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Temperature-Dependent Bifurcated Seasonal Shift of Phytoplankton Community Composition in the Coastal Water off Southwestern Korea

  • Yoonja Kang
  • Hee-Yoon Kang
  • Dongyoung Kim
  • Young-Jae Lee
  • Tae-Ik Kim
  • Chang-Keun KangEmail author
Article
  • 18 Downloads

Abstract

Coastal water around the archipelago off southwestern Korea has been bathed in an unprecedented pool of warm water in summer in recent years. Here, we examined phytoplankton community responses to amplified seasonal temperature fluctuation around the archipelago based on chemotaxonomic analysis in association with physicochemical properties in the shallow coastal water from June 2016 to March 2018. Concentrations of dissolved inorganic nutrients were significantly higher during the warm season than during the cold season. Canonical correspondence analysis revealed that water temperature was a main driver controlling the phytoplankton community. Generalized additive models denoted that small phytoplankton groups (cryptophytes, cyanobacteria, and prasinophytes) were more resistant to high temperatures (> 25°C) compared with diatoms. Indeed, dominance of diatoms was significant (80%) during the cold season and sharply declined (to 49%) during the warm season. Small phytoplankton were dominant (62%) as the water temperature exceeded 22°C. Our results highlight the effects of temperature-dependent bifurcated seasonality on phytoplankton communities in coastal waters. Furthermore, unprecedentedly high summer temperatures in August 2016 coincided with a remarkable increase in the importance (∼70%) of small phytoplankton. Accumulating evidence provides indications regarding future scenarios: while small phytoplankton will probably account for summer blooms, diatom blooms will shift to winter.

Keywords

coastal warming phytoplankton dynamics chemotaxonomic analysis diatoms small phytoplankton cryptophytes cyanobacteria 

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Notes

Acknowledgments

We would like to express our gratitude to Changseong Kim, Jaebin Jang, Kwanghun Lee for their analytical assistance. This study was financed by National Institute of Fisheries Science (grant no. R2018009; HYPERLINK “http://www.nifs.go.krhttps://doi.org/www.nifs.go.kr). This study was also partially supported by “Long-term change of structure and function in marine ecosystems of Korea” funded by the Ministry of Oceans and Fisheries, Korea.

References

  1. Ahn Y, Shanmugam P, Moon J, Ryu J (2008) Satellite remote sensing of a low-salinity water plume in the East China Sea. Ann Geophys 26:2019–2035CrossRefGoogle Scholar
  2. Altman JC, Paerl HW (2012) Composition of inorganic and organic nutrient sources influences phytoplankton community structure in the New River Estuary, North Carolina. Aquat Ecol 46:269–282CrossRefGoogle Scholar
  3. Arrigo KR, van Dijken GL, Alderkamp AC, Erickson ZK, Lewis KM, Lowry KE, Joy-Warren HL, Middag R, Nash-Arrigo JE, Selz V (2017) Early spring phytoplankton dynamics in the Western Antarctic Peninsula. J Geophys Res-Oceans 122:9350–9369CrossRefGoogle Scholar
  4. Atkinson D (1994) Temperature and organism size: a biological law for ectotherms? Adv Ecol Res 25:1–58CrossRefGoogle Scholar
  5. Bénard R, Levasseur M, Scarratt M, Blais M-A, Mucci A, Ferreyra G, Starr M, Gosselin M, Tremblay J-É, Lizotte M (2018) Experimental assessment of the sensitivity of an estuarine phytoplankton fall bloom to acidification and warming. Biogeosciences 15:4883–4904CrossRefGoogle Scholar
  6. Bopp L, Monfray P, Aumont O, Dufresne JL, Le Treut H, Madec G, Terray L, Orr JC (2001) Potential impact of climate change on marine export production. Global Biogeochem Cy 15:81–99CrossRefGoogle Scholar
  7. Bouwman AF, Beusen A, Overbeek C, Bureau D, Pawlowski M, Glibert P (2013a) Hindcasts and future projections of global inland and coastal nitrogen and phosphorus loads due to finfish aquaculture. Rev Fish Sci 21:112–156CrossRefGoogle Scholar
  8. Bouwman L, Beusen A, Glibert PM, Overbeek C, Pawlowski M, Herrera J, Mulsow S, Yu R, Zhou M (2013b) Mariculture: significant and expanding cause of coastal nutrient enrichment. Environ Res Lett 8:044026. doi: https://doi.org/10.1088/1748-9326/8/4/044026 CrossRefGoogle Scholar
  9. Boyd PW, Rynearson TA, Armstrong EA, Fu F, Hayashi K, Hu Z, Hutchins DA, Kudela RM, Litchman E, Mulholland MR, Passow U, Strzepek RF, Whittaker KA, Yu E, Thomas MK (2013) Marine phytoplankton temperature versus growth responses from polar to tropical waters — outcome of a scientific community — wide study. PLoS One 8:e63091. doi: https://doi.org/10.1371/journal.pone.0063091 CrossRefGoogle Scholar
  10. Braaten BR, Bergheim A (2007) Cage aquaculture and environmental impacts. Aquacult Eng Environ 661:49–91Google Scholar
  11. Chivers WJ, Walne AW, Hays GC (2017) Mismatch between marine plankton range movements and the velocity of climate change. Nat Commun 8:14434. doi: https://doi.org/10.1038/ncomms14434 CrossRefGoogle Scholar
  12. Choi YH, Seong KT, Ko WJ, Lee MJ, Ju KH, Lee MS (2015) Environmental characteristics of the abalone mariculture area. In: Proceedings of the Conference on The Korean Society for Marine Environment and Energy, Jeju, 21–22 May 2015Google Scholar
  13. Choi YH, Sung KT, Choi HG, Ju KH (2016) Characteristics of water mass in the southwestern coast of Korea in summer of 2016. In: Proceedings of the Conference on Korean Environmental Sciences. Daegu, 3–4 Nov 2016Google Scholar
  14. Chung CC, Hwang SPL, Chang J (2003) Identification of a high-affinity phosphate transporter gene in a prasinophyte alga, Tetraselmis chuii, and its expression under nutrient limitation. Appl Environ Microb 69:754–759CrossRefGoogle Scholar
  15. Cloern JE, Foster S, Kleckner A (2014) Phytoplankton primary production in the world’s estuarine-coastal ecosystems. Biogeosciences 11:2477–2501CrossRefGoogle Scholar
  16. Daufresne M, Lengfellner K, Sommer U (2009) Global warming benefits the small in aquatic ecosystems. P Natl Acad Sci USA 106:12788–12793CrossRefGoogle Scholar
  17. Davis TW, Berry DL, Boyer GL, Gobler CJ (2009) The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae 8:715–725CrossRefGoogle Scholar
  18. Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926–929CrossRefGoogle Scholar
  19. Dortch Q (1990) The interaction between ammonium and nitrate uptake in phytoplankton. Mar Ecol-Prog Ser 61:183–201CrossRefGoogle Scholar
  20. Dortch Q, Whitledge TE (1992) Does nitrogen or silicon limit phytoplankton production in the Mississippi River plume and nearby regions? Cont Shelf Res 12:1293–1309CrossRefGoogle Scholar
  21. Falkowski PG, Oliver MJ (2007) Mix and match: how climate selects phytoplankton. Nat Rev Microbiol 5:813–819CrossRefGoogle Scholar
  22. Feng YY, Hou LC, Ping NX, Ling TD, Kyo CI (2004) Development of mariculture and its impacts in Chinese coastal waters. Rev Fish Biol Fisher 14:1–10CrossRefGoogle Scholar
  23. Flombaum P, Gallegos JL, Gordillo RA, Rincón J, Zabala LL, Jiao N, Karl DM, Li WKW, Lomas MW, Veneziano D, Vera CS, Vrugt JA, Martiny AC (2013) Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. P Natl Acad Sci USA 110:9824–9829CrossRefGoogle Scholar
  24. Forster J, Hirst AG, Atkinson D (2012) Warming-induced reductions in body size are greater in aquatic than terrestrial species. P Natl Acad Sci USA 109:19310–19314CrossRefGoogle Scholar
  25. Geider RJ (1987) Light and temperature dependence of the carbon to chlorophyll a ratio in microalgae and cyanobacteria: implications for physiology and growth of phytoplankton. New Phytol 160:1–34CrossRefGoogle Scholar
  26. Gobler CJ, Koch F, Kang Y, Berry DL, Tang YZ, Lasi M, Walters L, Hall L, Miller JD (2013) Expansion of harmful brown tides caused by the pelagophyte, Aureoumbra lagunensis DeYoe et Stockwell, to the US East Coast. Harmful Algae 27:29–41CrossRefGoogle Scholar
  27. Gobler CJ, Sunda WG (2012) Ecosystem disruptive algal blooms of the brown tide species, Aureococcus anophagefferens and Aureoumbra lagunensis. Harmful Algae 14:36–45CrossRefGoogle Scholar
  28. Goldburg R, Elliott MS, Naylor R (2001) Marine aquaculture in the United States: environmental impacts and policy options. PEW Oceans Commission, Virginia, 33 pGoogle Scholar
  29. Griffiths JR, Kadin M, Nascimento FJA, Tamelander T, Törnroos A, Bonaglia S, Bonsdorff E, Brüchert V, Gårdmark A, Järnström M, Kotta J, Lindegren M, Nordström MC, Norkko A, Olsson J, Weigel B, Žydelis R, Blenckner T, Niiranen S, Winder M (2017) The importance of benthic-pelagic coupling for marine ecosystem functioning in a changing world. Glob Change Biol 23:2179–2196CrossRefGoogle Scholar
  30. Guo X, Miyazawa Y, Yamagata T (2006) The Kuroshio onshore intrusion along the shelf break of the East China Sea: The origin of the Tsushima Warm Current. J Phys Oceanogr 36:2205–2231CrossRefGoogle Scholar
  31. Han SY, Kim JK, Tashiro F, Kai Y, Yoo JT (2019) Relative importance of ocean currents and fronts in population structures of marine fish: a lesson from the cryptic lineages of the Hippocampus mohnikei complex. Mar Biodivers 49:263–275CrossRefGoogle Scholar
  32. Hare CE, Leblanc K, DiTullio GR, Kudela RM, Zhang Y, Lee PA, Riseman S, Hutchins DA (2007) Consequences of increased temperature and CO2 for phytoplankton community structure in the Bering Sea. Mar Ecol-Prog Ser 352:9–16CrossRefGoogle Scholar
  33. Hastie TJ (2017) Generalized additive models. In: Chamber JM, Hastie TJ (eds) Statistical models in S. CRC Press, Florida, pp 249–307Google Scholar
  34. Holmer M, Duarte CM, Heilskov A, Olesen B, Terrados J (2003) Biogeochemical conditions in sediments enriched by organic matter from net-pen fish farms in the Bolinao area, Philippines. Mar Pollut Bull 46:1470–1479CrossRefGoogle Scholar
  35. Honkanen T, Helminen H (2000) Impacts of fish farming on eutrophication: comparisons among different characteristics of ecosystem. Int Rev Hydrobiol 85:673–686CrossRefGoogle Scholar
  36. Howarth RW (2008) Coastal nitrogen pollution: a review of sources and trends globally and regionally. Harmful Algae 8:14–20CrossRefGoogle Scholar
  37. Hwang JH, Van SP, Choi BJ, Chang YS, Kim YH (2014) The physical processes in the Yellow Sea. Ocean Coast Manage 102:449–457CrossRefGoogle Scholar
  38. IPCC (2001) Climate change 2001: the scientific basis. Cambridge University Press, Cambridge, 881 pGoogle Scholar
  39. Jeffrey SW, Humphrey GF (1997) Application of pigment methods to oceanography. In: Jeffrey SW, Mantoura RFC, Wright SW (eds) Phytoplankton pigments in oceanography. UNESCO Publishing, pp 457–553Google Scholar
  40. Jeong HD, Kwon CH, Kim SW, Cho KD (2009) Fluctuation of tidal front and expansion of cold water region in the southwestern sea of Korea. J Korean Soc Mar Environ Saf 15:289–296Google Scholar
  41. Jiang ZB, Chen QZ, Zeng JN, Liao YB, Shou L, Liu J (2012) Phytoplankton community distribution in relation to environmental parameters in three aquaculture systems in a Chinese subtropical eutrophic bay. Mar Ecol-Prog Ser 446:73–89CrossRefGoogle Scholar
  42. Kang Y, Koch F, Gobler CJ (2015) The interactive roles of nutrient loading and zooplankton grazing in facilitating the expansion of harmful algal blooms caused by the pelagophyte, Aureoumbra lagunensis, to the Indian River Lagoon, FL, USA. Harmful Algae 49:162–173CrossRefGoogle Scholar
  43. Karentz D, Smayda TJ (1984) Temperature and seasonal occurrence patterns of 30 dominant phytoplankton species in Narragansett Bay over a 22-year period (1959-1980). Mar Ecol-Prog Ser 18:277–293CrossRefGoogle Scholar
  44. Kim B, Choi A, Kim HC, Jung RH, Lee WC, Hyun JH (2011) Rate of sulfate reduction an diron reduction in the sediment associated with ablone aquaculture in the southern coastal wateres of Korea. Ocean Polar Res 33:435–445CrossRefGoogle Scholar
  45. Kim JK, Choi OI, Chang DS, Kim JI (2002) Fluctuation of bag-net catches off Wando, Korea and the effect of sea water temperature. Korean J Fish Aquat Sci 35:497–503Google Scholar
  46. Kim JK, Kang CB, Ahn G, Oki D, Kim YU, Tabeta O (2005) Distribution of fish larvae and juveniles in the East China Sea and the Yellow Sea in spring during 1994–1997. Korean J Fish Aquat Sci 38:29–38Google Scholar
  47. Ko JC, Kim JT, Kim SH, Rho HK (2003) Fluctuation characteristic of temperature and salinity in coastal waters around Jeju Island. Korean J Fish Aquat Sci 36:306–316Google Scholar
  48. Kremp A, Godhe A, Egardt J, Dupont S, Suikkanen S, Casabianca S, Penna A (2012) Intraspecific variability in the response of bloom-forming marine microalgae to changed climate conditions. Ecol Evol 2:1195–1207CrossRefGoogle Scholar
  49. Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso JP (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Change Biol 19:1884–1896CrossRefGoogle Scholar
  50. Kwak JH, Han E, Lee SH, Park HJ, Kim K-R, Kang C-K (2017) A consistent structure of phytoplankton communities across the warm-cold regions of the water mass on a meridional transect in the East/Japan Sea. Deep-Sea Res Pt II 143:36–14CrossRefGoogle Scholar
  51. Kwak JH, Lee SH, Hwang J, Suh YS, Park H, Chang KI, Kim KR, Kang CK (2014) Summer primary productivity and phytoplankton community composition driven by different hydrographic structures in the East/Japan Sea and the Western Subarctic Pacific. J Geophys Res-Oceans 119:4505–4519CrossRefGoogle Scholar
  52. Lee CK, Park TG, Park YT, Lim WA (2013) Monitoring and trends in harmful algal blooms and red tides in Korean coastal waters, with emphasis on Cochlodinium polykrikoides. Harmful Algae 30:S3–S14CrossRefGoogle Scholar
  53. Lee YW, Park M, Kim YS, Kim S S, Kang CK (2011) Application of hotosynthetic pigment analysis using a HPLC and CHEMTAX program to studies of phytoplankton community composition. The Sea 16:117–124CrossRefGoogle Scholar
  54. Li W, Smith J, Platt T (1984) Temperature response of photosynthetic capacity and carboxylase activity in Arctic marine phytoplankton. Mar Eco-Prog Ser 17:237–243CrossRefGoogle Scholar
  55. Lie HJ, Cho CH (1997) Surface current fields in the East China Sea. J Oceanogr Soc Korea 32:1–7Google Scholar
  56. Lie HJ, Cho CH (2002) Recent advances in understanding the circulation and hydrography of the East China Sea. Fish Oceanogr 11:318–328CrossRefGoogle Scholar
  57. Lie HJ, Cho CH, Lee JH, Lee S (2003) Structure and eastward extension of the Changjiang River plume in the East China Sea. J Geophys Res-Oceans 108:3077. doi: https://doi.org/10.1029/2001JC001194 CrossRefGoogle Scholar
  58. Liefer JD, Garg A, Campbell DA, Irwin AJ, Finkel ZV (2018) Nitrogen starvation induces distinct photosynthetic responses and recovery dynamics in diatoms and prasinophytes. PLoS One 13:e0195705. doi: https://doi.org/10.1371/journal.pone.0195705 CrossRefGoogle Scholar
  59. Lima FP, Wethey DS (2012) Three decades of high-resolution coastal sea surface temperatures reveal more than warming. Nat Commun 3:704. doi: https://doi.org/10.1038/ncomms1713 CrossRefGoogle Scholar
  60. Liu X, Xiao W, Landry MR, Chiang K-P, Wang L, Huang B (2016) Responses of phytoplankton communities to environmental variability in the East China Sea. Ecosystems 19:832–849CrossRefGoogle Scholar
  61. Mackey M, Mackey D, Higgins H, Wright S (1996) CHEMTAX-a program for estimating class abundances from chemical markers: application to HPLC measurements of phytoplankton. Mar Ecol-Prog Ser 144:265–283CrossRefGoogle Scholar
  62. Marañón E, Cermeño P, Huete-Ortega M, López-Sandoval DC, Mouriño-Carballido B, Rodríguez-Ramos T (2014) Resource supply overrides temperature as a controlling factor of marine phytoplankton growth. PLoS One 9:e99312. doi: https://doi.org/10.1371/journal.pone.0099312 CrossRefGoogle Scholar
  63. Marañón E, Lorenzo MP, Cermeño P, Mouriño-Carballido B (2018) Nutrient limitation suppresses the temperature dependence of phytoplankton metabolic rates. ISME J 12:1836–1845CrossRefGoogle Scholar
  64. Marshall W, Laybourn-Parry J (2002) The balance between photosynthesis and grazing in Antarctic mixotrophic cryptophytes during summer. Freshwater Biol 47:2060–2070CrossRefGoogle Scholar
  65. Morán XAG, López-Urrutia, Calvo-Díaz A, Li WKW (2010) Increasing importance of small phytoplankton in a warmer ocean. Glob Change Biol 16:1137–1144CrossRefGoogle Scholar
  66. Mulholland MR, Lomas MW (2008) Nitrogen uptake and assimilation In: Capone DG, Bronk DA, Carpenter EJ (eds) Nitrogen in the marine environment. Elsevier, Amsterdam, pp 303–384CrossRefGoogle Scholar
  67. Nan C, Zhang H, Zhao G (2004) Allelopathic interactions between the macroalga and eight microalgal species. J Sea Res 52:259–268CrossRefGoogle Scholar
  68. NFRDI (2008) Research on the scheme of competitiveness strengthening in aquaculture industry. Natonal Fisheries Research and Development Institute, Busan, 289 pGoogle Scholar
  69. NIFS (2018) Monitoring the production of abalone aquaculture farms. National Institute of Fisheries Science, Busan, 190 p Oh HJ, Kim SH, Moon SY (2008) The characteristics of phytoplankton community of cold water in the around sea of Wando in summer, 2005. J Environ Sci 17:949–956Google Scholar
  70. Paerl HW, Hall NS, Peierls BL, Rossignol KL (2014) Evolving paradigms and challenges in estuarine and coastal eutrophication dynamics in a culturally and climatically stressed World. Estuar Coast 37:243–258CrossRefGoogle Scholar
  71. Park JH, Cho YS, Lee WC, Hong SJ, Kim HC, Kim JB (2012) Comparison of material flux at the sediment-water interface in marine finfish and abalone cage farms, southern coast of Korea: In-situ and laboratory incubation examination. J Korean Soc Mar Environ Saf 18:536–544CrossRefGoogle Scholar
  72. Parsons TR (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press. doi: https://doi.org/10.1016/C2009-0-07774-5
  73. Raven JA (1998) The twelfth tansley lecture, small is beautiful: the picophytoplankton. Funct Ecol 12:503–513CrossRefGoogle Scholar
  74. Sar G, Lo Martire M, Sanfilippo M, Pulican G, Cortese G, Mazzola A, Manganaro A, Pusceddu A (2011) Impacts of marine aquaculture at large spatial scales: evidences from N and P catchment loading and phytoplankton biomass. Mar Environ Res 71:317–324CrossRefGoogle Scholar
  75. Schaum CE, Buckling A, Smirnoff N, Studholme DJ, Yvon-Durocher G (2018) Environmental fluctuations accelerate molecular evolution of thermal tolerance in a marine diatom. Nat Commun 9:1719. doi:  https://doi.org/10.1038/s41467-018-03906-5 CrossRefGoogle Scholar
  76. Sinha E, Michalak A, Balaji V (2017) Eutrophication will increase during the 21st century as a result of precipitation changes. Science 357:405–408CrossRefGoogle Scholar
  77. Smith D, Horne A (1988) Experimental measurement of resource competition between planktonic microalgae and macroalgae (seaweeds) in mesocosms simulating the San Francisco Bay-Estuary, California. Hydrobiologia 159:259–268CrossRefGoogle Scholar
  78. Šupraha L, Bosak S, Ljubešić Z, Mihanović H, Olujić G Mikac I, Viličić D (2014) Cryptophyte bloom in a mediterranean estuary: high abundance of Plagioselmis cf. prolonga in the Krka River estuary (eastern Adriatic Sea). Sci Mar 78:329–338CrossRefGoogle Scholar
  79. Tang YZ, Kang Y, Berry D, Gobler CJ (2015) The ability of the red macroalga, Porphyra purpurea (Rhodophyceae) to inhibit the proliferation of seven common harmful microalgae. J Appl Phycol 27:531–544CrossRefGoogle Scholar
  80. Thomas MK, Aranguren-Gassis M, Kremer CT, Gould MR, Anderson K, Klausmeier CA, Litchman E (2017) Temperature-nutrient interactions exacerbate sensitivity to warming in phytoplankton. Glob Change Biol 23:3269–3280CrossRefGoogle Scholar
  81. Thomas MK, Kremer CT, Klausmeier CA, Litchman E (2012) A global pattern of thermal adaptation in marine phytoplankton. Science 338:1085–1088CrossRefGoogle Scholar
  82. Toseland A, Daines SJ, Clark JR, Kirkham A, Strauss J, Uhlig C, Lenton TM, Valentin K, Pearson GA, Moulton V, Mock T (2013) The impact of temperature on marine phytoplankton resource allocation and metabolism. Nat Clim Change 3:979–984CrossRefGoogle Scholar
  83. Ware DM, Thomson RE (2005) Bottom-up ecosystem trophic dynamics determine fish production in the Northeast Pacific. Science 308:1280–1284CrossRefGoogle Scholar
  84. Yang HW, Cho YK, Seo GH, You SH, Seo JW (2014) Interannual variation of the southern limit in the Yellow Sea Bottom Cold Water and its causes. J Marine Syst 139:119–127CrossRefGoogle Scholar
  85. Yoo JT, Seong KT, Kim YH (2015) Changes in the community structure of fish collected by a gape net iwth wings in the coastal waters of Jindo Island in response to a cold water appreance in the southewestern sea of Korea. Korean J Fish Aquat Sci 48:776–782Google Scholar
  86. Yvon-Durocher G, Montoya JM, Trimmer M, Woodward G (2011) Warming alters the size spectrum and shifts the distribution of biomass in freshwater ecosystems. Glob Change Biol 17:1681–1694CrossRefGoogle Scholar
  87. Yvon-Durocher G, Dossena M, Trimmer M, Woodward G, Allen AP (2015) Temperature and the biogeography of algal stoichiometry. Global Ecol Biogeogr 24:562–570CrossRefGoogle Scholar
  88. Zapata M, Rodríguez F, Garrido JL (2000) Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Mar Ecol-Prog Ser 195:29–45CrossRefGoogle Scholar
  89. Zhang J (2002) Biogeochemistry of Chinese estuarine and coastal waters: nutrients, trace metals and biomarkers. Reg Environ Change 3:65–76CrossRefGoogle Scholar
  90. Zhang J, Liu S, Ren J, Wu Y, Zhang G (2007) Nutrient gradients from the eutrophic Changjiang (Yangtze River) Estuary to the oligotrophic Kuroshio waters and re-evaluation of budgets for the East China Sea Shelf. Prog Oceanogr 74:449–478CrossRefGoogle Scholar
  91. Zhang M, Chen F, Shi X, Yang Z, Kong F (2017) Association between temporal and spatial beta diversity in phytoplankton. Ecography 41:1345–1356CrossRefGoogle Scholar
  92. Zhang Y, Bleeker A, Liu J (2015) Nutrient discharge from China’s aquaculture industry and associated environmental impacts. Environ Res Lett 10:045002. doi: https://doi.org/10.1088/1748-9326/10/4/045002 CrossRefGoogle Scholar

Copyright information

© KSO, KIOST and Springer 2019

Authors and Affiliations

  • Yoonja Kang
    • 1
  • Hee-Yoon Kang
    • 1
  • Dongyoung Kim
    • 1
  • Young-Jae Lee
    • 1
  • Tae-Ik Kim
    • 2
  • Chang-Keun Kang
    • 1
    Email author
  1. 1.School of Earth Sciences and Environmental EngineeringGwangju Institute of Science and TechnologyGwangjuKorea
  2. 2.Southwest Sea Fisheries Research InstituteNational Institute of Fisheries ScienceTongyeongKorea

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