Skip to main content
SpringerLink
Log in

Effects of ambient DIN:DIP ratio on the nitrogen uptake of harmful dinoflagellate Prorocentrum minimum and Prorocentrum donghaiense in turbidistat

  • N:P Ratios, Nutrient Loads and Ecology
  • Published:
Chinese Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

The effects of varying nitrogen (N): phosphorus (P) ratios on the growth and N-uptake and assimilation of the harmful dinoflagellates Prorocentrum minimum and Prorocentrum donghaiense were examined in turbidistat culture experiments. Algal cultures were supplied with media containing PO 3−4 in various concentrations to obtain a wide range of N:P ratios. Experiments to determine rates of N uptake and assimilation of different N sources (NO −3 , NH +4 , urea and glycine by P. minimum and NO −3 , NH +4 by P. donghaiense) were conducted using 15N tracer techniques at each N:P ratio. The growth rates suggested nutrient limitation at both high and low N:P ratios relative to the Redfield ratio. On a diel basis, the growth of both species was regulated by the light-dark cycle, which may be a result of regulation of both lightdependent growth and light-independent nutrient uptake. Maximum growth rates of both species always occurred at the beginning of light phase. In P-rich medium (low N:P ratio), both species had higher N assimilation rates, suggesting N limitation. Low assimilation coefficients at high N:P ratios suggested P limitation of N uptake and assimilation. NO −3 and NH +4 contributed more than 90% of the total N uptake of P. minimum. Reduced N sources were more quickly assimilated than NO −3 . Highest average daily growth rates were recorded near an N:P ratio of 12 for both species. The N uptake rates of cultures at N:P ratios near Redfield ratio were more balanced with growth rates. The linkage between growth rates and N uptake/assimilation rates were conceptually described by the variation of cell N quota. The N:P ratios affect the N uptake and growth of Prorocentrum spp., and may regulate their bloom progression in eutrophic ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anderson D M, Burkholder J M, Cochlan W P, Glibert P M, Gobler C J, Heil C A, Kudela R M, Parsons M L, Rensel J E J, Townsend D W, Trainer V L, Vargo G A. 2008. Harmful algal blooms and eutrophication: Examining linkages from selected coastal regions of the united states. Harmful Algae, 8(SI): 39–53.

    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(4B): 704–726.

    Article  Google Scholar 

  • Bennett W N, Boraas M E. 1989. Comparison of population-dynamics between slow-growing and fast-growing strains of the rotifer Brachionus calyciflorus pallas in continuous culture. Oecologia., 81(4): 494–500.

    Article  Google Scholar 

  • Bulgakov N G, Levich A P. 1999. The nitrogen: Phosphorus ratio as a factor regulating phytoplankton community structure. Arch. Hydrobiol., 146(1): 3–22.

    Google Scholar 

  • Burns C L, Pennock J R, Lores E M, R M G. 2000. The effect of nitrogen source on the growth and toxicity of three potentially harmful dinoflagellates. J. Phycol., 36(3). (Abstract only)

  • Chisholm S W, Nobbs P A, Stross R G. 1975. Simulation of algal growth and competition in a phosphate-limited cyclostat. Abstracts of Papers of the American Chemical Society, 42–42.

  • Degens E T, Mopper K. 1976. Factors controlling distribution and early diagenesis of organic marine sediments. In: Riley J P, Chester R eds. Chemical oceanography, Vol.6. Academic London, New York, San Francisco. p.60–114.

    Google Scholar 

  • Doemel W N, Brooks A E. 1975. Detergent phosphorus and algal growth. Water Res., 9(8): 713–719.

    Article  Google Scholar 

  • Droop M R. 1968. Vitamin B12 and marine ecology 4. Kinetics of uptake growth and inhibition in Monochrysis lutheri. J. Mar. Biol. Assoc. U.K., 48: 689–733.

    Article  Google Scholar 

  • Droop M R. 1973. Some thoughts on nutrient limitation in algae. J. Phycol., 9(3): 264–272.

    Google Scholar 

  • Eppley R W, Renger E H. 1974. Nitrogen assimilation of an oceanic diatom in nitrogen-limited continuous culture. J. Phycol., 10(1): 15–23.

    Google Scholar 

  • Falkowski P G, Dubinsky Z, Wyman K. 1985. Growthirradiance relationships in phytoplankton. Limnol. Oceanogr., 30(2): 311–321.

    Article  Google Scholar 

  • Fan C, Glibert P M, Alexander J, Lomas M W. 2003a. Characterization of urease activity in three marine phytoplankton species, Aureococcus anophagefferens, Prorocentrum minimum, and Thalassiosira weissflogii. Mar. Biol., 142(5): 949–958.

    Google Scholar 

  • Fan C L, Glibert P M. 2005. Effects of light on nitrogen and carbon uptake during a Prorocentrum minimum bloom. Harmful Algae, 4(3): 629–641.

    Article  Google Scholar 

  • Fan C L, Glibert P M, Burkholder J M. 2003b. Characterization of the affinity for nitrogen, uptake kinetics, and environmental relationships for Prorocentrum minimum in natural blooms and laboratory cultures. Harmful Algae, 2(4): 283–299.

    Article  Google Scholar 

  • Fenaux R, Malara G, Claustre H. 1985. A turbidostat driven and controlled by microcomputer. Aquaculture, 48(1): 91–95.

    Article  Google Scholar 

  • Fisher T R, Peele E R, Ammerman J W, Harding L W. 1992. Nutrient limitation of phytoplankton in Chesapeake Bay. Mar. Ecol. Prog. Ser., 82(1): 51–63.

    Article  Google Scholar 

  • Frisch H L, Gotham I J. 1977. Periodic algal cyclostat populations. J. Theor. Biol., 66(4): 665–678.

    Article  Google Scholar 

  • Glibert P M, Anderson D M, Gentien P, Graneli E, Sellner K G. 2005. The global, complex phenomena of harmful algal blooms. Oceanography, 18(2): 136–147.

    Google Scholar 

  • Glibert P M, Burkholder J M. 2006. The complex relationships between increasing fertilization of the earth, coastal eutrophication and proliferation of harmful algal blooms. In: Graneli E, Turner J eds. Ecology of Harmful Algae. Springer. p.341–354.

  • Glibert P M, Burkholder J M, Graneli E, Anderson D M. 2008a. Advances and insights in the complex relationships between eutrophication and HABs: Preface to the special issue. Harmful Algae, 8(SI): 1–2.

    Article  Google Scholar 

  • Glibert P M, Capone D G. 1993. Mineralization and assimilation in aquatic, sediment, and wetland systems. In: Knowles R, Blackburn T H eds. Nitrogen Isotope Techniques. p.243–272. Academic Press.

  • Glibert P M, Harrison J, Heil C, Seitzinger S. 2006. Escalating worldwide use of urea—a global change contributing to coastal eutrophication. Biogeochemistry, 77(3): 441–463.

    Article  Google Scholar 

  • Glibert P M, Mayorga E, Seitzinger S. 2008b. Prorocentrum minimum tracks anthropogenic nitrogen and phosphorus inputs on a global basis: Application of spatially explicit nutrient export models. Harmful Algae, 8(SI): 33–38.

    Article  Google Scholar 

  • Glibert P M, Terlizzi D E. 1999. Cooccurrence of elevated urea levels and dinoflagellate blooms in temperate estuarine aquaculture ponds. Appl. Environ. Microbiol., 65(12): 5 594–5 596.

    Google Scholar 

  • Goldman J C, Glibert P M. 1982. Comparative rapid ammonium uptake by 4 species of marine-phytoplankton. Limnol. Oceanogr., 27(5): 814–827.

    Article  Google Scholar 

  • Gotham I J, Frisch H L. 1981. A simple-model for cell-volume and developmental compartments in nutrient limited cyclostat cultures of algae. J. Theor. Biol., 92(4): 435–467.

    Article  Google Scholar 

  • Gotham I J, Rhee G Y. 1981. Comparative kinetic-studies of phosphate-limited growth and phosphate-uptake in phytoplankton in continuous culture. J. Phycol., 17(3): 257–265.

    Article  Google Scholar 

  • Gotham I J, Rhee G Y. 1982. Effects of nitrate and phosphate limitation on cyclostat growth of 2 fresh-water diatoms. J. Gen. Microbiol., 128(1): 199–205.

    Google Scholar 

  • Guillard R R L, Ryther J H. 1962. Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can. J. Microbiol., 8(2): 229–239.

    Article  Google Scholar 

  • Hallegraeff G M. 1993. A review of harmful algal blooms and their apparent global increase. Phycologia, 32(2): 79–99.

    Article  Google Scholar 

  • Harding L W, Coats D W. 1988. Photosynthetic physiology of Prorocentrum mariae-lebouriae (dinophyceae) during its subpycnocline transport in Chesapeake Bay. J. Phycol., 24(1): 77–89.

    Article  Google Scholar 

  • Harding L W, Meeson B W, Tyler M A. 1983. Photoadaptation and diel periodicity of photosynthesis in the dinoflagellate Prorocentrum mariae-lebouriae. Mar. Ecol. Prog. Ser., 13(1): 73–85.

    Article  Google Scholar 

  • Hartig J H, Horvath F J. 1982. A preliminary assessment of Michigan phosphorus detergent ban. J. Water Pollut. Control Fed., 54(2): 193–197.

    Google Scholar 

  • Heil C A, Glibert P M, Fan C L. 2005. Prorocentrum minimum (pavillard) schiller—a review of a harmful algal bloom species of growing worldwide importance. Harmful Algae, 4(3): 449–470.

    Article  Google Scholar 

  • Heil C A, Revilla M, Glibert P M, Murasko S. 2007. Nutrient quality drives differential phytoplankton community composition on the southwest Florida shelf. Limnol. Oceanogr., 52(3): 1 067–1 078.

    Article  Google Scholar 

  • Heisler J, Glibert P M, Burkholder J M, Anderson D M, Cochlan W, Dennison W C, Dortch Q, Gobler C J, Heil C A, Humphries E, Lewitus A, Magnien R, Marshall H G, Sellner K, Stockwell D A, Stoecker D K, Suddleson M. 2008. Eutrophication and harmful algal blooms: A scientific consensus. Harmful Algae, 8(SI): 3–13.

    Article  Google Scholar 

  • Hill S H, Abbott M R, Denman K L. 1985. A computer-controlled turbidostat for the culture of planktonic algae. Can. J. Fish. Aquat. Sci., 42(4): 744–753.

    Article  Google Scholar 

  • Hirsbrunner M. 1981. A Chemostatanlage zur kontinuierlichen Kultur von Algen. Schweiz. Z. Hydrol., 43(2): 370–376.

    Article  Google Scholar 

  • Hodgkiss I J, Ho K C. 1997. Are changes in N:P ratios in coastal waters the key to increased red tide blooms? Hydrobiologia, 352: 141–147.

    Article  Google Scholar 

  • Jeong H J, Du Y Y, Park J Y, Song J Y, Kim S T, Lee S H, Kim K Y, Yih W H. 2005a. Feeding by phototrophic red-tide dinoflagellates: Five species newly revealed and six species previously known to be mixotrophic. Aquat. Microb. Ecol., 40(2): 133–150.

    Article  Google Scholar 

  • Jeong H J, Park J Y, Nho J H, Park M O, Ha J H, Seong K A, Jeng C, Seong C N, Lee K Y, Yih W H. 2005b. Feeding by red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquat. Microb. Ecol., 41(2): 131–143.

    Article  Google Scholar 

  • Kalyuzhin V A. 1998. The growth of a turbidostat yeast culture in the presence of high concentrations of various compounds in a steady-state regime and under osmotic shock. Microbiology, 67(5): 499–503.

    Google Scholar 

  • Lagus A, Suomela J, Weithoff G, Heikkila K, Helminen H, Sipura J. 2004. Species-specific differences in phytoplankton responses to N and P enrichments and the N:P ratio in the Archipelago sea, Northern Baltic Sea. J. Plankton Res., 26(7): 779–798.

    Article  Google Scholar 

  • Lane L, Rhoades S, Thomas C, Van Heukelem L. 2000. Analytical Services Laboratory Standard Operating Procedures. University of Maryland Center for Environmental Science, Cambridge, Maryland.

    Google Scholar 

  • Li A S, Stoecker D K, Coats D W, Adam E J. 1996. Ingestion of fluorescently labeled and phycoerythrin-containing prey by mixotrophic dinoflagellates. Aquat. Microb. Ecol., 10(2): 139–147.

    Article  Google Scholar 

  • Li J, Glibert P M, Zhou M. 2010. Temporal and spatial variability in nitrogen uptake kinetics during dinoflagellate blooms in the east China sea. Harmful Algae, 9(6): 531–539.

    Article  Google Scholar 

  • Li J, Glibert P M, Zhou M, Lu S, Lu D. 2009. Relationships between nitrogen and phosphorus forms and ratios and the development of dinoflagellate blooms in the East China Sea. Mar. Ecol. Prog. Ser., 383: 11–26.

    Article  Google Scholar 

  • Lindroth P, Mopper K. 1979. High-performance liquid-chromatographic determination of subpicomole amounts of amino-acids by precolumn fluorescence derivatization with ortho-phthaldialdehyde. Anal. Chem., 51(11): 1 667–1 674.

    Article  Google Scholar 

  • Litke D W. 1999. Review of phosphorus control measures in the united states and their effects on water quality, U.S. Geological Survey. U.S. Geological Survey, Water-Resources Investigations Report 99-4007, 38p.

  • Lomas M W, Glibert P M. 1999a. Interactions between NH +4 and NO uptake and assimilation: Comparison of diatoms and dinoflagellates at several growth temperatures. Mar. Biol., 133(3): 541–551.

    Article  Google Scholar 

  • Lomas M W, Glibert P M. 1999b. Temperature regulation of nitrate uptake: A novel hypothesis about nitrate uptake and reduction in cool-water diatoms. Limnol. Oceanogr., 44(3): 556–572.

    Article  Google Scholar 

  • Lomas M W, Glibert P M. 2000. Comparisons of nitrate uptake, storage, and reduction in marine diatoms and flagellates. J. Phycol., 36(5): 903–913.

    Article  Google Scholar 

  • Lu D D, Goebel J. 2001. Five red tide species in genus Prorocentrum including the description of Prorocentrum donghaiense Lu sp. nov. from the East China Sea. Chin. J. Oceanol. Limnol., 19(4): 337–344.

    Article  Google Scholar 

  • Maki A W, Porcella D B, Wendt R H. 1984. The impact of detergent phosphorus bans on receiving water-quality. Water Res., 18(7): 893–903.

    Article  Google Scholar 

  • Malone T C, Garside C, Haines K C, Roels O A. 1975. Nitrate uptake and growth of Chaetoceros sp. in large outdoor continuous cultures. Limnol. Oceanogr., 20(7): 9–19.

    Article  Google Scholar 

  • McDuff R E, Chisholm S W. 1982. The calculation of insitu growth-rates of phytoplankton populations from fractions of cells undergoing mitosis—a clarification. Limnol. Oceanogr., 27(4): 783–788.

    Article  Google Scholar 

  • Monod J. 1950. La technique de culture continue theorie et applications. Annales de l’Institut Pasteur, 79(4): 390–410.

    Google Scholar 

  • NRC. 2000. Clean coastal waters: Understanding and reducing the effects of nutrient pollution. National Academies Press.

  • Paasche E, Bryceson I, Tangen K. 1984. Interspecific variation in dark nitrogen uptake by dinoflagellates. J. Phycol., 20(3): 394–401.

    Article  Google Scholar 

  • Paerl H W, Valdes L M, Joyner A R, Piehler M F. 2004. Solving problems resulting from solutions: Evolution of a dual nutrient management strategy for the eutrophying Neuse River estuary, North Carolina. Environ. Sci. Technol., 38(11): 3 068–3 073.

    Article  Google Scholar 

  • Phillips D J H, Tanabe S. 1989. Aquatic pollution in the Far-East. Mar. Pollut. Bull., 20(7): 297–303.

    Article  Google Scholar 

  • Revilla M, Alexander J, Glibert P M. 2005. Urea analysis in coastal waters: Comparison of enzymatic and direct methods. Limnol. and Oceanogr-Meth., 3: 290–299.

    Article  Google Scholar 

  • Rhee G Y. 1978. The continuous culture in phytoplankton ecology. In: Droop M R, Jannasch H W eds. Advances in Aquatic Microbiology. Academic Press, London. Vol.2, p.151–203.

    Google Scholar 

  • Rhee G Y. 1973. Continuous culture study of phosphate uptake, growth-rate and polyphosphate in Scenedesmus sp. J. Phycol., 9(4): 495–506.

    Google Scholar 

  • Rhee G Y, Gotham I J. 1981. The effect of environmental-factors on phytoplankton growth—light and the interactions of light with nitrate limitation. Limnol. Oceanogr., 26(4): 649–659.

    Article  Google Scholar 

  • Salerno M, Stoecker D K. 2009. Ectocellular glucosidase and peptidase activity of the mixotrophic dinoflagellate Prorocentrum minimum (dinophyceae). J. Phycol., 45(1): 34–45.

    Article  Google Scholar 

  • Sciandra A. 1991. Coupling and uncoupling between nitrate uptake and growth-rate in Prorocentrum minimum (dinophyceae) under different frequencies of pulsed nitrate supply. Mar. Ecol. Prog. Ser., 72(3): 261–269.

    Article  Google Scholar 

  • Sharfstein B, Roels O A, Harris V, Lee V. 1977. Effect of detergent legislation on phosphorus in effluent and receiving waters. J. Water Pollut. Control Fed., 49(9): 2 017–2 021.

    Google Scholar 

  • Skipnes O, Eide I, Jensen A. 1980. Cage culture turbidostat—a device for rapid-determination of algal growth-rate. Appl. Environ. Microbiol., 40(2): 318–325.

    Google Scholar 

  • Smayda T J. 1997. Harmful algal blooms: Their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol. Oceanogr., 42(5): 1 137–1 153.

    Google Scholar 

  • Smayda T J. 2002. Adaptive ecology, growth strategies and the global bloom expansion of dinoflagellates. J. Oceanogr., 58(2): 281–294.

    Article  Google Scholar 

  • Stoecker D K, Gustafson D E. 2003. Cell-surface proteolytic activity of photosynthetic dinoflagellates. Aquat. Microb. Ecol., 30(2): 175–183.

    Article  Google Scholar 

  • Stoecker D K, Li A S, Coats D W, Gustafson D E, Nannen M K. 1997. Mixotrophy in the dinoflagellate Prorocentrum minimum. Mar. Ecol. Prog. Ser., 152(1–3): 1–12.

    Article  Google Scholar 

  • Suttle C A, Harrison P J. 1988. Ammonium and phosphate-uptake rates, N-P supply ratios, and evidence for N-limitation and P-limitation in some oligotrophic lakes. Limnol. Oceanogr., 33(2): 186–202.

    Article  Google Scholar 

  • Tyler M A, Seliger H H. 1978. Annual subsurface transport of a red tide dinoflagellate to its bloom area—water circulation patterns and organism distributions in Chesapeake Bay. Limnol. Oceanogr., 23(2): 227–246.

    Article  Google Scholar 

  • USDA. 2008. Fertilizer consumption and use—By year. United states department of agriculture. http://www.ers.usda.gov/Data/FertilizerUse/.

  • Vrede T, Ballantyne A, Mille-Lindblom C, Algesten G, Gudasz C, Lindahl S, Brunberg A K. 2009. Effects of N: P loading ratios on phytoplankton community composition, primary production and N fixation in a eutrophic lake. Freshw. Biol., 54(2): 331–344.

    Article  Google Scholar 

  • Watson T G. 1972. Present status and future prospects of turbidostat. J. Appl. Chem. Biotechnol. Abstr., 22(2): 229.

    Article  Google Scholar 

  • Yoshida T, Rao B S M, Ohasa S, Taguchi H. 1979. Dynamic analysis of a mixed culture in chemostat. J. Ferment. Technol., 57(6): 546–553.

    Google Scholar 

  • Zhou M, Yan T, Zou J. 2003. Preliminary analysis of the characteristics of red tide areas in Changjiang River estuary and its adjacent sea. Chin. J. Appl. Ecol., 14(7): 1 031–1 038. (in Chinese)

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Horn Point Laboratory, University of Maryland Center for Environmental Science, PO Box 775, Cambridge, MD, 21613, USA

    Ji Li  (李纪), Patricia M. Glibert & Jeffrey A. Alexander

Authors
  1. Ji Li  (李纪)
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patricia M. Glibert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jeffrey A. Alexander
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ji Li  (李纪).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, J., Glibert, P.M. & Alexander, J.A. Effects of ambient DIN:DIP ratio on the nitrogen uptake of harmful dinoflagellate Prorocentrum minimum and Prorocentrum donghaiense in turbidistat. Chin. J. Ocean. Limnol. 29, 746–761 (2011). https://doi.org/10.1007/s00343-011-0504-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-011-0504-x

Keyword

Search

Navigation