Skip to main content

Advertisement

Log in

Bacterial and phytoplankton dynamics in a sub-tropical estuary

  • Primary research paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Heterotrophic bacterial and phytoplankton biomass, production, specific growth rates and growth efficiencies were studied in July 2001 and January 2002 during both spring and neap tides, along a tidal cycle, at three sites in a subtropical estuary. Major freshwater inputs located in the Northern region led to differences in both phytoplankton and bacterioplankton biomass and activity along the estuary. While in the Northern region phytoplankton is light-limited, with mean phytoplankton production (PP) between 1.1 and 1.9 μg C l−1 h−1 and mean specific growth rates (PSG) between 0.14 and 0.16 d−1, the Southern region registered values as high as 24.7 μg C l−1 h−1 for PP and 2.45 d−1 (mean PP between 3.4 and 7.3 μg C l−1 h−1; mean PSG between 0.28 and 0.57 d−1). On the other hand, maximum bacterial production (BP: 63.8 μg C l−1 h−1) and specific growth rate (BSG: 32.26 d−1) were observed in the Northern region (mean BP between 3.4 and 12.8 μg C l−1 h−1; mean BSG between 1.98 and 6.67 day−1). These bacterial activity rates are among the highest recorded rates in estuarine and coastal waters, indicating that this system can be highly heterotrophic, due to high loads of allochthonous carbon (mainly derived from mangrove forest). Our results also showed that, despite that BP rates usually exceeded PP, in the Southern region BP may be partially supported (∼45%) by PP, since a significant regression was observed between BP and PP (r = 0.455, P < 0.001).

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

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abreu, P. C., B. B. Biddanda & C. Odebrecht, 1992. Bacterial dynamics of the Patos Lagoon. Estuary, Southern Brazil (32°8, 52°W): relationship with phytoplankton production and suspended material. Estuarine, Coastal and Shelf Science 35: 621–635.

    Article  Google Scholar 

  • Admiraal, W., J. Beukema & F. B. van Es, 1985. Seasonal fluctuations in the biomass and metabolic activity of bacterioplankton and phytoplankton in a well-mixed estuary: the Ems-Dollard (Wadden Sea). Journal of Plankton Research 7: 877–890.

    Article  Google Scholar 

  • Albright, L. J. & S. K. McRae, 1987. Annual bacterioplankton biomasses and productivities in a temperate west coast Canadian fjord. Applied and Environmental Microbiology 53: 1277–1285.

    PubMed  CAS  Google Scholar 

  • Almeida, M. A., M. A. Cunha & F. Alcântara, 2002. Seasonal change in the proportion of bacterial and phytoplankton production along a salinity gradient in a shallow estuary. Hydrobiologia 475/476: 251–262.

    Article  Google Scholar 

  • Aminot, A. & M. Chaussepied, 1983. Manuel des analyses chimiques en milieu marin. C.N.E.X.O., Brest.

    Google Scholar 

  • APHA (AMERICAN PUBLIC HEALTH ASSOCIATION, Inc.), 1985. Standard Methods for the Examination of Water and Wastewater, 16th edn. Washington, D.C.

  • Artigas, L. F., 1998. Seasonal variability in microplanktonic biomasses in the Gironde dilution plume (Bay of Biscay): relative importance of bacteria. Oceanologica Acta 21: 563–580.

    Article  CAS  Google Scholar 

  • Bano, N., M. Nisa, N. Khan, M. Saleem, P. J. Harrison, S. I. Ahmed & F. Azam, 1997. Significance of bacteria in the flux of organic matter in the tidal creeks of the mangrove ecosystem of the Indus River delta, Pakistan. Marine Ecology Progress Series 157: 1–12.

    Article  CAS  Google Scholar 

  • Barrera-Alba, J. J., S. M. F. Gianesella, F. M. P. Saldanha-Corrêa & G. A. O. Moser, 2004. On the determination of a conversion factor from labeled thymidine incorporation by bacteria to cell production in a Sub-tropical estuary: preliminary results. Brazilian Journal of Oceanography 52: 239–243.

    Article  Google Scholar 

  • Bell, R. T., 1993. Estimating production of heterotrophic bacterioplankton via incorporation of tritiated thymidine. In Kemp P. F., B. F. Sherr, E. B. Sherr & J. J. Cole (eds), Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Inc., Boca Raton, Florida: 495–503.

  • Bray, G. A., 1960. A simple efficient liquid scintillator for counting aqueous solution in a liquid scintillation counter. Analytical Biochemistry 1: 279–285.

    Article  CAS  Google Scholar 

  • Carmouze, J. P., 1994. O metabolismo dos ecossistemas aquáticos. Fundamentos teóricos métodos de estudo e análises químicas. FAPESP (eds), São Paulo, Brazil.

  • Cloern, J. E., C. Grenz & L. Vidergar-Lucas, 1995. An empirical model of phytoplankton chlorophyll:carbon ratio. The conversion factor between productivity and growth rate. Limnology and Oceanography 40: 1313–1321.

    Google Scholar 

  • Cole, J. J., S. Findlay & M. L. Pace, 1988. Bacterial production in fresh and saltwater ecosystems: a cross-system overview. Marine Ecology Progress Series 43: 1–10.

    Article  Google Scholar 

  • Crump, B. C. & J. A. Baross, 1996. Particle-attached bacteria and heterotrophic plankton associated with the Columbia River estuarine turbidity maxima. Marine Ecology Progress Series 138: 265–273.

    Article  Google Scholar 

  • Crump, B. C., J. A. Baross & C. A. Simenstad, 1998. Dominance of particle-attached bacteria in the Columbia River estuary, USA. Aquatic Microbial Ecology 14: 7–18.

    Article  Google Scholar 

  • Ducklow, H. W., 1982. Chesapeake Bay nutrient and plankton dynamics. 1. Bacterial biomass and production during spring tidal destratification in the York River, Virginia, estuary. Limnology and Oceanography 27: 651–659.

    CAS  Google Scholar 

  • Ducklow, H. W. & D. L. Kirchman, 1983. Bacterial dynamics and distribution during a spring diatom bloom in the Hudson River plume, USA. Journal of Plankton Research 5: 333–355.

    Article  Google Scholar 

  • Ducklow, H. W. & D. L. Carlson, 1992. Oceanic bacterial production. In Marshall K. C. (ed), Advances in Microbial Ecology, Vol. 12, Plenum Press, New York: 113–181.

    Google Scholar 

  • Ducklow, H. W., D. L. Kirchman & H. L. Qhinby, 1992. Determination of bacterioplankton growth rates during the North Atlantic spring phytoplankton bloom. Microbial Ecology 24: 125–144.

    Article  CAS  Google Scholar 

  • Engel, A. & U. Passow, 2001. The carbon and nitrogen content of transparent exopolymer particles (TEP) derived from diatom exudates. Marine Ecology Progress Series 219: 1–10.

    Article  CAS  Google Scholar 

  • Ferreyra, G. A., B. Mostajir, I. R. Schloss, K. Chatila, M. E. Ferrario, P. Sargian, S. Roy, J. Prod’homme & S. Demers, 2006. Ultraviolet-B radiation effects on the structure and function of lower trophic levels of the marine planktonic food web. Photochemistry and Photobiology 82: 887–897.

    Article  PubMed  CAS  Google Scholar 

  • Findlay, S., M. L. Pace, D. Lints, J. J. Cole, N. F. Caraco & B. Peierls, 1991. Weak coupling of bacterial and algal production in a heterotrophic ecosystem: The Hudson River estuary. Limnology and Oceanography 36: 268–278.

    Google Scholar 

  • Fuhrman, J. A., J. W. Ammerman & F. Azam, 1980. Bacterioplankton in the coastal euphotic zone: distribution, activity and possible relationships with phytoplankton. Marine Biology 60: 201–207.

    Article  Google Scholar 

  • Fuhrman, J. A. & F. Azam, 1980. Bacterioplankton secondary production estimates for coastal waters of British Columbia, Antarctica, and California. Applied and Environmental Microbiology 39: 1085–1095.

    PubMed  CAS  Google Scholar 

  • Furnas, M. J., 1990. In situ growth rates of marine phytoplankton: approaches to measurement, community and species growth rates. Journal of Plankton Research 12: 1117–1151.

    Article  Google Scholar 

  • Gasol, J. M., M. D. Doval, J. Pinhassi, J. Calderón-Paz, N. Guixa-Boixareu, D. Vaqué & C. Pedrós-Alió, 1998. Diel variations in bacterial heterotrophic activity and growth in the northwestern Mediterranean Sea. Marine Ecology Progress Series 164: 107–124.

    Article  Google Scholar 

  • Gianesella-Galvão, S. M. F., 1982. Standing-Stock and Potential of Phytoplankton Production in the Bay of Santos, Brazil. Boletim do Instituto Oceanográfico 31: 85–94.

    Google Scholar 

  • Gordon, D. C. Jr., 1969. Examination of methods of particulate organic carbon analysis. Deep-Sea Research 16: 661–665.

    CAS  Google Scholar 

  • Goosen, N. K., P. Van Rijswijk, J. Kromkamp & J. Peene, 1997. Regulation of annual variation in heterotrophic bacterial production in the Schelde estuary (SW Netherlands), Aquatic Microbial Ecology 12: 223–232.

    Article  Google Scholar 

  • Grasshoff, K., M. Ehrhardt, & K. Kremling, 1983. Methods of Seawater Analysis, 2nd edn. Verlag Chemie, Wienhien.

    Google Scholar 

  • Griffith, P., F. K. Shiah, K. Gloersen, H. W. Ducklow & M. Fletcher, 1994. Activity and distribution of attached bacteria in Chesapeake Bay. Marine Ecology Progress Series 108: 1–10.

    Article  Google Scholar 

  • Hoch, M. P. & D. L. Kirchman, 1993. Seasonal and Inter.-annual variability in bacterial production and biomass in a temperate estuary. Marine Ecology Progress Series 98: 283–295.

    Article  Google Scholar 

  • Iriberri, J., M. Unanue, I. Barcina & L. Egea, 1987. Seasonal variation in population density and heterotrophic activity of attached and free-living bacteria in coastal waters. Applied and Environmental Microbiology 53: 2308–2314.

    PubMed  CAS  Google Scholar 

  • Jeffrey, S. W. & G. F. Humphrey, 1975. New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algal and natural phytoplankton. Biochem. Physiol. Planzen (BPP) Bd. 167 S: 191–194.

    Google Scholar 

  • Jonas, R. B. & J. H. Tuttle, 1990. Bacterioplankton and organic carbon dynamics in the lower mesohaline Chesapeake Bay. Applied and Environmental Microbiology 56: 747–757.

    PubMed  CAS  Google Scholar 

  • Kormas, K. A., K. Kapiris, M. Thessalou-Legaki & A. Nicolaidou, 1998. Quantitative relationships between phytoplankton, bacteria and protists in Aegean semi-enclosed embayment (Maliakos Gulf, Greece). Aquatic Microbial Ecology 15: 255–264.

    Article  Google Scholar 

  • Kumari, L. K., P. M. A. Bhattathiri, S. G. P. Matondkar & J. John, 2002. Primary productivity in Mandovi-Zuari estuaries in Goa. Journal of the Marine Biological Association of India 44: 1– 3.

    Google Scholar 

  • Laanbroek, H. J. & J. C. Verplanke, 1986. Seasonal changes in percentages of attached bacteria enumerated in a tidal and a stagnant coastal basin: relation to bacterioplankton productivity. FEMS Microbiology Ecology 38: 87–98.

    Article  Google Scholar 

  • Lund, J. W. G., C. Kippling & E. D. Le Gren, 1958. The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11:143–170.

    Article  Google Scholar 

  • Mackereth, F. J. H., J. E. Heron, & J. F. Talling (eds), 1978. Water analysis: some revised methods for limnologist. Freshwater Biological Association. n 36. Titus Wilson & Sons Inc., Kendall.

  • Malone, T. C. & H. W. Ducklow, 1990. Microbial biomass in the coastal plume of Chesapeake Bay: phytoplanktonbacterioplankton relationships. Limnology and Oceanography 35: 296–312.

    CAS  Google Scholar 

  • Manager, R. J., M. L. Pace, P. A. del Giorgio, N. F. Caraco & J. J. Cole, 2004. Longitudinal Spatial Patterns of Bacterial Production and Respiration in a Large River–Estuary: Implications for Ecosystem Carbon Consumption. Ecosystems 8: 1–14.

    Google Scholar 

  • Mesquita, H. D. S. L., 1994. Planktonic microbial community oxygen consumption rate in Cananéia waters (25°S 48°W), Brazil. Netherlands Journal of Aquatic Ecology 28: 441–451.

    Google Scholar 

  • Middelburg, J. J. & J. Nieuwenhuize, 2000. Uptake if dissolved inorganic nitrogen in turbid, tidal estuaries. Marine Ecology Progress Series 192: 79–88.

    Article  CAS  Google Scholar 

  • Murrell, M. C., J. T. Hollibaugh, M. W. Silver & P. S. Wong, 1999. Bacterioplankton dynamics in Northern San Francisco Bay: Role of particle association and seasonal freshwater flow. Limnology and Oceanography 44: 295–308.

    Google Scholar 

  • Murrell, M. C, 2003. Bacterioplankton dynamics in a subtropical estuary: Evidence for substrate limitation. Aquatic Microbial Ecology 32: 239–250.

    Article  Google Scholar 

  • Odebrecht, C., P. C. Abreu, O. O. Möller Jr., L. F. Niencheski, L. A. Proenca & L. C. Torgan, 2005. Drought effects on pelagic properties in the shallow and turbid Patos Lagoon, Brazil. Estuaries 28: 675–685.

    Google Scholar 

  • Pan, L. A., J. Zhang & L. H. Zhang, 2007. Picophytoplankton, nanophytoplankton, heterotrohpic bacteria and viruses in the Changjiang Estuary and adjacent coastal waters. Journal of Plankton Research 29: 187–197.

    Article  Google Scholar 

  • Passow, U. & A. L. Alldredge, 1995. A dye-binding assay for the spectrophotometric measurement of transparent exopolymer particles (TEP). Limnology and Oceanography 40: 1326–1335.

    CAS  Google Scholar 

  • Pedrós-Aliós, C. & T. D. Brock, 1983. The importance of attachment to particles for planktonic bacteria. Archiv für Hydrobiologie 98: 354–379.

    Google Scholar 

  • Poole, H. H. & W. R. G. Atkins, 1929. Photo-electric measurements of submarine illumination throughout the year. Journal of Marine Biological Association 16: 297–324.

    Google Scholar 

  • Porter, K. G. & Y. S. Feig, 1980. The use of DAPI for identifying and counting aquatic microflora. Limnology and Oceanography 25: 943–948.

    Article  Google Scholar 

  • Raymond, P. A., J. E. Bauer & J. J. Cole, 2000. Atmospheric CO2 evasion, dissolved inorganic carbon production, and net heterotrophy in the York River estuary. Limnology and Oceanography 45: 1707–1717.

    CAS  Google Scholar 

  • Revilla, M., A. Iriarte, I. Madariaga & E. Orive, 2000. Bacterial and phytoplankton dynamics along a trophic gradient in a shallow temperate estuary. Estuarine Coastal and Shelf Science 50: 297–313.

    Article  Google Scholar 

  • Shiah, F. K. & H. W. Ducklow, 1994. Temperature regulation of heterotrophic bacterioplankton abundance production, and specific growth rate in Chesapeake Bay. Limnology and Oceanography 39:1243–1258.

    Article  Google Scholar 

  • Smith, D. C. & F. Azam, 1992. A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Marine Microbiological Food Webs 6:107–114.

    Google Scholar 

  • Staroscik, A. M. & D. C. Smith, 2004. Seasonal patterns in bacterioplankton abundance and production in Narragansett Bay, Rhode Island, USA. Aquatic Microbial Ecology 35: 275–282.

    Article  Google Scholar 

  • Steemann-Nielsen, E., 1952. The use of radio-active carbon (14C) for measuring organic production in the sea. Journal du Conseil Permanent International pour l’Exploration de la Mer. 18: 117–140.

    Google Scholar 

  • UNESCO, 1973. International oceanographic tables, Vol 2. National Institute of Oceanography of Great Britain, Paris.

    Google Scholar 

  • Tundisi, J. G., C. Teixeira, K. M. Tundisi, M. B. Kutner & L. Kinoshita, 1978. Plankton studies in a mangrove environment. IX. Comparative investigations with coastal oligotrophic waters. Revista Brasileira de Biologia 38:301–320.

    Google Scholar 

  • Utermöhl, H., 1958. Zur Vervollkommnung der quantitativen Phytoplankton-methodik. Mitteilungen-Internationale Vereinigung fur Theoretische und Angewandte Limnologie 9: 1–38.

    Google Scholar 

  • Ward, F. J. & M. Nakanish, 1971. A comparison of Geiger-Müeller and liquid scintilation counting methods in estimating primary productivity. Limnology and Oceanography 16: 560–563.

    Google Scholar 

  • Williams, P. J. L. B, 1981 Incorporation of microheterotrophic processes into the classical paradigm of the planktonic food web. Kieler Meeresforschungen 5: 1–28.

    Google Scholar 

  • Wright, R. T. & R. B. Coffin, 1983. Planktonic bacteria in estuaries and coastal waters of Northern Massachusetts: spatial and temporal distribution. Marine Ecology Progress Series 11: 205–216.

    Article  Google Scholar 

Download references

Acknowledgments

We thank many people involved in this work, in particular, A.C.C. Jakovac and F. P. Ricci for their help during sampling and analysis, T. Edison da Silva, M. dos Santos and the crew of “B/Pq Albacora” for their valuable help during sampling. The work was supported by FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo) through grant 2000/07162-6 and a fellowship to Barrera-Alba from the Agencia Española de Cooperación Internacional (AECI). Thanks to CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for the grant to Gianesella (302830/2003-0). And thanks also to Prof. James Hesson and PhD James T. Lee for the help in English revision.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José Juan Barrera-Alba.

Additional information

Handling editor: P. Viaroli

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barrera-Alba, J.J., Gianesella, S.M.F., Moser, G.A.O. et al. Bacterial and phytoplankton dynamics in a sub-tropical estuary. Hydrobiologia 598, 229–246 (2008). https://doi.org/10.1007/s10750-007-9156-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-007-9156-4

Keywords