton. J Plankton Res, 2003, 11: 1331-1346

[39] Sun J, Liu DY, Qian SB. Quantative research and analysis method for marine phytoplankton: an introduction to utermöhl method and its modification. J Oceanol Huanghai Bohai Seas, 2002, 20: 105-112

[40] Sun L, Yang Y, Xian T, Lu Z-M, Fu Y-F. Strong enhancement of chlorophyll a concentration by a weak tropical cyclone. Mar Ecol Prog Ser, 2010, 404: 39-50

[41] Tang DL, Kawamura H, Van DT, Lee M. Offshore phytoplankton biomass increase and its oceanographic causes in the South China Sea. Mar Ecol Prog Ser, 2004, 268: 31-41

[42] Thompson P, Paerl HW, Campbell L, Yin K, McDonald K. Tropical cyclones: what are their impacts on phytoplankton ecology?. J Plankton Res, 2023, 45: 180-204

[43] Tian J, Yang Q, Zhao W. Enhanced diapycnal mixing in the South China Sea. J Phys Oceanogr, 2009, 39: 3191-3203

[44] Tomas CR. Identifying marine phytoplankton, 1997, San Diego CA. Academic Press

[45] Utermöhl VH. Neue wege in der quantitativen erfassung des planktons. SIL Proc, 1931, 5: 567-596

[46] Vallina SM, Marrase C, Gasol JM, Bahamon N, Follows MJ, Gland GL, Cermeño P. Seasonal dynamics of phytoplankton community assembly at the Blanes Bay Microbial Observatory (BBMO), NW Mediterranean Sea. Prog Oceanogr, 2023, 219: 103125

[47] Wang G, Cao W, Wang G. The seasonal variation of the phytoplankton size class in northern South China Sea. IOP Conf Ser Earth Environ Sci, 2014, 17: 012121

[48] Wang L, Lau KH, Fung CH, Gan JP. The relative vorticity of ocean surface winds from the QuikSCAT satellite and its effect on the genesis of tropical cyclones in the South China Sea. Tellus A, 2007, 59: 1-8

[49] Wang R, Ding X, Shen H, Jiang T, Tang J, Lü H. Phytoplankton blooms with sequential cyclonic and anticyclonic eddies during the passage of tropical cyclone Hibaru. Tellus A, 2024, 76: 1-13

[50] Wang Y. Composite of typhoon-induced sea surface temperature and chlorophyll-a responses in the South China Sea. J Geophys Res Oceans, 2020, 125: e2020JC016243

[51] Welschmeyer NA. Fluorometric analysis of Chlorophyll a in the presence of Chlorophyll b and pheopigments. Limnol Oceanogr, 1994, 39: 1985-1992

[52] Xing X, Boss E, Chen S, Chai F. Seasonal and daily-scale photoacclimation modulating the phytoplankton chlorophyll-carbon coupling relationship in the mid-latitude northwest Pacific. J Geophys Res Oceans, 2021, 126: 1-18

[53] Yamaji I. Illustrations of the Marine Plankton of Japan, 1991, Tokyo. Hoikusha Press: 1-158

[54] Yan W, Chen Z, Zhang L, Wang F, Zhang G, Sun J. Nanophytoplankton and microphytoplankton in the western tropical Pacific Ocean: its community structure, cell size and carbon biomass. Front Mar Sci, 2023, 10: 1147271

[55] Ye HJ, Sui Y, Tang DL, Afanasyev Y. A subsurface chlorophyll a bloom induced by Tropical cyclone in the South China Sea. J Mar Syst, 2018, 128: 138-145

[56] Yu Y, Xing X, Liu H, Yuan Y, Wang Y, Chai F. The variability of chlorophyll-a and its relationship with dynamic factors in the basin of the South China Sea. J Mar Syst, 2019, 200: 103230

[57] Zhao H, Tang DL, Wang Y. Comparison of phytoplankton blooms triggered by two tropical cyclones with different intensities and translation speeds in the South China Sea. Mar Ecol Prog Ser, 2008, 365: 57-65

[58] Zhao H, Wang Y. Phytoplankton increases induced by tropical cyclones in the South China Sea during 1998–2015. J Geophys Res Oceans, 2018, 123: 2903-2920

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The Author(s), under exclusive licence to Ocean University of China