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A Lagrangian study of plankton trophodynamics over a diel cycle in a eutrophic estuary under upwelling influence

Published online by Cambridge University Press:  19 July 2017

Suzana G. Leles ,
Gleyci A. O. Moser ,
Jean L. Valentin  and
Gisela M. Figueiredo
Suzana G. Leles*
Affiliation:
Departamento de Biologia Marinha, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Avenida Prof. Rodolpho Rocco 211, 21941-902 Rio de Janeiro, RJ, Brasil
Gleyci A. O. Moser
Affiliation:
Departamento de Oceanografia Biológica, Faculdade de Oceanografia, Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier 524, 20550-900 Rio de Janeiro, RJ, Brasil
Jean L. Valentin
Affiliation:
Departamento de Biologia Marinha, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Avenida Prof. Rodolpho Rocco 211, 21941-902 Rio de Janeiro, RJ, Brasil
Gisela M. Figueiredo
Affiliation:
Departamento de Biologia Marinha, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Avenida Prof. Rodolpho Rocco 211, 21941-902 Rio de Janeiro, RJ, Brasil
*
Correspondence should be addressed to: S.G. Leles, Departamento de Biologia Marinha, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Avenida Prof. Rodolpho Rocco 211, 21941-902 Rio de Janeiro, RJ, Brasil email: 842283@swansea.ac.uk
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Abstract

A Lagrangian study was conducted in a eutrophic estuary (Guanabara Bay, Brazil) to investigate in situ plankton trophodynamics under the influence of the cold, nutrient-rich South Atlantic Coastal Water in a short-term temporal variability (scale of hours). We tested the hypothesis that the base of the plankton food web is composed of small cells and that microzooplankton is the main consumer of this assemblage. Samples of pico-, nano- and microplankton, as well as copepods, were collected during spring, when the entry of upwelling water in the Bay is commonly observed, and near the surface every 3 h during the 1-day sampling period. Potential predation of dinoflagellates, ciliates, copepod nauplii, copepodites and adult copepods was estimated based on predator-prey size relationships. The main trophic links in the Guanabara Bay food web for the period analysed were nanophytoplankton-copepods, nanophytoplankton-ciliates, and autotrophic dinoflagellates-heterotrophic dinoflagellates. According to microphytoplankton availability, adult copepods could not satisfy their food requirement, and nanophytoplankton represented an important supplementary food source. In fact, diel variations of nano- and microplankton biomass were opposite to that of copepods suggesting predation control by the latter on the former. The trophodynamics of Guanabara Bay, under the influence of upwelling water, resulted in marked differences from other eutrophic estuaries around the world.

Keywords

plankton food webLagrangian samplingpredationsizeeutrophic estuaryupwelling
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Issue 7 , November 2018 , pp. 1547 - 1558
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

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Footnotes

*

Current address: Department of Biosciences, College of Science, Swansea University, Swansea SA2 8PP, UK

References

REFERENCES

Aminot, A. and Chaussepied, M. (1983) Manuel des analyses chimiques en milieu marin. Brest: Centre National pour l'Exploitation des Océans (CNEXO).Google Scholar
Barton, A.D., Pershing, A.J., Litchman, E., Record, N.R., Edwards, K.F., Finkel, Z.V., Kiørboe, T. and Ward, B.A. (2013) The biogeography of marine plankton traits. Ecology Letters 16, 522–534.Google Scholar
Berggreen, U., Hansen, B. and Kiørboe, T. (1988) Food size spectra, ingestion and growth of the copepod Acartia tonsa during development: implications for determination of copepod production. Marine Biology 99, 341–352.Google Scholar
Braga, E.S. and Niencheski, L.F.H. (2006) Composição das massas de água e seus potenciais produtivos na área entre o Cabo de São Tomé (RJ) e o Chuí (RS). In Rossi-Wongtschowski, C.L.D.B. and Madureira, L.S.P. (eds) O ambiente oceanográfico da plataforma continental e do talude na região Sudeste-Sul do Brasil. São Paulo: Edusp, pp. 161–218.Google Scholar
Caron, D.A. (1984) The role of heterotrophic microflagellates in plankton communities. PhD thesis. Woods Hole Oceanographic Institution, MA, USA.Google Scholar
Chen, B., Liu, H., Landry, M., Chen, M., Sun, J., Shek, L., Chen, X. and Harrison, P. (2009) Estuarine nutrient loading affects phytoplankton growth and microzooplankton grazing at two contrasting sites in Hong Kong coastal waters. Marine Ecology Progress Series 379, 77–90.Google Scholar
Durbin, G. and Durbin, A.G. (1978) Length and weight relationships of Acartia clausi from Narragansett Bay, R.I. Limnology and Oceanography 23, 958–969.Google Scholar
Fenchel, T. (1988) Marine plankton food chains. Annual Review of Ecology and Systematics 19, 19–38.Google Scholar
Figueiredo, G.M., Nash, R.D.M. and Montagnes, D.J.S. (2005) The role of the generally unrecognised microprey source as food for larval fish in the Irish Sea. Marine Biology 148, 395–404.Google Scholar
Finkel, Z.V., Vaillancourt, C.J., Irwin, A.J., Reavie, E.D. and Smol, J.P. (2009) Environmental control of diatom community size structure varies across aquatic ecosystems. Proceedings of the Royal Society of Biology 276, 1627–1634.Google Scholar
Fistarol, G.O., Coutinho, F.H., Moreira, A.P.B., Venas, T., Cánovas, A., de Paula, S.E.M., Coutinho, R., de Moura, R.L., Valentin, J.L., Tenenbaum, D.R., Paranhos, R., Valle, R.A.B., Vicente, A.C.P., Filho, G.M.A., Pereira, R.C., Kruger, R., Rezende, C.E., Thompson, C.C., Salomon, P.S. and Thompson, F.L. (2015) Environmental and sanitary conditions of Guanabara Bay, Rio de Janeiro. Frontiers in Microbiology 6, 1–17.Google Scholar
Froneman, P.W. (2002) Trophic cascading in an oligotrophic temperate estuary, South Africa. Journal of Plankton Research 24, 807–816.Google Scholar
Froneman, P.W. and McQuaid, C.D. (1997) Preliminary investigation of the ecological role of microzooplankton in the Kariega Estuary, South Africa. Estuarine, Coastal and Shelf Science 45, 689–695.Google Scholar
Fuchs, H. and Franks, P. (2010) Plankton community properties determined by nutrients and size-selective feeding. Marine Ecology Progress Series 413, 1–15.Google Scholar
Fuhrman, J.A., Eppley, R.W., Hagström, A. and Azam, F. (1985) Diel variations in bacterioplankton, phytoplankton, and related parameters in the Southern California Bight. Marine Ecology Progress Series 27, 9–20.Google Scholar
Gifford, D.J. (1988) Impact of grazing by microzooplankton in the Northwest Arm of Halifax Harbour, Nova Scotia. Marine Ecology Progress Series 47, 249–258.Google Scholar
Gifford, D.J. and Caron, D.A. (2000) Sampling, preservation, enumeration and biomass of marine protozooplankton. In Harris, R.P., Wiebe, P., Lenz, J., Skjoldal, H.R. and Huntley, M. (eds) ICES Zooplankton Methodology Manual. London: Academic Press, pp. 193–221.Google Scholar
Gomes, E.A.T., Santos, V.S., Tenenbaum, D.R. and Villac, M.C. (2007) Protozooplankton characterization of two contrasting sites in a tropical coastal ecosystem (Guanabara Bay, RJ). Brazilian Journal of Oceanography 55, 29–38.Google Scholar
Guenther, M., Lima, I., Mugrabe, G., Tenenbaum, D.R., Gonzalez-Rodriguez, E. and Valentin, J.L. (2012) Small time scale plankton structure variations at the entrance of a tropical eutrophic bay (Guanabara Bay, Brazil). Brazilian Journal of Oceanography 60, 405–414.Google Scholar
Guenther, M., Paranhos, R., Rezende, C.E., Gonzalez-Rodriguez, E. and Valentin, J.L. (2008) Dynamics of bacterial carbon metabolism at the entrance of a tropical eutrophic bay influenced by tidal oscillation. Aquatic Microbial Ecology 50, 123–133.Google Scholar
Hansen, B., Bjørsen, P.K. and Hansen, P.J. (1994) The size ratio between planktonic predators and their prey. Limnology and Oceanography 39, 395–403.Google Scholar
Hansen, P.J., Koefoed, P. and Hansen, B.W. (1997) Zooplankton grazing and growth: scaling within the 2–2,000-μm body size range. Limnology and Oceanography 42, 687–704.Google Scholar
Heinle, D.R., Harris, R.P., Ustach, J.F. and Flemer, D.A. (1977) Detritus as food source for estuarine copepods. Marine Biology 40, 341–353.Google Scholar
Hunt, R.J. and Matveev, V.F. (2005) The effects of nutrients and zooplankton community structure on phytoplankton growth in a subtropical Australian reservoir: an eclosure study. Limnologica 35, 90–101.Google Scholar
Iriarte, A., Madariaga, I., Revilla, M. and Sarobe, A. (2003) Short-term variability in microbial food web dynamics in a shallow tidal estuary. Aquatic Microbial Ecology 31, 145–161.Google Scholar
Jakobsen, H.H. and Hansen, P.J. (1997) Prey size selection, grazing and growth response of the small heterotrophic dinoflagellate Gymnodinium sp. and the ciliate Balanion comatum – a comparative study. Marine Ecology Progress Series 158, 75–86.Google Scholar
Jakobsen, H.H. and Strom, S.L. (2004) Circadian cycles in growth and feeding rates of heterotrophic protist plankton. Limnology and Oceanography 49, 1915–1922.Google Scholar
Jeong, H.J., Du Yoo, Y., Kim, S.T. and Kang, N.S. (2004) Feeding by the heterotrophic dinoflagellate Protoperidinium bipes on the diatom Skeletonema costatum. Aquatic Microbial Ecology 36, 171–179.Google Scholar
Jeong, H.J., Kim, T.H., Yoo, Y.D., Yoon, E.Y., Kim, J.S., Seong, K.A., Kim, K.Y. and Park, J.Y. (2011) Grazing impact of heterotrophic dinoflagellates and ciliates on common red-tide euglenophyte Eutreptiella gymnastica in Masan Bay, Korea. Harmful Algae 10, 576–588.Google Scholar
Jeong, H.J., Seong, K.A., Yoo, Y.D., Kim, T.H., Kang, N.S., Kim, S., Park, J.Y., Kim, J.S., Kim, G.H. and Song, J. (2008) Feeding and grazing impact by small marine heterotrophic dinoflagellates on heterotrophic bacteria. Journal of Eukaryotic Microbiology 55, 271–288.Google Scholar
Justić, D., Rabalais, N.N. and Turner, R.E. (1995) Stoichiometric nutrient balance and origin of coastal eutrophication. Marine Pollution Bulletin 30, 41–46.Google Scholar
Kamiyama, T., Tsujino, M., Matsuyama, Y. and Uchida, T. (2005) Growth and grazing rates of the tintinnid ciliate Favella taraikaensis on the toxic dinoflagellate Alexandrium tamarense. Marine Biology 147, 989–997.Google Scholar
Kim, J.S. and Jeong, H.J. (2004) Feeding by the heterotrophic dinoflagellates Gyrodinium dominans and G. spirale on the red-tide dinoflagellate Prorocentrum minimum. Marine Ecology Progress Series 280, 85–94.Google Scholar
Kiørboe, T., Møhlenberg, F. and Riisgárd, H.U. (1985) In situ feeding rates of planktonic copepods: a comparison of four methods. Journal of Experimental Marine Biology and Ecology 88, 67–81.Google Scholar
Kjerfve, B., Ribeiro, C.H.A., Dias, G.T.M., Filippo, A.M. and Quaresma, V.S. (1997) Oceanographic characteristics of an impacted coastal bay: Baía de Guanabara, Rio de Janeiro, Brazil. Continental Shelf Research 17, 1609–1643.Google Scholar
Kozlowsky-Suzuki, B., Carlsson, P., Rühl, A. and Granéli, E. (2006) Food selectivity and grazing impact on toxic Dinophysis spp. by copepods feeding on natural plankton assemblages. Harmful Algae 5, 57–68.Google Scholar
Landry, M.R., Ohman, M.D., Goericke, R., Stukel, M.R. and Tsyrklevich, K. (2009) Lagrangian studies of phytoplankton growth and grazing relationships in a coastal upwelling ecosystem off Southern California. Progress in Oceanography 83, 208–216.Google Scholar
Ledwell, J.R., Watson, A.J. and Law, C.S. (1993) Evidence for slow mixing across the pycnocline from an open-ocean tracer-release experiment. Nature 364, 701–703.Google Scholar
Loferer-Krössbacher, M., Klima, J. and Psenner, R. (1998) Determination of bacterial cell dry mass by transmission electron microscopy and densitometric image analysis. Applied and Environmental Microbiology 64, 688–694.Google Scholar
Longhurst, A., Sathyendranath, S., Platt, T. and Caverhill, C. (1995) An estimate of global primary production in the ocean from satellite radiometer data. Journal of Plankton Research 17, 1245–1271.Google Scholar
Lonsdale, D.J., Cosper, E.M., Kim, W., Doall, M., Divadeenam, A. and Jonasdottir, S.H. (1996) Food web interactions in the plankton of Long Island bays, with preliminary observations on brown tide effects. Marine Ecology Progress Series 134, 247–263.Google Scholar
López, E., Viesca, L. and Anadón, R. (2007) Seasonal variation in abundance and feeding rates of the first stages of copepods in a temperate sea. Marine Ecology Progress Series 352, 161–175.Google Scholar
MacArthur, R.H. and Pianka, E.R. (1966) On optimal use of a patchy environment. American Naturalist 100, 603–609.Google Scholar
McManus, G.B. and Ederington-Cantrell, M.C. (1992) Phytoplankton pigments and growth rates, and microzooplankton grazing in a large temperate estuary. Marine Ecology Progress Series 87, 77–85.Google Scholar
Menden-Deuer, S. and Lessard, E.J. (2000) Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnology and Oceanography 45, 569–579.Google Scholar
Menden-Deuer, S., Lessard, E.J. and Satterberg, J. (2001) Effect of preservation on dinoflagellates and diatom cell volume and consequences for carbon biomass predictions. Marine Ecology Progress Series 222, 41–50.Google Scholar
Morales, C.E., Harris, R.P., Head, R.N. and Tranter, P.R.G. (1993) Copepod grazing in the oceanic northeast Atlantic during a 6 week drifting station: the contribution of size classes and vertical migrants. Journal of Plankton Research 15, 185–211.Google Scholar
Muir, L.R. (1982) Identification of internal tides in tidal current records from the middle estuary of the St. Lawrence. In El-Shaarawi, A.H. and Esterby, S.R. (eds) Developments in water science. Ontario: Elsevier, pp. 189–207.Google Scholar
Murrel, M.C. and Hollibaugh, J.T. (1998) Microzooplankton grazing in northern San Francisco Bay measured by the dilution method. Aquatic Microbial Ecology 15, 53–63.Google Scholar
Neveux, J. and Lantoine, F. (1993) Spectrofluorometric assay of chlorophylls and phaeopigments using the least squares approximation technique. Deep Sea Research Part I: Oceanographic Research Papers 40, 1747–1765.Google Scholar
Ohman, M.D., Durbin, E.G., Runge, J.A., Sullivan, B.K. and Field, D.B. (2008) Relationship of predation potential to mortality of Calanus finmarchicus on Georges Bank, northwest Atlantic. Limnology and Oceanography 53, 1643–1655.Google Scholar
Olbers, D., Willebrand, J. and Carsten, E. (2012) Ocean dynamics. Germany: Springer.Google Scholar
Pagano, M., Champalbert, G., Maryse, A., Kouassi, E., Arfi, R., Got, P., Troussellier, M., N'Dour, E.H., Corbin, D. and Bouvy, M. (2006) Herbivorous and microbial grazing pathways of metazooplankton in the Senegal River Estuary (West Africa). Estuarine, Coastal and Shelf Science 67, 369–381.Google Scholar
Parvathi, A., Jasna, V., Haridevi, K.C., Jina, S., Greeshma, M., Breezy, J. and Nair, M. (2013) Diurnal variations in bacterial and viral production in Cochin estuary, India. Environmental Monitoring and Assessment 185, 8077–8088.Google Scholar
Pérez, M.T., Dolan, J.R., Vidussi, F. and Fukai, E. (2000) Diel vertical distribution of planktonic ciliates within the surface layer of the NW Mediterranean (May 1995). Deep Sea Research Part I: Oceanographic Research Papers 47, 479–503.Google Scholar
Porter, K.G. and Feig, Y.S. (1980) The use of DAPI for identifying and counting aquatic microflora. Limnology and Oceanography 25, 943–948.Google Scholar
R Core Team (2016) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
Riemann, B., Simonsen, P. and Stensgaard, L. (1989) The carbon and chlorophyll content of phytoplankton from various nutrient regimes. Journal of Plankton Research 11, 1037–1045.Google Scholar
Riisgård, H.U., Madsen, C.V., Barth-Jensen, C. and Purcel, J.E. (2012) Population dynamics and zooplankton-predation impact of the indigenous scyphozoan Aurelia aurita and the invasive ctenophore Mnmiopsis leidyi in Limfjorden (Denmark). Aquatic Invasions 7, 147–162.Google Scholar
Robertson, J.R. (1983) Predation by estuarine zooplankton on tintinnid ciliates. Estuarine, Coastal and Shelf Science 16, 27–36.Google Scholar
Santos, A.L., Mendes, C., Gomes, N.C.M., Henriques, I., Correia, A., Almeida, A. and Cunha, A. (2009) Short-term variability of abundance, diversity and activity of estuarine bacterioneuston and bacterioplankton. Journal of Plankton Research 12, 1545–1555.Google Scholar
Santos, V.S., Villac, M.C., Tenenbaum, D.R. and Paranhos, R. (2007) Auto- and heterotrophic nanoplankton and filamentous bacteria of Guanabara Bay (RJ, Brazil): estimates of cell/filament numbers versus carbon content. Brazilian Journal of Oceanography 55, 133–143.Google Scholar
Sato, M., Yoshikawa, T., Takeda, S. and Furuya, K. (2007) Application of the size-fractionation method to simultaneous estimation of clearance rates by heterotrophic flagellates and ciliates of pico- and nanophytoplankton. Journal of Experimental Marine Biology and Ecology 349, 334–343.Google Scholar
Schwamborn, R., Bonecker, L.C., Galvão, L.B., Silva, T.A. and Neumann-Leitão, S. (2004) Mesozooplankton grazing under conditions of extreme eutrophication in Guanabara Bay, Brazil. Journal of Plankton Research 26, 983–992.Google Scholar
Stoecker, D.K. and Egloff, D.A. (1987) Predation by Acartia tonsa Dana on planktonic ciliates and rotifers. Journal of Experimental Marine Biology and Ecology 110, 53–68.Google Scholar
Stramma, L. and England, M. (1999) On the water masses and mean circulation of the South Atlantic Ocean. Journal of Geophysical Research 104, 863–883.Google Scholar
Teira, E., Martínez-García, S., Fernández, E., Calvo-Díaz, A. and Morán, X.A.G. (2010) Lagrangian study of microbial plankton respiration in the subtropical North Atlantic Ocean: bacterial contribution and short-term temporal variability. Aquatic Microbial Ecology 61, 31–43.Google Scholar
Tillmann, U. and Reckermann, M. (2002) Dinoflagellate grazing on the raphidophyte Fibrocapsa japonica. Aquatic Microbial Ecology 26, 247–257.Google Scholar
Tiselius, P. (1989) Contribution of aloricate ciliates to the diet of Acartia clausi and Centropages hamatus in coastal waters. Marine Ecology Progress Series 56, 49–56.Google Scholar
Turner, J.T. and Tester, P.A. (1992) Zooplankton feeding ecology: bacterivory by metazoan microzooplankton. Journal of Experimental Marine Biology and Ecology 160, 149–167.Google Scholar
Utermöhl, H. (1958) Zur vervollkommnung der quantitativen phytoplankton-methodik. Mitteilungen Internationale Vereiningung für Theoretische und Angewandte Limnologie 9, 1–38.Google Scholar
Vargas, C.A. and González, H.E. (2004) Plankton community structure and carbon cycling in a coastal upwelling system. I. Bacteria, microprotozoans and phytoplankton in the diet of copepods and appendicularians. Aquatic Microbial Ecology 34, 151–164.Google Scholar
Verity, P.G. and Borkman, D.G. (2010) A decade of change in the Skidaway River Estuary. III. Plankton. Estuaries and Coasts 33, 513–540.Google Scholar
Verity, P.G., Robertson, C.Y., Tronzo, C.R., Andrews, M.G., Nelson, J.R. and Sieracki, M.E. (1992) Relationships between cell volume and the carbon and nitrogen content of marine photosynthetic nanoplankton. Limnology and Oceanography 37, 1434–1446.Google Scholar
Wirtz, K.W. (2012) Who is eating whom? Morphology and feeding type determine the size relation between planktonic predators and their ideal prey. Marine Ecology Progress Series 445, 1–12.Google Scholar
Zhang, W. and Wang, R. (2000) Summertime ciliate and copepod nauplii distributions and micro-zooplankton herbivorous activity in the Laizhou Bay, Bohai Sea, China. Estuarine, Coastal and Shelf Science 51, 103–114.Google Scholar