Kuroshio intrusion drives the Trichodesmium assemblage and shapes the phytoplankton community during spring in the East China Sea

Abstract

To understand the influence of Kuroshio intrusion on the phytoplankton community, a field investigation was conducted in spring 2017 in the East China Sea (ECS), and 130 seawater samples were collected and analyzed. Trichodesmium comprised the highest cell abundance contributing about 66% of the total phytoplankton followed by diatoms (17%) and dinoflagellates (16%). The dominance of the Kuroshio Waters (KW) and the Taiwan Warm Currents (TWC) were higher than the Coastal Waters (CW). The vertical distribution of physicochemical parameters depicted the intrusion of KW at the bottom layer, but it failed to reach the surface as strong upwelling was not initiated. Therefore, the dissolved inorganic phosphate (DIP) concentrations and P/N ratios were the lowest in the CW and the upper water layers, which limited the diatom growth in this area. Besides, the dinoflagellates cell abundance was also lower except in the surface and CW, though they comprised the maximum richness of species among the phytoplankton community. However, the unique characteristics such as diazotrophy and gas vacuoles of Trichodesmium made the situation advantageous, and they comprised the maximum cell abundance in this area especially in KW and the TWC. Temperature, DIP and P/N ratios appeared to be the major environmental drivers for Trichodesmium proliferation in the ECS during the study period.

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Data Availability Statement

The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Bergman B, Sandh G, Lin S J, Larsson J, Carpenter E J. 2013. Trichodesmium—a widespread marine cyanobacterium with unusual nitrogen fixation properties. FEMS Microbiology Reviews, 37(3): 286–302.

    Google Scholar 

  2. Breitbarth E, Oschlies A, LaRoche J. 2007. Physiological constraints on the global distribution of Trichodesmium-effect of temperature on diazotrophy. Biogeosciences, 4(1): 53–61.

    Google Scholar 

  3. Capone D G, Zehr J P, Paerl H W, Bergman B, Carpenter E J. 1997. Trichodesmium, a globally significant marine cyanobacterium. Science, 276(5316): 1 221–1 229.

    Google Scholar 

  4. Chai C, Yu Z M, Song X X, Cao X H. 2006. The status and characteristics of eutrophication in the Yangtze River (Changjiang) estuary and the adjacent East China Sea, China. Hydrobiologia, 563(1): 313–328.

    Google Scholar 

  5. Chang J, Chiang K P, Gong G C. 2000. Seasonal variation and cross-shelf distribution of the nitrogen-fixing cyanobacterium, Trichodesmium, in southern East China Sea. Continental Shelf Research, 20(4–5): 479–492.

    Google Scholar 

  6. Chappell P D, Webb E A. 2010. A molecular assessment of the iron stress response in the two phylogenetic clades of Trichodesmium. Environmental Microbiology, 12(1): 13–27.

    Google Scholar 

  7. Chen C T A. 2008. Distributions of nutrients in the East China Sea and the South China Sea connection. Journal of Oceanography, 64(5): 737–751

    Google Scholar 

  8. Chen Y L L, Chen H Y, Lin Y H, Yong T C, Taniuchi Y, Tuo S H. 2014. The relative contributions of unicellular and filamentous diazotrophs to N2 fixation in the South China Sea and the upstream Kuroshio. Deep Sea Research Part I: Oceanographic Research Papers, 85: 56–71.

    Google Scholar 

  9. Ding C L. 2009. The Abundance, the Spatial and Temporal Distributions of Cyanobacteria in the Yellow Sea, the East China Sea and the South China Sea. Ocean University of China, Qingdao. (in Chinese with English abstract)

    Google Scholar 

  10. do Rosario Gomes H, Xu Q, Ishizaka J, Carpenter E J, Yager P L, Goes J I. 2018. The influence of riverine nutrients in niche partitioning of phytoplankton communities-a contrast between the Amazon River plume and the Changjiang (Yangtze) River diluted water of the East China Sea. Frontiers in Marine Science, 5: 343.

    Google Scholar 

  11. Estrada M, Berdalet E. 1997. Phytoplankton in a turbulent world. Scientia Marina, 61(S1): 125–140

    Google Scholar 

  12. Falkowski P G. 1997. Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature, 387(6630): 272–275.

    Google Scholar 

  13. Gao S, Wang Y P. 2008. Changes in material fluxes from the Changjiang River and their implications on the adjoining continental shelf ecosystem. Continental Shelf Research, 28(12): 1 490–1 500.

    Google Scholar 

  14. Guo S J, Feng Y Y, Wang L, Dai M H, Liu Z L, Bai Y, Sun J. 2014. Seasonal variation in the phytoplankton community of a continental-shelf sea: the East China Sea. Marine Ecology Progress Series, 516: 103–126.

    Google Scholar 

  15. Hewson I, Poretsky R S, Dyhrman S T, Zielinski B, White A E, Tripp H J, Montoya J P, Zehr J P. 2009. Microbial community gene expression within colonies of the diazotroph, Trichodesmium, from the Southwest Pacific Ocean. The ISME Journal, 3(11): 1 286.

    Google Scholar 

  16. Hutchins D A, Walworth N G, Webb E A, Saito M A, Moran D, McIlvin M R, Gale J, Fu F X. 2015. Irreversibly increased nitrogen fixation in Trichodesmium experimentally adapted to elevated carbon dioxide. Nature Communications, 6(1): 8155.

    Google Scholar 

  17. Jiang Z B, Chen J F, Zhai H C, Zhou F, Yan X J, Zhu Y L, Xuan J L, Shou L, Chen Q Z. 2019. Kuroshio shape composition and distribution of filamentous diazotrophs in the East China Sea and southern Yellow Sea. Journal of Geophysical Research: Oceans, 124(11): 7 421–7 436.

    Google Scholar 

  18. Jiang Z B, Chen J F, Zhou F, Zhai H C, Zhang D S, Yan X J. 2017. Summer distribution patterns of Trichodesmium spp. in the Changjiang (Yangtze River) estuary and adjacent East China Sea shelf. Oceanologia, 59(3): 248–261.

    Google Scholar 

  19. Jiang Z B, Li H L, Zhai H C, Zhou F, Chen Q Z, Chen J F, Zhang D S, Yan X J. 2018. Seasonal and spatial changes in Trichodesmium associated with physicochemical properties in East China Sea and southern Yellow Sea. Journal of Geophysical Research: Biogeosciences, 123(2): 509–530.

    Google Scholar 

  20. LaRoche J, Breitbarth E. 2005. Importance of the diazotrophs as a source of new nitrogen in the ocean. Journal of Sea Research, 53(1–2): 67–91.

    Google Scholar 

  21. Li H M, Shi X Y, Wang H, Han X R. 2014a. An estimation of nutrient fluxes to the East China Sea continental shelf from the Taiwan Strait and Kuroshio subsurface waters in summer. Acta Oceanologica Sinica, 33(11): 1–10.

    Google Scholar 

  22. Li H M, Tang H J, Shi X Y, Zhang C S, Wang X L. 2014b. Increased nutrient loads from the Changjiang (Yangtze) River have led to increased harmful algal blooms. Harmful Algae, 39: 92–101.

    Google Scholar 

  23. Mills M M, Ridame C, Davey M, La Roche J, Geider R J. 2004. Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature, 429(6989): 292–294.

    Google Scholar 

  24. Moore C M, Mills M M, Achterberg E P, Geider R J, LaRoche J, Lucas M I, McDonagh E L, Pan X, Poulton A J, Rijkenberg M J A, Suggett D J, Ussher S J, Woodward E M S. 2009. Large-scale distribution of Atlantic nitrogen fixation controlled by iron availability. Nature Geoscience, 2(12): 867–871.

    Google Scholar 

  25. 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): 1 007–1 017.

    Google Scholar 

  26. Paerl H W, Prufert-Bebout L E, Guo C Z. 1994. Iron-stimulated N2 fixation and growth in natural and cultured populations of the planktonic marine cyanobacteria Trichodesmium spp. Applied and Environmental Microbiology, 60(3): 1 044–1 047.

    Google Scholar 

  27. Qu B X, Song J M, Yuan H M, Li X G, Li N. 2018. Carbon chemistry in the mainstream of Kuroshio current in eastern Taiwan and its transport of carbon into the east China sea shelf. Sustainability, 10(3): 791.

    Google Scholar 

  28. Romans K M, Carpenter E J, Bergman B. 1994. Buoyancy regulation in the colonial diazotrophic cyanobacterium Trichodesmium tenue: ultrastructure and storage of carbohydrate, polyphosphate, and nitrogen. Journal of Phycology, 30(6): 935–942.

    Google Scholar 

  29. Shi X Y, Li H M, Wang H. 2014. Nutrient STRUCTURE of the Taiwan Warm Current and estimation of vertical nutrient fluxes in upwelling areas in the East China Sea in summer. Journal of Ocean University of China, 13(4): 613–620.

    Google Scholar 

  30. Shiozaki T, Furuya K, Kodama T, Kitajima S, Takeda S, Takemura T, Kanda J. 2010. New estimation of N2 fixation in the western and central Pacific Ocean and its marginal seas. Global Biogeochemical Cycles, 24(1): GB1015.

    Google Scholar 

  31. Shiozaki T, Takeda S, Itoh S, Kodama T, Liu X, Hashihama F, Furuya K. 2015. Why is Trichodesmium abundant in the Kuroshio? Biogeosciences, 12(23): 6 931–6 943.

    Google Scholar 

  32. Smayda T J, Reynolds C S. 2003. Strategies of marine dinoflagellate survival and some rules of assembly. Journal of Sea Research, 49(2): 95–106.

    Google Scholar 

  33. Sun J, Liu D Y, Qian S B. 2002. A quantative research and analysis method for marine phytoplankton: an introduction to Utermöhl method and its modification. Journal of Oceanography of Huanghai & Bohai Seas, 20(2): 105–112. (in Chinese with English abstract)

    Google Scholar 

  34. Sun J, Liu D Y, Ning X R, Liu C G. 2003. Phytoplankton in the Prydz Bay and the adjacent Indian sector of the southern ocean during the austral summer 2001/2002. Oceanologia et Limnologia Sinica, 34(5): 519–532. (in Chinese with English abstract)

    Google Scholar 

  35. Tilman D. 1977. Resource competition between plankton algae: an experimental and theoretical approach. Ecology, 58(2): 338–348.

    Google Scholar 

  36. Tseng Y F, Lin J, Dai M, Kao S J. 2014. Joint effect of freshwater plume and coastal upwelling on phytoplankton growth off the Changjiang River. Biogeosciences, 11(2): 409–423.

    Google Scholar 

  37. Villareal T A, Carpenter E J. 2003. Buoyancy regulation and the potential for vertical migration in the oceanic cyanobacterium Trichodesmium. Microbial Ecology, 45(1): 1–10.

    Google Scholar 

  38. Wang B D. 2006. Cultural eutrophication in the Changjiang (Yangtze River) plume: history and perspective. Estuarine, Coastal and Shelf Science, 69(3–4): 471–477.

    Google Scholar 

  39. Wang B D, Wang X L. 2007. Chemical hydrography of coastal upwelling in the East China Sea. Chinese Journal of Oceanology and Limnology, 25(1): 16–26.

    Google Scholar 

  40. Wang B D, Wang X L, Zhan R. 2003. Nutrient conditions in the Yellow Sea and the East China Sea. Estuarine, Coastal and Shelf Science, 58(1): 127–136.

    Google Scholar 

  41. Wang Y H, Wu H, Gao L, Shen F, Liang X S. 2019. Spatial distribution and physical controls of the spring algal blooming off the Changjiang River estuary. Estuaries and Coasts, 42(4): 1 066–1 083.

    Google Scholar 

  42. Welschmeyer N A. 1994. Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnology and Oceanography, 39(8): 1 985–1 992.

    Google Scholar 

  43. Wu H. 2015. Cross-shelf penetrating fronts: a response of buoyant coastal water to ambient pycnocline undulation. Journal of Geophysical Research: Oceans, 120(7): 5 101–5 119.

    Google Scholar 

  44. Xu Q, Sukigara C, Goes J I, do Rosario Gomes H, Zhu Y L, Wang S Q, Shen A, de Raús Maúre E, Matsuno T, Yuji W, Yoo S, Ishizaka J. 2019. Interannual changes in summer phytoplankton community composition in relation to water mass variability in the East China Sea. Journal of Oceanography, 75(1): 61–79.

    Google Scholar 

  45. Yang D Z, Yin B S, Chai F, Feng X R, Xue H J, Gao G D, Yu F. 2018. The onshore intrusion of Kuroshio subsurface water from February to July and a mechanism for the intrusion variation. Progress in Oceanography, 167: 97–115.

    Google Scholar 

  46. Yang D Z, Yin B S, Liu Z L, Bai T, Qi J F, Chen H Y. 2012. Numerical study on the pattern and origins of Kuroshio branches in the bottom water of southern East China Sea in summer. Journal of Geophysical Research: Oceans, 117(C2): C02014.

    Google Scholar 

  47. Yang D Z, Yin B S, Liu Z L, Feng X R. 2011. Numerical study of the ocean circulation on the East China Sea shelf and a Kuroshio bottom branch northeast of Taiwan in summer. Journal of Geophysical Research: Oceans, 116(C5): C05015.

    Google Scholar 

  48. Yang D Z, Yin B S, Sun J C, Zhang Y. 2013. Numerical study on the origins and the forcing mechanism of the phosphate in upwelling areas off the coast of Zhejiang province, China in summer. Journal of Marine Systems, 123-124: 1–18.

    Google Scholar 

  49. Zhang C S, Wang J T, Zhu D D, Wang X L, Li J. 2008. The preliminary analysis of nutrients in harmful algal blooms in the East China Sea in the spring and summer of 2005. Acta Oceanologica Sinica, 30(2): 153–159. (in Chinese with English abstract)

    Google Scholar 

  50. Zhang J, Liu S M, Ren J L, Wu Y, Zhang G L. 2007. Nutrient gradients from the eutrophic Changjiang (Yangtze River) Estuary to the oligotrophic Kuroshio waters and reevaluation of budgets for the East China Sea Shelf. Progress in Oceanography, 74(4): 449–478.

    Google Scholar 

  51. Zhang Q L, Liu H W, Qin S S, Yang D Z, Liu Z L. 2014. The study on seasonal characteristics of water masses in the western East China Sea shelf area. Acta Oceanologica Sinica, 33(11): 64–74.

    Google Scholar 

  52. Zhao Y, Yu R C, Kong F Z, Wei C J, Liu Z, Geng H X, Dai L, Zhou Z X, Zhang Q C, Zhou M J. 2019. Distribution patterns of picosized and nanosized phytoplankton assemblages in the East China Sea and the Yellow Sea: implications on the impacts of Kuroshio intrusion. Journal of Geophysical Research: Oceans, 124(2): 1 262–1 276.

    Google Scholar 

  53. Zhou F, Xue H J, Huang D J, Xuan J L, Ni X B, Xiu P, Hao Q. 2015. Cross-shelf exchange in the shelf of the East China Sea. Journal of Geophysical Research: Oceans, 120(3): 1 545–1 572.

    Google Scholar 

  54. Zhou Z X, Yu R C, Sun C J, Feng M, Zhou M J. 2019. Impacts of Changjiang River discharge and Kuroshio intrusion on the diatom and dinoflagellate blooms in the East China Sea. Journal of Geophysical Research: Oceans, 124(7): 5 244–5 257.

    Google Scholar 

  55. Zhou Z X, Yu R C, Zhou M J. 2017a. Resolving the complex relationship between harmful algal blooms and environmental factors in the coastal waters adjacent to the Changjiang River estuary. Harmful Algae, 62: 60–72.

    Google Scholar 

  56. Zhou Z X, Yu R C, Zhou M J. 2017b. Seasonal succession of microalgal blooms from diatoms to dinoflagellates in the East China Sea: a numerical simulation study. Ecological Modelling, 360: 150–162.

    Google Scholar 

  57. Zhu Z Y, Wu Y, Zhang J, Du J Z, Zhang G S. 2014. Reconstruction of anthropogenic eutrophication in the region off the Changjiang Estuary and central Yellow Sea: from decades to centuries. Continental Shelf Research, 72: 152–162.

    Google Scholar 

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Acknowledgment

Data and samples were collected onboard of R/V Xiangyanghong 18 implementing the open research cruise NORC2017-02 supported by NSFC Shiptime Sharing Project (project number: 41649902), We thank Mr. Gang QIAN for collecting phytoplankton water samples, and the two anonymous reviewers for their comments on improving this manuscript.

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Correspondence to Jun Sun.

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Supported by the National Key Research and Development Project of China (No. 2019YFC1407805), the National Natural Science Foundation of China (Nos. 41876134, 41676112, 41276124), the Key Project of Natural Science Foundation for Tianjin (No. 17JCZDJC40000), the University Innovation Team Training Program for Tianjin (No. TD12-5003), the Tianjin 131 Innovation Team Program (No. 20180314), and the Changjiang Scholar Program of Chinese Ministry of Education (No. T2014253) to SUN Jun

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Yue, J., Noman, M.A. & Sun, J. Kuroshio intrusion drives the Trichodesmium assemblage and shapes the phytoplankton community during spring in the East China Sea. J. Ocean. Limnol. 39, 536–549 (2021). https://doi.org/10.1007/s00343-020-9344-x

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Keyword

  • Kuroshio waters
  • phytoplankton
  • Trichodesmium
  • community shift