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Estuaries and Coasts

, Volume 38, Issue 5, pp 1678–1691 | Cite as

Changes in the Phytoplankton Composition in a Temperate Estuarine System (1960 to 2010)

  • Ana C. Brito
  • Teresa Moita
  • Carla Gameiro
  • Teresa Silva
  • Tânia Anselmo
  • Vanda Brotas
Article

Abstract

The main aim of this study was to evaluate the temporal changes in the phytoplankton community of the Tagus Estuary and to identify the stressors involved. Environmental and phytoplankton data were gathered from several studies conducted in the 1960s, 1980s and from 1999 to 2010 (2000s). Phytoplankton data included information on the community composition through microscopy. No significant change was found between temperature and nitrogen values in the three periods. Chlorophyll a concentrations varied throughout the years, and the lowest concentrations were observed after 2004. Significant differences were also found between phytoplankton cell abundances, lower in the 1980s compared to the ones recorded in the 2000s. In the 1980s, diatoms were the most abundant group in the majority of samples and were found to be associated with nitrogen concentrations (canonical correspondence analysis), which was not observed in the 2000s. In the period 2006–2007, the importance of diatoms decreased and smaller cells became more abundant (e.g. cryptophytes, euglenophytes, prasinophytes). The ratio cryptophyta/bacillariophyta seems to yield an increase from <1 in 1980s to >1 in 2006–2007. Mesodinium rubrum and Dinophysis produce recurrent toxic blooms in the adjacent coastal area. We can speculate that the estuary can be a cryptophyte producer to sustain the cryptophytes-M. rubrum-Dinophysis trophic relationship. A top-down hypothesis (shellfish grazing) is considered to explain the change in the phytoplankton community. A quantitative tool, the Phytoplankton Community Index (PCI), yielded a significant deviation of the community, from the 1980s to the 2000s, suggesting a shift toward the dominance of small cells.

Keywords

Phytoplankton community Chlorophyll a Life forms Phytoplankton Community Index (PCI) Invasive bivalve Tagus estuary Portugal 

Notes

Acknowledgments

Ana Brito was funded by a Portuguese Pos-doc Grant from FCT (BPD/63017/2009) and by the Investigador FCT Program (IF/00331/2013). The authors wish to thank ValorSul SA for the financial support. This study was also supported by the Fundação para a Ciência e a Tecnologia (PEst-OE/MAR/UI0199/2014).

References

  1. Bidle, K.D., and P.G. Falkowski. 2004. Cell death in planktonic, photosynthetic microorganisms. Nature Reviews Microbiology 2: 643–655.CrossRefGoogle Scholar
  2. Braunschweig, F., Martins, F., Chambel, P., Neves, R. (2003). A methodology to estimate renewal time scales in estuaries: the Tagus Estuary case. Ocean Dynamics, 53, 137–145.Google Scholar
  3. Brito, A., A. Newton, P. Tett, J. Icely, and T. Fernandes. 2010. The yield of microphytobenthic chlorophyll from nutrients: enriched experiments in microcosms. Journal of Experimental Marine Biology and Ecology 384: 30–43.CrossRefGoogle Scholar
  4. Brito, A., T. Quental, M.A.C. Branco, M. Falcão, A. Newton, J. Icely, and T. Moita. 2012a. Phytoplankton dynamics in Southern Portuguese coastal lagoons during a discontinuous period of 40 years: an overview. Estuarine, Coastal and Shelf Science 110: 147–156.CrossRefGoogle Scholar
  5. Brito, A., V. Brotas, M. Caetano, T.P. Coutinho, A. Bordalo, J. Icely, J.M. Neto, J. Serôdio, and T. Moita. 2012b. Defining phytoplankton class boundaries in Portuguese transitional waters: an evaluation of the ecological quality status according to the Water Framework Directive. Ecological Indicators 19: 5–14.CrossRefGoogle Scholar
  6. Cabeçadas, L. 1999. Phytoplankton production in the Tagus Estuary (Portugal). Oceanologica Acta 22: 205–214.CrossRefGoogle Scholar
  7. Cabeçadas, G., M.E. Cunha, T. Moita, J. Pissarra, and M.A. Sampayo. 1983. Red tide in Cascais bay, Portugal. Boletim do Instituto Nacional de Investigação das Pescas 10: 81–123.Google Scholar
  8. Cabrita, T., and T. Moita. 1995. Spatial and Temporal variation of physico-chemical conditions and phytoplankton during a dry year in the Tagus estuary (Portugal). Netherlands Journal of Aquatic Ecology 29: 323–332.CrossRefGoogle Scholar
  9. Calbet, A., and M. Landry. 2004. Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnology and Oceanography 49: 51–57.CrossRefGoogle Scholar
  10. Cebrian, J., and I. Valiela. 1999. Seasonal patterns in phytoplankton biomass in coastal ecosystem. Journal of Plankton Research 21: 429–444.CrossRefGoogle Scholar
  11. Chainho, P. 2008. Long-term trends in intertidal and subtidal benthic communities in response to water quality improvement measures. PhD Thesis. University of Lisbon, 192 pp. Available in: http://repositorio.ul.pt/bitstream/10451/1691/1/3712_Tese_Chainho.pdf.
  12. Cloern, J. 1987. Turbidity as a controlo n phytoplankton biomass and productivity in estuaries. Continental Shelf Research 7: 1367–1381.CrossRefGoogle Scholar
  13. Cloern, J. 1999. The relative importance of light and nutriente limitation of phytoplankton growth: a simple index of coastal ecosystem sensitibity to nutriente enrichment. Aquatic Ecology 33: 3–16.CrossRefGoogle Scholar
  14. Cloern, J. 2001. Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series 210: 223–253.CrossRefGoogle Scholar
  15. Colijn, F. 1984. Characteristics of primary production in the Dutch Wadden Sea. Netherlands Institute for Sea Research Publication Series 10: 41–50.Google Scholar
  16. Costanza, R., and M. Mageau. 1999. What is a healthy ecosystem? Aquatic Ecology 33: 105–115.CrossRefGoogle Scholar
  17. Diehl, S., S. Berger, R. Ptacnik, and A. Wild. 2002. Phytoplankton, light, and nutrientes in a gradient of mixing depths: field experiments. Ecology 83: 399–411.CrossRefGoogle Scholar
  18. Estrada, M. 1984. Phytoplankton distribution and composition off the coast of Galicia (northwest of Spain). Journal of Plankton Research 6: 417–434.CrossRefGoogle Scholar
  19. Falkowski, P.G., and J.A. Raven. 2007. Aquatic photosynthesis. Princeton University Press, 484 pp.Google Scholar
  20. Gameiro, C., and V. Brotas. 2010. Patterns of phytoplankton variability in the Tagus Estuary (Portugal). Estuaries and Coasts 33: 311–323.CrossRefGoogle Scholar
  21. Gameiro, C., P. Cartaxana, M.T. Cabrita, and V. Brotas. 2004. Variability in chlorophyll and phytoplankton composition in an estuarine system. Hydrobiologia 525: 113–124.CrossRefGoogle Scholar
  22. Gameiro, C., P. Cartaxana, and V. Brotas. 2007. Environmental drivers of phytoplankton distribution and composition in Tagus Estuary, Portugal. Estuarine, Coastal and Shelf Science 75: 21–34.CrossRefGoogle Scholar
  23. Gameiro, C., J. Zwolinski, and V. Brotas. 2011. Light control on phytoplankton production in a shallow and turbid estuarine system. Hydrobiologia 669: 249–263.CrossRefGoogle Scholar
  24. Garaulet, L. 2011. Estabelecimento do bivalve exótico Ruditapes philippinarum (Adams & reeve, 1850) no estuário do Tejo: caracterização da população actual e análise comparative com a congénere native Ruditapes decussatus (Linnaeus, 1758) e macrofauna bentónica acompanhante. MSc Thesis, Universidade de Lisboa, 100 pp. Available in: http://repositorio.ul.pt/bitstream/10451/5602/1/ulfc092734_tm_lucia_garaulet.pdf
  25. Gaspar, M. 2010. Distribuição, abundância e estrutura demográfica da amêijoa-japonesa (Ruditapes philippinarum) no rio Tejo. Relatório IPIMAR, 6 pp.Google Scholar
  26. Gustafson, D., D. Stoecker, M. Johnson, W. van Heukelem, and K. Sneider. 2000. Cryptophyte algae are robber of their organelles by the marine ciliate Mesodinium rubrum. Nature 405: 1049–52.CrossRefGoogle Scholar
  27. Harding, L.W. 1994. Long-term trends in the distribution of phytoplankton in Chesapeake Bay: roles of light, nutrients and stramflow. Marine Ecology Progress Series 104: 267–291.CrossRefGoogle Scholar
  28. Hooper, D.U., F.S. Chapin, J.J. Ewel, A. Hector, P. Inchausti, S. Lavorel, J.H. Lawton, D.M. Lodge, M. Loreau, S. Naeem, B. Schmid, H. Setala, A.J. Symstad, J. Vandermeet, and D.A. Wardle. 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75: 3–35.CrossRefGoogle Scholar
  29. Irigoien, X., and J. Castel. 1997. Light limitation and distribution of chlorophyll pigments in a highly turbid estuary: the Gironde (SW France). Estuarine, Coastal and Shelf Science 44: 507–517.CrossRefGoogle Scholar
  30. Kasim, M., and H. Mukai. 2006. Contribution of benthic and epiphytic diatoms to clam and oyter production in the Akkeshi-ko Estuary. Journal of Oceanography 62: 267–281.CrossRefGoogle Scholar
  31. Kromkamp, J., and J. Peene. 1995. Possibility of net phytoplankton primary production in the turbid Schelde Estuary (SW Netherlands). Marine Ecology Progress Series 121: 249–259.CrossRefGoogle Scholar
  32. Lorenzen, G. 1967. Determination of chlorophyll and phaeopigments spectrophotometric equations. Limnology and Oceanography 12: 343–346.CrossRefGoogle Scholar
  33. MacIntyre, H., and J. Cullen. 1996. Primary production by suspended and benthic microalgae in a turbid estuary: time-scales of variability in San Antonio Bay, Texas. Marine Ecology Progress Series 145: 245–268.CrossRefGoogle Scholar
  34. Margalef, R. 1978. Life forms of phytoplankton as survival alternatives in an unstable environment. Oceanologica Acta 1: 493–509.Google Scholar
  35. Martins, M., J. Ferreira, T. Calvão, H. Figueiredo. 1984. Nutrientes no estuário do Tejo – comparação da situação em caudais médios e em cheia, com destaque para alterações na qualidade da água, Commun. I. Simpósio Luso-Brasileiro de engenharia sanitária e ambiental.Google Scholar
  36. Moita, T. 2001. Estrutura, variabilidade e dinâmica do fitoplâncton na costa de Portugal continental. PhD Thesis. University of Lisbon, 272 pp. Available in: https://www.ipma.pt/pt/publicacoes/pescas/index.jsp?page=teses.xml.
  37. Monbet, Y. 1992. Control of phytoplankton biomass in estuaries: a comparative analysis of microtidal and macrotidal estuaries. Estuaries 15: 563–571.CrossRefGoogle Scholar
  38. Murray, A., C. Gibbs, and A. Longmore. 1986. Determination of chlorophyll in marine waters: intercomparison of a rapid HPLC method with full HPLC, spectrophotometric and fluorometric method. Marine Chemistry 19: 211–227.CrossRefGoogle Scholar
  39. Nakamura, Y. 2004. Suspension feeding and growth of juvenile Manila clam Ruditapes philippinarum reared in the laboratory. Fisheries Science 70: 215–222.CrossRefGoogle Scholar
  40. Park, M.G., H.S. Kim, G. Myung, Y.G. Kang, and W. Yih. 2006. First successful culture of the marine dinoflagellate Dinophysis acuminata. Aquatic Microbial Ecology 45: 101–106.CrossRefGoogle Scholar
  41. Pereira, P., M.J. Botelho, T. Cabrita, C. Vale, T. Moita, and C. Gonçalves. 2011. Winter-nutrient composition linkage to algae-produced toxins in shellfish at a eutrophic coastal lagoon (Óbidos lagoon, Portugal). Estuarine, Coastal and Shelf Science 112: 61–72.CrossRefGoogle Scholar
  42. Peterson, T.D., R.L. Golda, M.L. Garcia, B. Li, M. Maier, J. Needoba, and P. Zuber. 2013. Associations between Mesodinium rubrum and cryptophyte algae in the Columbia River estuary. Aquatic Microbial Ecology 68: 117–130.CrossRefGoogle Scholar
  43. Ribeiro, S., and A. Amorim. 2008. Environmental drivers of temporal succession in recente dinoflagellate cyst assemblages from a coastal site in the North-East Atlantic (Lisbon Bay, Portugal). Marine Micropaleontology 68: 156–178.CrossRefGoogle Scholar
  44. Roy, S., C. Llewellyn, E. Skarstad, G. Johnsen. 2012. Phytoplankton pigments: characterization, chemotaxonomy and applications in oceanography. Cambridge University Press, 845 pp.Google Scholar
  45. Santos, A., M. Calijuri, E. Morais, M. Adorno, P. Falco, D. Carvalho, G. Deberdt, and S. Benassi. 2003. Comparison of three methods for chlorophyll determination: spectrophotometry and fluorimetry in samples containing pigment mixtures and spectrophotometry in samples with separate pigments through high performance liquid chromatography. Acta Limnolofica Brasiliensia 15: 12.Google Scholar
  46. Schaeffer, D., E. Herricks, and H. Kerster. 1988. Ecosystem health: I. Measuring ecosystem health. Environmental Management 12: 445–455.CrossRefGoogle Scholar
  47. Silva, E., M.E. Assis, and M.A. Sampayo. 1969. Primary productivity in the Tagus and Sado estuaries from May 1967 to May 1968. Notas e Estudos do Instituto de Biologia Marítima, N. 37.Google Scholar
  48. Silva, A., C.R. Mendes, S. Palma, and V. Brotas. 2008. Short-time scale variation of phytoplankton succession in Lisbon bay (Portugal) as revealed by microscopy cell counts and HPLC pigment analysis. Estuarine, Coastal and Shelf Science 79: 230–238.CrossRefGoogle Scholar
  49. Tett, P. 2006. Using the PCI-LF: a draft user guide. Napier University, Edinburgh. Available in: http://www.lifesciences.napier.ac.uk/research/Envbiofiles/PCI.htm.
  50. Tett, P., R. Gowen, T. Fernandes, L. Gilpin, M. Huxham, K. Kennington, P. Read, M. Service, M. Wilkinson, and S. Malcolm. 2007. Defining and detecting undesirable disturbance in the context of marine eutrophication. Marine Pollution Bulletin 55: 282–297.CrossRefGoogle Scholar
  51. Tett, P., C. Carreira, D.K. Mills, S. van Leeuwen, J. Foden, E. Bresnan, and R. Gowen. 2008. Use of a Phytoplankton Community Index to assess the health of coastal waters. ICES Journal of Marine Science 65: 1475–1482.CrossRefGoogle Scholar
  52. Underwood, G.J.C., and J. Kromkamp. 1999. Primary production by phytoplankton and microphytobenthos in estuaries. Advances in Ecological Research 29: 93–153.CrossRefGoogle Scholar
  53. Utermöhl, H. 1958. Zur Vervolkommung der quantitativen Phytoplankton: methodik. Mitteilungen Internationale Vereinigung für Theoretische und Angewandte. Limnologie 9: 1e38.Google Scholar
  54. Vale, C., and B. Sundby. 1987. Suspended sediment fluctuations in the Tagus estuary on semi-diurnal and fortnightly time scales. Estuarine, Coastal and Shelf Science 25: 495–508.CrossRefGoogle Scholar
  55. Valiela, I. 1984. Marine ecological processes. New York: Springer. 546 pp.CrossRefGoogle Scholar
  56. Zhou, M.-J., Z.-L. Shen, and Yu. R-C. 2008. Responses of a coastal phytoplankton community to increased nutrient input from the Changjiang (Yangtze) River. Continental Shelf Research 28: 1483–1489.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2014

Authors and Affiliations

  • Ana C. Brito
    • 1
    • 3
  • Teresa Moita
    • 2
  • Carla Gameiro
    • 1
    • 3
  • Teresa Silva
    • 1
    • 3
  • Tânia Anselmo
    • 1
    • 3
  • Vanda Brotas
    • 1
    • 3
  1. 1.CO-FCUL, Centro de OceanografiaFaculdade de Ciências da Universidade de LisboaLisbonPortugal
  2. 2.IPMA, Instituto Português do Mar e da AtmosferaLisbonPortugal
  3. 3.MARE-Marine and Environmental Sciences CentreFaculdade de Ciências da Universidade de LisboaLisbonPortugal

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