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Small time scale plankton structure variations at the entrance of a tropical eutrophic bay (Guanabara Bay, Brazil)

Mariana Guenther Isabel Lima Glenda Mugrabe Denise Rivera Tenenbaum Eliane Gonzalez-Rodriguez Jean Louis Valentin About the authors


The dynamics of the plankton compartments at the entrance of Guanabara Bay (SE Brazil) were assessed during a short-term temporal survey to estimate their trophic correlations. Size-fractioned phytoplankton (picoplankton: < 2µm, nanoplankton: 2-20µm and microplankton: > 20µm) biomass and photosynthetic efficiency, composition and abundance of the auto-and heterotrophic nano-and microplankton, and mesozooplankton were evaluated at a fixed station for 3 consecutive days at 3-h intervals, in the surface and bottom (20m) layers. The variability of almost all plankton compartments in the surface layer was directly dependent on temperature, indicating the great influence of the circulation at the entrance of the bay on plankton structure. In the surface layer, the mesozooplankton seems to be sustained by both autotrophic nano-and picoplankton, this last being channeled through the microzooplankton. Near the bottom, both auto-and heterotrophic microplankton are probably supporting the mesozooplankton biomass. Our findings thus suggest that the entrance of Guanabara bay presents a multivorous food web, i.e., a combination of both grazing and microbial trophic pathways.

Phytoplankton; Microzooplankton; Mesozooplankton; Grazing food web; Microbial food web; Carbon fluxes

A dinâmica dos vários compartimentos do plâncton foi avaliada durante uma série de curta duração na entrada da baía de Guanabara (SE do Brasil), com o objetivo de estimar suas correlações tróficas. A biomassa e eficiência fotossíntética das três frações do fitoplâncton (picoplâncton: < 2µm, nanoplâncton: 2-20µm e microplâncton: > 20µm), juntamente com a composição e abundância do nano-e microplâncton auto-e heterótrofos e do mesozooplâncton, foram determinadas em uma estação fixa durante 3 dias consecutivos, a intervalos de 3h, nas camadas de superfície e de fundo (20m). A variabilidade de quase todos os compartimentos do plâncton na superfície foi diretamente relacionada à temperatura, indicando forte influência da circulação da entrada da baía na estrutura planctônica. Na camada superficial, o mesozooplâncton parece ser alimentado pelo nano-e picoplâncton autótrofos, esse último sendo sustentado pelo microzooplâncton. Próximo ao fundo, o microplâncton auto-e heterótrofo estão possivelmente sustentando a biomassa mesozooplanctônica. Nossos resultados sugerem, portanto, que na entrada da baía de Guanabara esteja estabelecida uma rede trófica multívora, i.e., uma combinação entre as cadeias microbiana e de pastagem.

Fitoplâncton; Microzooplâncton; Mesozooplâncton; Rede trófica de pastagem; Rede trófica microbiana; Fluxos de carbono

  • ADJOU, M; BENDTSEN, J; RICHARDSON, K. Modeling the influence from ocean transport, mixing and grazing on phytoplankton diversity. Ecol. Model., v. 225, p. 1927, 2012.
  • BOLTOVSKOY, D. South Atlantic Zooplankton Leiden: Backhuys Publishers, 1999. 1706 p.
  • CALBET, A.; LANDRY, M. R. Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol. Oceanogr., v. 49, p. 51-57, 2004.
  • CALBET, A.; SAIZ, E. The ciliate-copepod link in marine ecosystems. Aquat. Microb. Ecol., v. 38, p. 157-167, 2005.
  • CAMPBELL, R. G.; SHERR, E. B.; ASHJIAN, C. J.; PLOURDE, S.; SHERR, B. F.; HILL, V.; STOCKWELL, A. Mesozooplankton prey preference and grazing impact in the western Arctic Ocean. DeepSeaRes. II, v. 56, p. 1274-1289, 2009.
  • CHEN, M.; LIU, H. Experimental simulation of trophic interactions among omnivorous copepods, heterotrophic dinoflagellates and diatoms. J. Exp. Mar. Biol. Ecol., v. 403, p. 65-74, 2011.
  • DUCKLOW, H. W; STEINBERG, D. K.; BUESSELER, K. Upper ocean carbon export and the biological pump. Oceanography, v. 14, p.50-58, 2001.
  • DYER, K. R. Estuaries: a physical introduction. West Sussex: John Wiley and Sons , 1997. 195 p.
  • GASPARINI, S.; DARO, M. H.; ANTAJAN, E.; TACKX, M.; ROUSSEAU, V.; PARENT, J. Y.; LANCELOT, C. Mesozooplankton grazing during the Phaeocystis globosa bloom in the Southern Bight of the North Sea. J. Sea Res, v. 43, p. 345-356, 2000.
  • GIESECKE, R.; GONZALEZ, H. E. Mandible characteristics and allometric relations in copepods: a reliable method to estimate prey size and composition from mandible occurrence in predator guts. Rev. Chil. Hist. Nat. , v. 77, p. 607-616, 2004.
  • GIFFORD, S. M.; ROLLWAGEN-BOLLENS, G.; BOLLENS, S. M. Mesozooplankton omnivory in the upper San Francisco Estuary. Mar. Ecol. Prog. Ser., v. 348, p. 33-46, 2007.
  • GOMES, C.; MARAZZO, A; VALENTIN, J. L. 2004. The vertical migration behaviour of two calanoid copepods, Acartia tonsa Dana, 1849 and Paracalanus parvus (Claus, 1863) in a stratified tropical bay in Brazil. Crustaceana, v. 77, p. 941-954, 2004.
  • GOMES, E. A. T.; SANTOS, V. S.; TENENBAUM, D. R.; VILLAC, M. C. Protozooplankton characterization of two contrasting sites in a tropical coastal ecosystem (Guanabara Bay, RJ). Braz. J. Oceanogr., v. 55, p 2938, 2007.
  • GRIFFTHS, F. B.; FLEMINGER, A.; KIMOR, B.; VANUCCI, M. Shipboard and curating techiniques. In: UNESCO (Ed.). Zooplankton fixation and preservation - monographs on oceanographics methodology. Paris: UNESCO Regional Office, 1976. p. 17-19.
  • GUENTHER, M.; BOZELLI, R. Factors influencing algaeclay aggregation. Hydrobiologia 523: 217-223, 2004.
  • GUENTHER, M; GONZALEZ-RODRIGUEZ, E.; CARVALHO, W. F; REZENDE, C. E.; MUGRABE, G.; VALENTIN, J. L. Plankton trophic structure and particulate organic carbon production during a coastal downwelling-upwelling cycle. Mar. Ecol. Prog. Ser., v. 363, p. 109-119, 2008a.
  • GUENTHER, M.; PARANHOS, R.; REZENDE, C. E.; GONZALEZ-RODRIGUEZ, E.; VALENTIN, J. L. Dynamics of bacterial carbon metabolism at the entrance of a tropical eutrophic bay influenced by tidal oscillation. Aquat. Microb. Ecol., v. 50, p. 123-133, 2008b.
  • HARRIS, G. P.; PICCININ, B. B.; VANRYN, J. Physical variability and phytoplankton communities. 5. cell-size, niche diversification and the role of competition. Arch. Hydrobiol., v. 98, p: 215-239, 1983.
  • JICA. The study on recuperation of the Guanabara bay ecosystem Tokyo: Japan International Cooperation Agency, 1994. 537 p.
  • JONES, R. H.; FLYNN, K. J. Nutritional status and diet composition affect the value of diatoms as copepod prey. Science, v. 307, p. 1457-1459, 2005.
  • KLEPPEL G. S.; HAZZARD, S. E. Diet and egg production of the copepod Acartia tonsa in Florida Bay. II. Role of nutritional environment. Mar. Biol., v. 137, p. 111-121, 2000.
  • KÖPPEN, W. Versuch einer Klassifikation der Klimate, vorzugsweise nach ihren Beziehungen zur Pflanzenwelt. Geogr. Zeitsch., v. 6, p. 593-611; 657-679, 1900.
  • LEGENDRE, L.; Le FEVRE, J. Hydrodynamical singularities as controls of recycled versus export production in oceans. In: BERGER, W. H.; SMETACECK, V. S.; WEFER, G. (Ed.). Productivity of the ocean: present and past. Dahlem Konferenzen. Chichester: John Wiley, 1989. p. 49 -63.
  • LEGENDRE, L.; LE FEVRE, J. Microbial food webs and the export of biogenic carbon in oceans. Aquat. Microb. Ecol., v. 9, p. 69-77, 1995.
  • LEGENDRE, L.; RASSOULZADEGAN, F. Plankton and nutrient dynamics in Marine waters. Ophelia, v. 41, p. 153-172, 1995.
  • LEGENDRE, L.; RASSOULZADEGAN, F. Food-web mediated export of biogenic carbon in oceans: hydrodynamic control. Mar. Ecol. Prog. Ser., v. 145, p. 179-193, 1996.
  • LEGENDRE, L.; RIVKIN, R. B. Fluxes of carbon in the upper ocean: regulation by food-web control nodes. Mar. Ecol. Prog. Ser., v. 242, p. 95-109, 2002.
  • LIU, H.; DAGG, M. J.; STROM, S. Grazing by the calanoid copepod Neocalanus cristatus on the microbial food web in the coastal Gulf of Alaska. J. Plankton Res., v. 27, p. 647-662, 2005.
  • LIU, H.; CHEN, M.; SUZUKI, K.; WONG, C. K.; CHEN, B. Mesozooplankton selective feeding in subtropical coastal waters revealed by HPLC pigment analysis. Mar. Ecol. Prog. Ser., v. 407, p. 111-123, 2010.
  • MAYR, L. M.; TENEMBAUM, D. R.; VILLAC, M. C.; PARANHOS, R.; NOGUEIRA, C. R.; BONECKER, S. L. C.; BONECKER, A. C. T. Hydrobiological characterization of Guanabara Bay. In MAGOON, O.; NEVES C. (Ed.). Coastlines of Brazil New York: American Society of Civil Engineers, 1989. p. 124-138.
  • MIRANDA, L. B. de; CASTRO, B. M. de; KJERFVE, B. Princípios de oceanografia física dos estuários São Paulo: EDUSP, 2002. 414 p.
  • PARSONS, T.; MAITA, Y.; LALLI, C. A manual of chemical and biological methods for seawater analysis Oxford: Pergamon Press, 1984. 184 p.
  • REYNOLDS, C. S. Ecology of phytoplankton: ecology, biodiversity and conservation. Cambridge: Cambridge University Press, 2006. 535 p.
  • RIVKIN, R. B.; LEGENDRE, L. Roles of food web and heterotrophic microbial processes in upper ocean biogeochemistry: global patterns and processes. Ecol. Res., v. 17, p. 151-159, 2002.
  • ROMAN, M. R.; REAUGH M. L.; ZHANG, X. S. Ingestion of the dinoflagellate, Pfiesteria piscicida, by the calanoid copepod, Acartia tonsa Harmful Algae, v. 5, p. 435441, 2006.
  • SAIZ, E.; CALBET, A. 2011. Copepod feeding in the ocean: scaling patterns, composition of their diet and the bias of estimates due to microzooplankton grazing during incubations. Hydrobiologia, v. 666, p. 181-196, 2011.
  • SANCHEZ, N.; GONZALEZ, H. E.; IRIARTE, J. L. Trophic interactions of pelagic crustaceans in Comau Fjord (Chile): their role in the food web structure. J. Plankton Res., v. 33, p. 1212-1229, 2011.
  • SANTOS, V. S.; VILLAC, M. C.; TENENBAUM, D. R.; PARANHOS, R. Auto-and heterotrophic nanoplankton and filamentous bacteria of Guanabara bay (RJ, Brazil): estimates of cell/filament numbers versus carbon content. Braz. J. Oceanogr., v. 55, p. 133-143, 2007.
  • SCHWAMBORN, R; BONECKER, S. L. C; GALVÃO, I. B.; SILVA, T. A.; NEUMANN-LEITÃO, S. Mesozooplankton grazing under conditions of extreme eutrophication in Guanabara Bay, Brazil. J. Plankton Res., v. 26, p. 983-992, 2004.
  • SHERR, E. B.; SHERR, B. F. High-rates of consumption of bacteria by pelagic ciliates. Nature, v. 325, p. 710-711, 1987.
  • SHERR, E. B.; SHERR, B. F. Preservation and storage of samples for enumeration of heterotrophic protists. In KEMP, P. F.; SHERR, B. F.; SHERR, E. B.; COLE, J. J. (Ed.). Handbook of methods in aquatic microbial ecology Boca Raton: Lewis Publishers, 1993. p. 207-212.
  • SHERR, E.B.; SHERR, B. F. Significance of predation by protists in aquatic microbial food webs. Anton. Leeuw. Int. J. G., v. 81, p. 293-308, 2002.
  • STEEMANN-NIELSEN, E. 1952. The use of radio-active carbon (14C) for measuring organic production in the sea. J. Cons. Int. Explor. Mer, v. 18, p. 117-140, 1952.
  • STROM, S. L. Bacterivory: interactions between bacteria and their grazers. In KIRCHMAN, D. L. (Ed.). Microbial Ecology of the oceans New York: Wiley-Liss, 2000. p. 351-386.
  • STROM, S. Novel interactions between phytoplankton and microzooplankton: their influence on the coupling between growth and grazing rates in the sea. Hydrobiologia, v. 480, p. 41-54, 2002.
  • STUKEL, M. R.; LANDRY, M. R.; BENITEZ-NELSON, C. R.; GOERICKE, R. Trophic cycling and carbon export relationships in the California Current Ecosystem. Limnol. Oceanogr., v 56, p. 1866-1878, 2011.
  • TARBE, A.; UNREIN, F.; STENUITE, S; PIRLOT, S; SARMENTO, H; SINYINZA, D; DESCY. J. P. Protist herbivory: a key pathway in the pelagic food web of Lake Tanganyika. Microb. Ecol., v. 62, p. 314-323, 2011.
  • TIAN, R. C.; VEZINA, A. F.; LEGENDRE, L.; INGRAM, R. G.; KLEIN, B.; PACKARD, T.; ROY, S.; SAVENKOFF, C.; SILVERBERG, N.; THERRIAULT, J. C.; TREMBLAY, J. E. Effects of pelagic food-web interactions and nutrient remineralization on the biogeochemical cycling of carbon: a modeling approach. Deep-Sea Res II, v. 47, p. 637-662, 2000.
  • TORTAJADA, S.; NIQUIL, N.; BLANCHET, H.; GRAMI, B.; MONTANIÉ, H; DAVID, V; GLÉ, C; SAINT-BÉAT, B.; A. JOHNSON, G. A.; MARQUIS, E.; DEL AMO, Y.; DUBOIS, S.; VINCENT, D.; DUPUY, C.; JUDE, F.; HARTMANN, H. J.; SAUTOUR, B. 2012. Network analysis of the planktonic food web during the spring bloom in a semi enclosed lagoon (Arcachon, SW France). Acta Oecol., v. 40, p. 40-50, 2012.
  • UTERMÖHL, H. Zur Vervollkomnung der quantitativen Phytoplankton-Methodik. Mitt. Int. Verein. theor. angew. Limnol., v. 9, p. 1-38, 1958.
  • VALENTIN, J. L.; TENENBAUM, D. R.; BONECKER, A. C. T; BONECKER, S. L. C.; NOGUEIRA, C. R.; PARANHOS, R.; VILLAC, M. C. Caractéristiques hydrobiologiques de la baie de Guanabara (Rio de Janeiro, Brésil). J. Rech. Ocean., v. 24, p. 33-41, 1999.
  • VARGAS, C. A.; MARTINEZ, R. A.; CUEVAS, L. A.; PAVEZ, M. A.; CARTES, C.; GONZALEZ, H. E.; ESCRIBANO, R; DANERI, G. The relative importance of microbial and classical food webs in a highly productive coastal upwelling area. Limnol. Oceanogr., v. 52, p. 1495-1510, 2007.
  • VARGAS, C. A.; MARTÍNEZ, R. A. Grazing impact of natural populations of ciliates and dinoflagellates in a river-influenced continental shelf. Aquat. Microb. Ecol.,v. 56, p. 93-108, 2009.
  • VARGAS, C. A.; CONTRERAS, P. Y.; IRIARTE, J. L. 2012. Relative importance of phototrophic, heterotrophic, and mixotrophic nanoflagellates in the microbial food web of a river-influenced coastal upwelling area. Aquat. Microb. Ecol., v. 65, p. 233-248, 2012.
  • VILLAC, M. C.; TENENBAUM, D. R. The phytoplankton of Guanabara Bay, Brazil. I. Historical account of its biodiversity. Biota Neotrop., v. 10, p. 271-293, 2010.
  • WANDENESS, A. P.; MATTOS, M. A. R; NOGUEIRA, C. S. R. Copepoda (Crustacea) of Guanabara Bay, RJ. I. Specific composition. Arq. Biol. Tecnol., v. 40, p. 377-381, 1997.

Publication Dates

  • Publication in this collection
    18 Feb 2013
  • Date of issue
    Dec 2012


  • Received
    28 Mar 2011
  • Accepted
    12 Nov 2012
  • Reviewed
    29 Mar 2011
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