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Ammonium, nitrate and phytoplankton interactions in a freshwater tidal estuarine zone: potential effects of cultural eutrophication

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Abstract

Nitrate and ammonium are the most important nitrogen sources for phytoplankton growth. Differential utilization of inorganic nitrogenous compounds by phytoplankton has been observed and may have significant impacts on primary productivity at local scales. We used enrichment experiments with natural phytoplankton populations from the freshwater tidal zone of the Guadiana estuary, a coastal ecosystem increasingly subjected to anthropogenic influences, to study the effects of nitrate and ammonium on N-consumption and phytoplankton growth. In addition, we used combined additions of nitrate and ammonium to understand the inhibitory effect of ammonium over nitrate uptake. Ammonium concentrations in the freshwater tidal reaches of the Guadiana estuary throughout the sampling period were too low to exert an inhibitory effect on nitrate uptake or a toxic effect on phytoplankton growth. Nitrate was clearly the main nitrogen source for phytoplankton at the study site. Overall, nitrate seemed to become limiting at concentrations lower than 20 μM and N-limitation was particularly significant during summer. A trend of decreasing nitrate uptake with increasing ammonium concentrations and uptake suggested an overall preference for ammonium. However, preference for ammonium was group-specific, and it was observed mainly in green algae and cyanobacteria. In fact, cyanobacteria relied only on ammonium as their N-source. On the contrary, diatoms preferred nitrate, and did not respond to ammonium additions. The increasing eutrophication in the Guadiana estuary and particularly increased inputs of nitrogen as ammonium due to urban waste effluents may result in a shift in phytoplankton community composition, towards a dominance of cyanobacteria and green algae.

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References

  • Admiraal W (1977) Tolerance of estuarine benthic diatoms to high concentrations of ammonia, nitrite ion, nitrate ion and orthophosphate. Mar Biol 43:307–315

    Article  CAS  Google Scholar 

  • Baek SH, Shimode S, Han M-S, Kikuchi T (2008) Growth of dinoflagellates, Ceratium furca and Ceratium fusus in Sagami Bay, Japan: the role of nutrients. Harmful Algae 7:729–739

    Article  CAS  Google Scholar 

  • Balode M, Purina I, Béchemin C, Maestrini SY (1998) Effects of nutrient enrichment on the growth rates and community structure of summer phytoplankton from the Gulf of Riga, Baltic Sea. J Plankton Res 20:2251–2272

    Article  CAS  Google Scholar 

  • Barbosa AB, Domingues RB, Galvão HM (2010) Environmental forcing of phytoplankton in a Mediterranean estuary (Guadiana estuary, south-western Iberia): a decadal study of climatic and anthropogenic influences. Est Coasts 33:324–341

    Article  CAS  Google Scholar 

  • Blasco D, Conway HL (1982) Effect of ammonium on the regulation of nitrate assimilation in natural phytoplankton populations. J Exp Mar Biol Ecol 61:157–168

    Article  CAS  Google Scholar 

  • Borsuk ME, Stow CA, Reckhow KH (2004) Confounding effect of flow on estuarine response to nitrogen loading. J Environ Eng 130:605–614

    Article  CAS  Google Scholar 

  • Carpenter EJ, Dunham S (1985) Nitrogenous nutrient uptake, primary production, and species composition of phytoplankton in the Carmans River estuary, Long Island, New York. Limnol Oceanogr 30:513–526

    Article  CAS  Google Scholar 

  • Chang FH, McLean M (1997) Growth responses of Alexandrium minutum (Dinophyceae) as a function of three different nitrogen sources and irradiance. N Z J Mar Freshw Res 31:1–7

    Article  CAS  Google Scholar 

  • Cloern JE (2001) Our evolving conceptual model of the coastal eutrophication problem. Mar Ecol Prog Ser 210:223–253

    Article  CAS  Google Scholar 

  • Dokulil MT, Teubner K (2000) Cyanobacterial dominance in lakes. Hydrobiologia 438:1–12

    Article  CAS  Google Scholar 

  • Domingues RB, Galvão H (2007) Phytoplankton and environmental variability in a dam regulated temperate estuary. Hydrobiologia 586:117–134

    Article  CAS  Google Scholar 

  • Domingues RB, Barbosa A, Galvão H (2005) Nutrients, light and phytoplankton succession in a temperate estuary (the Guadiana, south-western Iberia). Est Coast Shelf Sci 64:249–260

    Article  Google Scholar 

  • Domingues RB, Anselmo TA, Barbosa AB, Sommer U, Galvão HM (2010) Nutrient limitation of phytoplankton growth in the freshwater tidal zone of a turbid, Mediterranean estuary. Est Coast Shelf Sci. doi:10.1016/j.ecss.2010.10.033

  • Dortch Q (1982) Response of marine phytoplankton to nitrogen deficiency: decreased nitrate uptake vs. enhanced ammonium uptake. Mar Biol 70:13–19

    Article  CAS  Google Scholar 

  • Dortch Q (1990) The interaction between ammonium and nitrate uptake in phytoplankton. Mar Ecol Prog Ser 61:183–201

    Article  CAS  Google Scholar 

  • Dortch Q, Clayton JR Jr, Thoresen SS, Ahmed SI (1984) Species differences in accumulation of nitrogen pools in phytoplankton. Mar Biol 81:237–250

    Article  CAS  Google Scholar 

  • Dugdale RC, Goering JJ (1967) Uptake of new and regenerated forms of nitrogen in primary production. Limnol Oceanogr 12:196–206

    Article  CAS  Google Scholar 

  • Dugdale RC, Wilkerson FP, Hogue VE, Marchi A (2007) The role of ammonium and nitrate in spring bloom development in San Francisco Bay. Est Coast Shelf Sci 73:17–29

    Article  Google Scholar 

  • Flores E, Herrero A (2005) Nitrogen assimilation and nitrogen control in cyanobacteria. Biochem Soc Trans 33:164–167

    Article  PubMed  CAS  Google Scholar 

  • Flynn KJ, Fasham MJR, Hipkin CR (1997) Modelling the interactions between ammonium and nitrate uptake in marine phytoplankton. Philos Trans R Soc Lond B 352:1625–1645

    Article  CAS  Google Scholar 

  • Fowler J, Cohen L (1990) Practical statistics for field biology. Wiley, London

    Google Scholar 

  • Grasshoff K, Ehrhardt M, Kremling K (1983) Methods of seawater analysis. Verlag Chemie, Weinheim

    Google Scholar 

  • Haas LW (1982) Improved epifluorescence microscopy for observing planktonic micro-organisms. Ann Inst Oceanogr 58:261–266

    Google Scholar 

  • Hillebrand H, Sommer U (1996) Nitrogenous nutrition of the potentially toxic diatom Pseudonitzschia pungens f. multiseries Hasle. J Plankton Res 18:295–391

    Article  Google Scholar 

  • Hyenstrand P, Burkert U, Pettersson A, Blomqvist P (2000) Competition between the green alga Scenedesmus and the cyanobacterium Synechococcus under different modes of inorganic nitrogen supply. Hydrobiologia 435:91–98

    Article  Google Scholar 

  • Incharoensakdi A, Wangsupa J (2003) Nitrate uptake by the halotolerant cyanobacterium Aphanothece halophytica grown under non-stress and salt-stress conditions. Curr Microbiol 47:255–259

    Article  PubMed  CAS  Google Scholar 

  • Intergovernmental Panel on Climate Change (IPCC) (2001) Climate change 2001: the scientific basis. Cambridge University Press, Cambridge

  • Leong SCY, Taguchi S (2004) Response of the dinoflagellate Alexandrium tamarense to a range of nitrogen sources and concentrations: growth rate, chemical carbon and nitrogen, and pigments. Hydrobiologia 515:215–224

    Article  CAS  Google Scholar 

  • Maguer J-F, L’Helguen S, Waeles M, Morin P, Riso R, Caradec J (2009) Size-fractionated phytoplankton biomass and nitrogen uptake in response to high nutrient load in the North Biscay Bay in spring. Cont Shelf Res 29:1103–1110

    Article  Google Scholar 

  • McCarthy J, Taylor W, Taft J (1977) Nitrogenous nutrition of the plankton in the Chesapeake Bay. I. Nutrient availability and phytoplankton preferences. Limnol Oceanogr 22:996–1011

    Article  CAS  Google Scholar 

  • Morales JA (1995) Sedimentología del estuario del río Guadiana. Ph.D. thesis, University of Huelva, 322 p. (in Spanish)

  • Nixon SW (1995) Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia 41:199–219

    Google Scholar 

  • Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford

    Google Scholar 

  • Pennock JR (1987) Temporal and spatial variability in phytoplankton ammonium and nitrate uptake in the Delaware Estuary. Est Coast Shelf Sci 24:841–857

    Article  CAS  Google Scholar 

  • Probyn TA (1985) Nitrogen uptake by size-fractionated phytoplankton populations in the southern Benguela upwelling system. Mar Ecol Prog Ser 22:249–258

    Article  CAS  Google Scholar 

  • Tada K, Suksomjit M, Ichimi K, Funaki Y, Montani S, Yamada M, Harrison PJ (2009) Diatoms grow faster using ammonium in rapidly flushed eutrophic Dokai Bay, Japan. J Oceanogr 65:885–891

    Article  CAS  Google Scholar 

  • Takeda S, Kamatani A, Kawanobe K (1995) Effects of nitrogen and iron enrichments on phytoplankton communities in the northwestern Indian Ocean. Mar Chem 50:229–241

    Article  CAS  Google Scholar 

  • Taub FB (2009) Community metabolism of aquatic closed ecological systems: effects of nitrogen sources. Adv Space Res 44:949–957

    Article  CAS  Google Scholar 

  • Torres-Valdés S, Purdie DA (2006) Nitrogen removal by phytoplankton uptake through a temperate non-turbid estuary. Est Coast Shelf Sci 70:473–486

    Article  Google Scholar 

  • Toscas PJ (2008) Spatial modelling of the probability of obtaining a detectable concentration of ammonia in Moreton Bay, Australia. Environ Monit Assess 137:379–385

    Article  PubMed  CAS  Google Scholar 

  • Twomey LJ, Piehler MF, Paerl HW (2005) Phytoplankton uptake of ammonium, nitrate and urea in the Neuse River Estuary, NC, USA. Hydrobiologia 533:123–134

    Article  CAS  Google Scholar 

  • Utermöhl H (1958) Zur Vervollkommung der quantitativen Phytoplankton-Methodik. Verh Internat Verein Limnol 9:1–38

    Google Scholar 

  • Venrick EL (1978) How many cells to count? In: Sournia A (ed) Phytoplankton manual. UNESCO, Paris, pp 167–180

    Google Scholar 

  • Wafar M, L’Helguen S, Raikar V, Maguer J-F, Le Corre P (2004) Nitrogen uptake by size-fractionated plankton in permanently well-mixed temperate coastal waters. J Plankton Res 26:1207–1218

    Article  CAS  Google Scholar 

  • Wilkerson FP, Dugdale RC, Hogue VE, Marchi A (2006) Phytoplankton blooms and nitrogen productivity in San Francisco Bay. Est Coasts 29:401–406

    CAS  Google Scholar 

  • Yoshiyama K, Sharp JH (2006) Phytoplankton response to nutrient enrichment in an urbanized estuary: apparent inhibition of primary production by overeutrophication. Limnol Oceanogr 51:424–434

    Article  CAS  Google Scholar 

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Acknowledgments

The authors would like to thank C. Luís and T.P. Anselmo for technical assistance. This work was financially supported by the Portuguese Foundation for Science and Technology (FCT) through project DYNCYANO (PTDC/AMB/64747/2006). FCT provided funding for R.B.D. through a Ph.D. Grant (SFRH/BD/27536/2006).

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Authors and Affiliations

  1. Centre for Marine and Environmental Research (CIMA), University of Algarve, Campus de Gambelas, 8005-139, Faro, Portugal

    Rita B. Domingues, Ana B. Barbosa & Helena M. Galvão

  2. Leibniz Institute of Marine Sciences (IFM-GEOMAR), Düsternbrooker Weg 20, 24105, Kiel, Germany

    Ulrich Sommer

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  1. Rita B. Domingues
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  2. Ana B. Barbosa
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  3. Ulrich Sommer
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  4. Helena M. Galvão
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Correspondence to Rita B. Domingues.

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Domingues, R.B., Barbosa, A.B., Sommer, U. et al. Ammonium, nitrate and phytoplankton interactions in a freshwater tidal estuarine zone: potential effects of cultural eutrophication. Aquat Sci 73, 331–343 (2011). https://doi.org/10.1007/s00027-011-0180-0

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  • DOI: https://doi.org/10.1007/s00027-011-0180-0

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