Aquatic Ecology

, Volume 49, Issue 2, pp 127–146 | Cite as

Are nutrients and light limiting summer phytoplankton in a temperate coastal lagoon?

  • Rita B. Domingues
  • Cátia C. Guerra
  • Ana B. Barbosa
  • Helena M. Galvão


The Ria Formosa coastal lagoon is one of the most important and vulnerable ecosystems in Portugal, and it is subjected to strong anthropogenic pressures and natural nutrient inputs associated with coastal upwelling. The aim of this study was to evaluate the occurrence of nutrient and light limitation of phytoplankton growth during the productive period, and assess potential impacts of limitation on ecosystem eutrophication. Inorganic nutrients were added to natural microcosms filled with water collected at the landward and seaward boundaries, in summer 2012. Experimental treatments were incubated in situ under two different light intensities during 24 h. Phytoplankton composition, abundance and biomass, net growth rates and nutrient consumption were evaluated. At the landward location, potential nutrient limitation by nitrogen was observed. Nitrogen addition led to a significant increase in N consumption, resulting in higher phytoplankton growth, mainly diatoms, in all N-enriched treatments, under both light intensities. Significant consumption of silica and phosphorus was not reflected on growth, and it was probably due to luxury consumption. At the seaward station, phytoplankton, mainly cyanobacteria and eukaryotic picophytoplankton, were primarily limited by light, due to a deeper mixed layer. Nutrients were not limiting the phytoplankton growth due to import of nutrients from upwelled waters to the adjacent coastal zone.


Eutrophication Limitation Phytoplankton Nutrients Light Coastal lagoons 



This work was financially supported by the Portuguese Foundation for Science and Technology (FCT) through project PHYTORIA (PTDC/MAR/114380/2009). FCT provided funding for R.B.D. through a postdoctoral fellowship (SFRH/BPD/68688/2010). We thank Kathleen Silvano for processing remote sensing data acquired within FCT’s project PHYTOCLIMA (PTDC/AAC-CLI/114512/2009).


  1. Admiraal W (1977) Tolerance of estuarine benthic diatoms to high concentrations of ammonia, nitrite ion, nitrate ion and orthophosphate. Mar Biol 43:307–315CrossRefGoogle Scholar
  2. Agawin NSR, Agustí S (1997) Abundance, frequency of dividing cells and growth rates of Synechococcus sp. (cyanobacteria) in the stratified Northwest Mediterranean Sea. J Plankton Res 19:1599–1615CrossRefGoogle Scholar
  3. Agawin NSR, Duarte CM, Agustí S, McManus L (2003) Abundance, biomass and growth rates of Synechococcus sp. in a tropical coastal ecosystem (Philippines, South China Sea). Est Coast Shelf Sci 56:493–502CrossRefGoogle Scholar
  4. Alvarez I, Gomez-Gesteira M, Castro M et al (2011) Comparative analysis of upwelling influence between the western and northern coast of the Iberian Peninsula. Cont Shelf Res 31:388–399CrossRefGoogle Scholar
  5. Andrade C (1990) O ambiente de barreira da Ria Formosa (Algarve, Portugal). Ph.D. Thesis, Universidade de Lisboa, PortugalGoogle Scholar
  6. Bakun A (1973) Coastal upwelling indices, west coast of North America, 1946–1971. US Dept. Commerce NOAA Technical Report NMFS-SSRF, New York 671Google Scholar
  7. Barbosa AB (2006) Estrutura e dinâmica da teia alimentar microbiana na Ria Formosa. 542 pGoogle Scholar
  8. Barbosa AB (2010) Seasonal and interanual variability of planktonic microbes in a mesotidal coastal lagoon (Ria Formosa, SE Portugal): impact of climatic changes and local human influences. In: Kennish MJ, Paerl HW (eds) Coast Lagoons Crit Habitats Environ Chang, CRC Press, pp 334–366Google Scholar
  9. Bec B, Husseini Ratrema J, Collos Y et al (2005) Phytoplankton seasonal dynamics in a Mediterranean coastal lagoon: emphasis on the picoeukaryote community. J Plankton Res 27:881–894. doi: 10.1093/plankt/fbi061 CrossRefGoogle Scholar
  10. Bec B, Collos Y, Souchu P et al (2011) Distribution of picophytoplankton and nanophytoplankton along an anthropogenic eutrophication gradient in French Mediterranean coastal lagoons. Aquat Microb Ecol 63:29–45. doi: 10.3354/ame01480 CrossRefGoogle Scholar
  11. Bouman HA, Ulloa O, Barlow R et al (2011) Water column stratification governs the community structure of subtropical marine picophytoplankton. Environ Microbiol Rep 3:473–482. doi: 10.1111/j.1758-2229.2011.00241.x CrossRefPubMedGoogle Scholar
  12. Brito AC, Quental T, Coutinho TP et al (2012) Phytoplankton dynamics in southern Portuguese coastal lagoons during a discontinuous period of 40 years: an overview. Estuar Coast Shelf Sci 110:147–156. doi: 10.1016/j.ecss.2012.04.014 CrossRefGoogle Scholar
  13. Bronk DA, See JH, Bradley P, Killberg L (2007) DON as a source of bioavailable nitrogen for phytoplankton. Biogeosciences 4:283–296Google Scholar
  14. Cabaço S, Machás R, Vieira V, Santos R (2008) Impacts of urban wastewater discharge on seagrass meadows (Zostera noltii). Estuar Coast Shelf Sci 78:1–13. doi: 10.1016/j.ecss.2007.11.005 CrossRefGoogle Scholar
  15. Carletti A, Heiskanen A-S (2009) Water framework directive intercalibration technical report-part 3: coastal and transitional waters. Office for Official Publications of the European Community.
  16. Carpenter EJ, Guillard RRL (1971) Interspecific differences in nitrate half-saturation constants for three species of marine phytoplankton. Ecology 52:183–185Google Scholar
  17. Cebrián J, Valiela I (1999) Seasonal patterns in phytoplankton biomass in coastal ecosystems. J Plankton Res 21:429–444Google Scholar
  18. Cloern JE (1999) The relative importance of light and nutrient limitation of phytoplankton growth: a simple index of coastal ecosystem sensitivity to nutrient enrichment. Aquat Ecol 3–16Google Scholar
  19. Cloern JE (2001) Our evolving conceptual model of the coastal eutrophication problem. Mar Ecol Prog Ser 210:223–253CrossRefGoogle Scholar
  20. Cochlan WP, Herndon J, Kudela RM (2008) Inorganic and organic nitrogen uptake by the toxigenic diatom Pseudo-nitzschia australis (Bacillariophyceae). Harmful Algae 8:111–118Google Scholar
  21. Collos Y, Vaquer A, Bibent B et al (2003) Response of coastal phytoplankton to ammonium and nitrate pulses: seasonal variations of nitrogen uptake and regeneration. Aquat Ecol 37:227–236CrossRefGoogle Scholar
  22. Collos Y, Vaquer A, Souchu P (2005) Acclimation of nitrate uptake by phytoplankton to high substrate levels. J Phycol 41:466–478. doi: 10.1111/j.1529-8817.2005.00067.x CrossRefGoogle Scholar
  23. Cravo A, Cardeira S, Pereira C et al (2014) Exchanges of nutrients and chlorophyll a through two inlets of Ria Formosa, South of Portugal, during coastal upwelling events. J Sea Res. doi: 10.1016/j.seares.2014.04.004 Google Scholar
  24. Domingues RB, Barbosa A, Galvão H (2005) Nutrients, light and phytoplankton succession in a temperate estuary (the Guadiana, south-western Iberia). Estuar Coast Shelf Sci 64:249–260. doi: 10.1016/j.ecss.2005.02.017 CrossRefGoogle Scholar
  25. Domingues RB, Barbosa A, Galvão H (2008) Constraints on the use of phytoplankton as a biological quality element within the Water Framework Directive in Portuguese waters. Mar Pollut Bull 56:1389–1395. doi: 10.1016/j.marpolbul.2008.05.006 CrossRefPubMedGoogle Scholar
  26. Domingues RB, Anselmo TP, Barbosa AB et al (2011a) Nutrient limitation of phytoplankton growth in the freshwater tidal zone of a turbid, Mediterranean estuary. Estuar Coast Shelf Sci 91:282–297. doi: 10.1016/j.ecss.2010.12.008 CrossRefGoogle Scholar
  27. Domingues RB, Anselmo TP, Barbosa AB et al (2011b) Light as a driver of phytoplankton growth and production in the freshwater tidal zone of a turbid estuary. Estuar Coast Shelf Sci 91:526–535. doi: 10.1016/j.ecss.2010.12.008 CrossRefGoogle Scholar
  28. Domingues RB, Barbosa AB, Sommer U, Galvão HM (2011c) Ammonium, nitrate and phytoplankton interactions in a freshwater tidal estuarine zone: potential effects of cultural eutrophication. Aquat Sci 73:331–343. doi: 10.1007/s00027-011-0180-0 CrossRefGoogle Scholar
  29. Domingues RB, Barbosa AB, Sommer U, Galvão HM (2012) Phytoplankton composition, growth and production in the Guadiana estuary (SW Iberia): unraveling changes induced after dam construction. Sci Total Environ 416:300–313Google Scholar
  30. Dortch Q, Whitledge TE (1992) Does nitrogen or silicon limit phytoplankton production in the Mississippi River plume and nearby regions? Cont Shelf Res 12:1293–1309Google Scholar
  31. Edwards V, Icely J, Newton A, Webster R (2005) The yield of chlorophyll from nitrogen: a comparison between the shallow Ria Formosa lagoon and the deep oceanic conditions at Sagres along the southern coast of Portugal. Estuar Coast Shelf Sci 62:391–403. doi: 10.1016/j.ecss.2004.09.004 CrossRefGoogle Scholar
  32. Fisher TR, Carlson PR, Barber RT (1982) Carbon and nitrogen primary productivity in three North Carolina estuaries. Estuar Coast Shelf Sci 15:621–644Google Scholar
  33. Fisher TR, Harding LW, Stanley DW, Ward LG (1988) Phytoplankton, nutrients, and turbidity in the Chesapeake, Delaware, and Hudson estuaries. Estuar Coast Shelf Sci 27:61–93Google Scholar
  34. Fisher TR, Hagy JD, Boynton WR, Williams MR (2006) Cultural eutrophication in the Choptank and Patuxent estuaries of Chesapeake Bay. Limnol Oceanogr 51:435–447Google Scholar
  35. Gobler CJ, Buck NJ, Sieracki ME, Sañudo-Wilhelmy SA (2006) Nitrogen and silicon limitation of phytoplankton communities across an urban estuary: the East River-Long Island Sound system. Estuar Coast Shelf Sci 68:127–138. doi: 10.1016/j.ecss.2006.02.001 CrossRefGoogle Scholar
  36. Grasshoff K, Ehrhardt M, Kremling K (1983) Methods of Seawater Analysis. Verlag Chemie. Weinheim, GermanyGoogle Scholar
  37. Guerra R, Pistocchi R, Vanucci S (2013) Dynamics and sources of organic carbon in suspended particulate matter and sediments in Pialassa Baiona lagoon (NW Adriatic Sea, Italy). Estuar Coast Shelf Sci 135:24–32Google Scholar
  38. Haas LW (1982) Improved epifluorescence microscopy for observing planktonic microorganisms. Ann Inst Oceanogr 58:261–266Google Scholar
  39. Harpole WS, Ngai JT, Cleland EE et al (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–862. doi: 10.1111/j.1461-0248.2011.01651.x CrossRefPubMedGoogle Scholar
  40. Hauss H, Franz JMS, Sommer U (2012) Changes in N: P stoichiometry influence taxonomic composition and nutritional quality of phytoplankton in the Peruvian upwelling. J Sea Res 73:74–85. doi: 10.1016/j.seares.2012.06.010 CrossRefGoogle Scholar
  41. Hillebrand H, Sommer U (1996) Nitrogenous nutrition of the potentially toxic diatom Pseudonitzschia pungens f. multiseries Hasle. J Plankton Res 18:295–391Google Scholar
  42. Huisman J, Jonker RR, Zonneveld C, Weissing FJ (1999) Competition for light between phytoplankton species: experimental tests of mechanistic theory. Ecology 80:211. doi: 10.2307/176991 CrossRefGoogle Scholar
  43. Irigoien X, Castel J (1997) Light limitation and distribution of chlorophyll pigments in a highly turbid estuary: the Gironde (SW France). Estuar Coast Shelf Sci 44:507–517Google Scholar
  44. IPCC - Intergovernmental Panel on Climate Change (2001) Climate change 2001: the scientific basis. Cambridge University Press, CambridgeGoogle Scholar
  45. Justic D, Rabalais NN, Turner RE, Dortch Q (1995) Changes in nutrient structure of river dominated coastal waters: stoichiometric nutrient balance and its consequences. Estuar Coast Shelf Sci 40:339–356Google Scholar
  46. Kocum E, Underwood G, Nedwell D (2002) Simultaneous measurement of phytoplanktonic primary production, nutrient and light availability along a turbid, eutrophic UK east coast estuary (the Colne Estuary). Mar Ecol Prog Ser 231:1–12. doi: 10.3354/meps231001 CrossRefGoogle Scholar
  47. Kromkamp J, Peene J, Rijswijk P et al (1995) Nutrients, light and primary production by phytoplankton and microphytobenthos in the eutrophic, turbid Westerschelde estuary (The Netherlands). Hydrobiologia 311:9–19. doi: 10.1007/BF00008567 CrossRefGoogle Scholar
  48. Larson CA, Belovsky GE (2013) Salinity and nutrients influence richness and eveness of phytoplankton communities in microscosm experiments from Great Salt Lake, Utah, USA. J Plankton Res 35:1154–1166Google Scholar
  49. Lesutiene J, Bukaveckas PA, Gasiunaite ZR et al (2014) Tracing the isotopic signal of a cyanobacteria bloom through the food web of a Baltic Sea coastal lagoon. Estuar Coast Shelf Sci 138:47–56Google Scholar
  50. Litchman E (1998) Population and community responses of phytoplankton to fluctuating light. Oecologia 117:247–257CrossRefGoogle Scholar
  51. Loureiro S, Newton A, Icely J (2005) Effects of nutrient enrichments on primary production in the Ria Formosa coastal lagoon (Southern Portugal). Hydrobiologia 550:29–45. doi: 10.1007/s10750-005-4357-1 CrossRefGoogle Scholar
  52. Loureiro S, Newton A, Icely JD (2006) Boundary conditions for the European Water Framework Directive in the Ria Formosa lagoon, Portugal (physico-chemical and phytoplankton quality elements). Estuar Coast Shelf Sci 67:382–398. doi: 10.1016/j.ecss.2005.11.029 CrossRefGoogle Scholar
  53. Loureiro S, Jauzein C, Garcés E et al (2009) The significance of organic nutrients in the nutrition of Pseudonitzschia delicatissima (Bacillariophyceae). J Plankton Res 31:399–410Google Scholar
  54. Ly J, Philippart CJM, Kromkamp JC (2014) Phosphorus limitation during a phytoplankton spring bloom in the western Dutch Wadden Sea. J Sea Res 88:109–120. doi: 10.1016/j.seares.2013.12.010 CrossRefGoogle Scholar
  55. Martin-Jézéquel V, Hildebrand M, Brzezinski MA (2000) Silicon metabolism in diatoms: implications for growth. J Phycol 36:821–840Google Scholar
  56. Newton A, Mudge SM (2005) Lagoon-sea exchanges, nutrient dynamics and water quality management of the Ria Formosa (Portugal). Estuar Coast Shelf Sci 62:405–414. doi: 10.1016/j.ecss.2004.09.005 CrossRefGoogle Scholar
  57. Newton A, Icely JD, Falcao M et al (2003) Evaluation of eutrophication in the Ria Formosa coastal lagoon, Portugal. Cont Shelf Res 23:1945–1961. doi: 10.1016/j.csr.2003.06.008 CrossRefGoogle Scholar
  58. Newton A, Icely J, Cristina S et al (2014) An overview of ecological status, vulnerability and future perspectives of European large shallow, semi-enclosed coastal systems, lagoons and transitional waters. Estuar Coast Shelf Sci 140:95–122. doi: 10.1016/j.ecss.2013.05.023 CrossRefGoogle Scholar
  59. Nobre AM, Ferreira JG, Newton A et al (2005) Management of coastal eutrophication: integration of field data, ecosystem-scale simulations and screening models. J Mar Syst 56:375–390Google Scholar
  60. Nogueira P, Domingues RB, Barbosa AB (2014) Are microcosm volume and sample pre-filtration relevant to evaluate phytoplankton growth? J Exp Mar Biol Ecol 461:323–330. doi: 10.1016/j.jembe.2014.09.006 CrossRefGoogle Scholar
  61. Odermatt D, Gitelson A, Brando VE et al (2012) Review of constituent retrieval in optically deep and complex waters from satellite imagery. Remote Sens Environ 118:116–126Google Scholar
  62. Olsen Y, Agustí S, Andersen T et al (2006) A comparative study of responses in planktonic food web structure and function in contrasting European coastal waters exposed to experimental nutrient addition. Limnol Oceanogr 51:488–503CrossRefGoogle Scholar
  63. O’Reilly JE, Maritorena S, Siegel DA et al (2000) Ocean color chlorophyll a algorithms for SeaWiFS, OC2, and OC4: Version 4. In: O’Reilly JE, Maritorena S, O’Brien MC et al (eds) SeaWiFS Postlaunch Calibration and Validation Analyses, Part 3. NASA Tech Memo 2000-206892, vol 11, NASA Goddard Space Flight Center: 8–22Google Scholar
  64. Örnólfsdóttir EB, Lumsden SE, Pinckney JL (2004) Nutrient pulsing as a regulator of phytoplankton abundance and community composition in Galveston Bay, Texas. J Exp Mar Biol Ecol 303:197–220. doi: 10.1016/j.jembe.2003.11.016 CrossRefGoogle Scholar
  65. Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, OxfordGoogle Scholar
  66. Pereira MG, Icely J, Mudge S et al (2007) Temporal and spatial variation of phytoplankton pigments in the Western Part of Ria Formosa Lagoon, Southern Portugal. Environ Forensic 8:205–220. doi: 10.1080/15275920701506151 CrossRefGoogle Scholar
  67. Phlips EJ, Badylak S, Lynch TC (1999) Blooms of the picoplanktonic cyanobacterium Synechococcus in Florida Bay, a subtropical inner-shelf lagoon. Limnol Oceanogr 44:1166–1175Google Scholar
  68. Piedras FR, Odebrecht C (2012) The response of surf-zone phytoplankton to nutrient enrichment (Cassino Beach, Brazil). J Exp Mar Biol Ecol 432–433:156–161. doi: 10.1016/j.jembe.2012.07.020 CrossRefGoogle Scholar
  69. Probyn TA (1985) Nitrogen uptake by size-fractionated phytoplankton populations in the southern Benguela upwelling system. Mar Ecol Prog Ser 22:249–258Google Scholar
  70. Redfield AC, Ketchum BH, Richards FA (1963) The influence of organisms in the composition of seawater. In: Hill MN (ed) The Sea, vol II. Wiley, New York, pp 26–77Google Scholar
  71. Relvas P, Barton ED, Dubert J et al (2007) Physical oceanography of the western Iberia ecosystem: latest views and challenges. Prog Oceanogr 74:149–173Google Scholar
  72. Robinson IS (2004) Measuring the ocean from space: the principles and methods of satellite oceanography. Springer/Praxis, HeidelbergGoogle Scholar
  73. Sarthou G, Timmermans KR, Blain S, Tréguer P (2005) Growth physiology and fate of diatoms in the ocean: a review. J Sea Res 53:25–42. doi: 10.1016/j.seares.2004.01.007 CrossRefGoogle Scholar
  74. Sommer U (1989) The role of competition for resources in phytoplankton succession. In: Sommer U (ed) Plankton Ecology: Succession in plankton communities. Springer-Verlag, pp 57–106Google Scholar
  75. Sterner RW (2008) On the phosphorus limitation paradigm for lakes. Int Rev Hydrobiol 93:433–445. doi: 10.1002/iroh.200811068 CrossRefGoogle Scholar
  76. Tada K, Suksomjit M, Ichimi K et al (2009) Diatoms grow faster using ammonium in rapidly flushed eutrophic Dokai Bay, Japan. J Oceanogr 65:885–891CrossRefGoogle Scholar
  77. Taylor D, Nixon S, Granger S, Buckley B (1995) Nutrient limitation and the eutrophication of coastal lagoons. Mar Ecol Prog Ser 127:235–244. doi: 10.3354/meps127235 CrossRefGoogle Scholar
  78. Timmermans KR, van der Wagt B, Veldhuis MJW et al (2005) Physiological responses of three species of marine pico-phytoplankton to ammonium, phosphate, iron and light limitation. J Sea Res 53:109–120. doi: 10.1016/j.seares.2004.05.003 CrossRefGoogle Scholar
  79. Vaquer A, Troussellier M, Courties C, Bibent B (1996) Standing stock and dynamics of picophytoplankton in the Thau Lagoon (northwest Mediterranean coast). Limnol Oceanogr 41:1821–1828CrossRefGoogle Scholar
  80. Venrick EL (1978) How many cells to count? In: Sournia A (ed) Phytoplankton Manual. UNESCO, Paris, pp 167–180Google Scholar
  81. Xu H, Paerl HW, Qin B et al (2010) Nitrogen and phosphorus inputs control phytoplankton growth in eutrophic Lake Taihu, China. Limnol Oceanogr 55:420–432. doi: 10.4319/lo.2010.55.1.0420 CrossRefGoogle Scholar
  82. Zhang HM, Bates JJ, Reynolds RW (2006) Assessment of composite global sampling: Sea surface wind speed. Geophys Res Lett 33(17):L17714Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Rita B. Domingues
    • 1
    • 2
  • Cátia C. Guerra
    • 1
  • Ana B. Barbosa
    • 1
  • Helena M. Galvão
    • 1
  1. 1.CIMA – Centre for Marine and Environmental ResearchUniversidade do AlgarveFaroPortugal
  2. 2.MARE – Marine and Environmental Sciences CentreFaculdade de Ciências, Universidade de LisboaLisbonPortugal

Personalised recommendations