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Regeneration and utilization of nutrients during collapse of a Mesodinium rubrum red tide and its influence on phytoplankton species composition

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Abstract

High-biomass red tides occur frequently in some semi-enclosed bays of Hong Kong where ambient nutrients are not high enough to support such a high phytoplankton biomass. These high-biomass red tides release massive inorganic nutrients into local waters during their collapse. We hypothesized that the massive inorganic nutrients released from the collapse of red tides would fuel growth of other phytoplankton species. This could influence phytoplankton species composition. We tested the hypothesis using a red tide event caused by Mesodinium rubrum (M. rubrum) in a semi-enclosed bay, Port Shelter. The red tide patch had a cell density as high as 5.0×105 cells L−1, and high chlorophyll a (63.71 μg L−1). Ambient inorganic nutrients (nitrate: \(\rm{NO}_3^-\), ammonium: \(\rm{NH}_4^+\), phosphate: \(\rm{PO}_4^{3-}\), silicate: \(\rm{SiO}_4^{3-}\)) were low both in the red tide patch and the non-red-tide patch (clear waters outside the red tide patch). Nutrient addition experiments were conducted by adding all the inorganic nutrients to water samples from the two patches followed by incubation for 9 days. The results showed that the addition of inorganic nutrients did not sustain high M. rubrum cell density, which collapsed after day 1, and did not drive M. rubrum in the non-red-tide patch sample to the same high-cell density in the red tide patch sample. This confirmed that nutrients were not the driving factor for the formation of this red tide event, or for its collapse. The death of M. rubrum after day 1 released high concentrations of \(\rm{NO}_3^-\), \(\rm{PO}_4^{3-}\), \(\rm{SiO}_4^{3-}\), \(\rm{NH}_4^+\), and urea. Bacterial abundance and heterotrophic activity increased, reaching the highest on day 3 or 4, and decreased as cell density of M. rubrum declined. The released nutrients stimulated growth of diatoms, such as Chaetoceros affinis var. circinalis, Thalassiothrix frauenfeldii, and Nitzschia sp., particularly with additions of \(\rm{SiO}_4^{3-}\) treatments, and other species. These results demonstrated that initiation of M. rubrum red tides in the bay was not directly driven by nutrients. However, the massive inorganic nutrients released from the collapse of the red tide could induce a second bloom in low-ambient nutrient water, influencing phytoplankton species composition.

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References

  • Adams H E, Crump B C, Kling G W. 2010. Temperature controls on aquatic bacterial production and community dynamics in arctic lakes and streams. Environ Microbiol, 12: 1319–1333

    Article  Google Scholar 

  • Anderson D M, Glibert P M, Burkholder J M. 2002. Harmful algal blooms and eutrophication: Nutrient sources, composition, and consequences. Estuaries, 25: 704–726

    Article  Google Scholar 

  • Bratbak G, Wilson W H, Heldal M. 1996. Viral control of Emiliania huxleyi blooms? J Mar Syst, 9: 75–81

    Article  Google Scholar 

  • Buchan A, LeCleir G R, Gulvik C A, González J M. 2014. Master recyclers: Features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol, 12: 686–698

    Article  Google Scholar 

  • Chrzanowski T, Kyle M. 1996. Ratios of carbon, nitrogen and phosphorus in Pseudomonas fluorescens as a model for bacterial element ratios and nutrient regeneration. Aquat Microb Ecol, 10: 115–122

    Article  Google Scholar 

  • Crawford D W, Purdie D A, Lockwood A P M, Weissman P. 1997. Recurrent red-tides in the southampton water estuary caused by the phototrophic ciliate Mesodinium rubrum. Estuar Coast Shelf Sci, 45: 799–812

    Article  Google Scholar 

  • Dagenais-Bellefeuille S, Morse D. 2013. Putting the N in dinoflagellates. Front Microbiol, 4: 369

    Article  Google Scholar 

  • Dierssen H, McManus G B, Chlus A, Qiu D, Gao B C, Lin S. 2015. Space station image captures a red tide ciliate bloom at high spectral and spatial resolution. Proc Natl Acad Sci USA, 112: 14783–14787

    Article  Google Scholar 

  • Donald D B, Bogard M J, Finlay K, Bunting L, Leavitt P R. 2013. Phytoplankton-specific response to enrichment of phosphorus-rich surface waters with ammonium, nitrate, and urea. Plos One, 8: e53277–14

    Article  Google Scholar 

  • Donald D B, Bogard M J, Finlay K, Leavitt P R. 2011. Comparative effects of urea, ammonium, and nitrate on phytoplankton abundance, community composition, and toxicity in hypereutrophic freshwaters. Limnol Oceanogr, 56: 2161–2175

    Article  Google Scholar 

  • Dugdale R C, Wilkerson F P, Hogue V E, Marchi A. 2007. The role of ammonium and nitrate in spring bloom development in San Francisco Bay. Estuar Coast Shelf Sci, 73: 17–29

    Article  Google Scholar 

  • EPD. 2017. Marine Water Quality in Hong Kong in 2016. Monitoring Group, Water Policy and Planning Group, EPD, HKSAR

    Google Scholar 

  • Fenchel T, Hansen P J. 2006. Motile behaviour of the bloom-forming ciliate Mesodinium rubrum. Mar Biol Res, 2: 33–40

    Article  Google Scholar 

  • Flynn K J, Stoecker D K, Mitra A, Raven J A, Glibert P M, Hansen P J, Granéli E, Burkholder J M. 2013. Misuse of the phytoplankton-zooplankton dichotomy: The need to assign organisms as mixotrophs within plankton functional types. J Plankton Res, 35: 3–11

    Article  Google Scholar 

  • Fuhrman J A, Azam F. 1982. Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: Evaluation and field results. Mar Biol, 66: 109–120

    Article  Google Scholar 

  • Fukuda R, Ogawa H, Nagata T, Koike I. 1998. Direct determination of carbon and nitrogen contents of natural bacterial assemblages in marine environments. Appl Environ Microbiol, 64: 3352–3358

    Google Scholar 

  • Glibert P M. 1997. Interactions of top-down and bottom-up control in planktonic nitrogen cycling. Hydrobiologia, 363: 1–12

    Article  Google Scholar 

  • Glibert P, Seitzinger S, Heil C, Burkholder J A, Parrow M, Codispoti L, Kelly V. 2005. The role of eutrophication in the global proliferation of harmful algal blooms. Oceanography, 18: 198–209

    Article  Google Scholar 

  • Glibert P M, Wilkerson F P, Dugdale R C, Parker A E, Alexander J, Blaser S, Murasko S. 2014. Phytoplankton communities from San Francisco Bay Delta respond differently to oxidized and reduced nitrogen substrates—Even under conditions that would otherwise suggest nitrogen sufficiency. Front Mar Sci, 1: 1–16

    Article  Google Scholar 

  • Glibert P M, Wilkerson F P, Dugdale R C, Raven J A, Dupont C L, Leavitt P R, Parker A E, Burkholder J A M, Kana T M. 2016. Pluses and minuses of ammonium and nitrate uptake and assimilation by phytoplankton and implications for productivity and community composition, with emphasis on nitrogen-enriched conditions. Limnol Oceanogr, 61: 165–197

    Article  Google Scholar 

  • Gustafson D E, Stoecker D K, Johnson M D, Van Heukelem W F, Sneider K. 2000. Cryptophyte algae are robbed of their organelles by the marine ciliate Mesodinium rubrum. Nature, 405: 1049–1052

    Article  Google Scholar 

  • Herfort L, Peterson T D, Prahl F G, McCue L A, Needoba J A, Crump B C, Roegner G C, Campbell V, Zuber P. 2012. Red waters of Myrionecta rubra are biogeochemical hotspots for the columbia river estuary with impacts on primary/secondary productions and nutrient cycles. Estuar Coast, 35: 878–891

    Article  Google Scholar 

  • Huang C, Qi Y. 1997. The abundance cycle and influence factors on red tide phenomena of Noctiluca scintillans (Dinophyceae) in Dapeng Bay, the South China Sea. J Plankton Res, 19: 303–318

    Article  Google Scholar 

  • Jiang H, Johnson M D. 2017. Jumping and overcoming diffusion limitation of nutrient uptake in the photosynthetic ciliate Mesodinium rubrum. Limnol Oceanogr, 62: 421–436

    Article  Google Scholar 

  • Knap A H, Michaels A, Close A R, Ducklow H, Dickson A G. 1996. Protocols for the joint global ocean flux study (JGOFS) core measurements. JGOFS, Reprint of the IOC Manuals and Guides No. 29, UNESCO 1994, 19

    Google Scholar 

  • Lai Z, Yin K. 2014. Physical-biological coupling induced aggregation mechanism for the formation of high biomass red tides in low nutrient waters. Harmful Algae, 31: 66–75

    Article  Google Scholar 

  • Liu H, Song X, Huang L, Tan Y, Zhang J. 2011. Phytoplankton biomass and production in northern South China Sea during summer: Influenced by Pearl River discharge and coastal upwelling. Acta Ecologica Sin, 31: 133–136

    Article  Google Scholar 

  • Lomas M W, Glibert P M. 1999. Temperature regulation of nitrate uptake: A novel hypothesis about nitrate uptake and reduction in cool-water diatoms. Limnol Oceanogr, 44: 556–572

    Article  Google Scholar 

  • Lomas M W, Rumbley C J, Glibert P M. 2000. Ammonium release by nitrogen sufficient diatoms in response to rapid increases in irradiance. J Plankton Res, 22: 2351–2366

    Article  Google Scholar 

  • Mccarthy J J, Goldman J C. 1979. Nitrogenous nutrition of marine phytoplankton in nutrient-depleted waters. Science, 203: 670–672

    Article  Google Scholar 

  • Mitra A, Flynn K J. 2010. Modelling mixotrophy in harmful algal blooms: More or less the sum of the parts? J Mar Syst, 83: 158–169

    Article  Google Scholar 

  • Myung G, Kim H S, Park J W, Park J S, Yih W. 2013. Sequestered plastids in Mesodinium rubrum are functionally active up to 80 days of phototrophic growth without cryptomonad prey. Harmful Algae, 27: 82–87

    Article  Google Scholar 

  • Parker A E, Hogue V E, Wilkerson F P, Dugdale R C. 2012. The effect of inorganic nitrogen speciation on primary production in the San Francisco Estuary. Estuar Coast Shelf Sci, 104-105: 91–101

    Article  Google Scholar 

  • Porter K G, Feig Y S. 1980. The use of DAPI for identifying and counting aquatic microflora1. Limnol Oceanogr, 25: 943–948

    Article  Google Scholar 

  • Price N M, Harrison P J. 1987. Comparison of methods for the analysis of dissolved urea in seawater. Mar Biol, 94: 307–317

    Article  Google Scholar 

  • Raven J A. 1991. Physiology of inorganic C acquisition and implications for resource use efficiency by marine phytoplankton: Relation to increased CO2 and temperature. Plant Cell Environ, 14: 779–794

    Article  Google Scholar 

  • Raven J A. 2011. The cost of photoinhibition. Physiologia Plantarum, 142: 87–104

    Article  Google Scholar 

  • Saba G K, Steinberg D K, Bronk D A, Place A R. 2011. The effects of harmful algal species and food concentration on zooplankton grazer production of dissolved organic matter and inorganic nutrients. Harmful Algae, 10: 291–303

    Article  Google Scholar 

  • Shiah F K, Ducklow H W. 1994. Temperature and substrate regulation of bacterial abundance, production and specific growth rate in Chesapeake Bay, USA. Mar Ecol Prog Ser, 103: 297–308

    Article  Google Scholar 

  • Sinsabaugh R L, Shah J J F. 2010. Integrating resource utilization and temperature in metabolic scaling of riverine bacterial production. Ecology, 91: 1455–1465

    Article  Google Scholar 

  • Slawyk G, Macisaac J J. 1972. Comparison of two automated ammonium methods in a region of coastal upwelling. Deep Sea Res Oceanogr Abstr, 19: 521–524

    Article  Google Scholar 

  • Tong M, Smith J L, Kulis D M, Anderson D M. 2015. Role of dissolved nitrate and phosphate in isolates of Mesodinium rubrum and toxin-producing Dinophysis acuminata. Aquat Microb Ecol, 75: 169–185

    Article  Google Scholar 

  • Vrede K, Heldal M, Norland S, Bratbak G. 2002. Elemental composition (C, N, P) and cell volume of exponentially growing and nutrient-limited bacterioplankton. Appl Environ Microbiol, 68: 2965–2971

    Article  Google Scholar 

  • Wilkerson F P, Dugdale R C, Hogue V E, Marchi A. 2006. Phytoplankton blooms and nitrogen productivity in San Francisco Bay. Estuar Coast, 29: 401–416

    Article  Google Scholar 

  • Yih W, Kim H S, Jeong H J, Myung G, Kim Y G. 2004. Ingestion of cryptophyte cells by the marine photosynthetic ciliate Mesodinium rubrum. Aquat Microb Ecol, 36: 165–170

    Article  Google Scholar 

  • Yih W, Kim H S, Myung G, Park J W, Yoo Y D, Jeong H J. 2013. The red-tide ciliate Mesodinium rubrum in Korean coastal waters. Harmful Algae, 30: S53–S61

    Article  Google Scholar 

  • Yin K. 2003. Influence of monsoons and oceanographic processes on red tides in Hong Kong waters. Mar Ecol Prog Ser, 262: 27–41

    Article  Google Scholar 

  • Yin K, Song X X, Liu S, Kan J, Qian P Y. 2008. Is inorganic nutrient enrichment a driving force for the formation of red tides? Harmful Algae, 8: 54–59

    Article  Google Scholar 

Download references

Acknowledgements

We acknowledge Sam Cheung and Mandy Tsoi for providing the assistance during field sampling and the nutrient addition experiments. This study was supported by the Guangdong-National Science Foundation of China (Grant Nos. U1701247) and the National Natural Science Foundation of China (Grant Nos. 91328203) and the International Science and Technology Cooperation Program of Guangdong (Grant No. 2013B051000042). Xiuxian Song was supported by the National Natural Science Foundation of China (Grant Nos. 50339040 & 40025614).

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Correspondence to Xiuxian Song, Hao Liu or Kedong Yin.

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Zhang, Y., Song, X., Harrison, P.J. et al. Regeneration and utilization of nutrients during collapse of a Mesodinium rubrum red tide and its influence on phytoplankton species composition. Sci. China Earth Sci. 61, 1384–1396 (2018). https://doi.org/10.1007/s11430-017-9233-x

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  • DOI: https://doi.org/10.1007/s11430-017-9233-x

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