Land-ocean fluxes in the Paranaguá Bay estuarine system, southern Brazil

Marone, Eduardo; Machado, Eunice C.; Lopes, Rubens M.; Silva, Eduardo Teixeira da

Abstracts

A worldwide modeling effort has been proposed by the LOICZ (Land-Ocean Interactions in the Coastal Zone) Program to foster the acquisition of intercomparable data on land-ocean fluxes in estuaries and continental shelf ecosystems from all continental margins. As part of the South American component of this initiative, we present flux estimates of water, salt, dissolved inorganic phosphorus (DIP), dissolved inorganic nitrogen (DIN) and plankton for the estuarine system of Paranaguá Bay, southern Brazil, based on the LOICZ modeling approach and local data obtained during the 1990's. This system is strongly influenced by a seasonal meteorological cycle, represented by the rainy/summer and dry/winter periods. Semi-diurnal tides of up to the 2.7-m range are responsible for the short time-scale dynamics. The model indicated a potential water export to the adjacent coast of up to 7 x 10(6) m³ d-1 in the dry season, and 28 x 10(6) m³ d-1 during the rainy season. The system exhibits seasonal and spatial variations in DIP and DIN fluxes. "DIP amounted to +2.3 x 10(6) mol P yr-1 and "DIN to -2.7 x 10(6) mol N yr-1, suggesting that net production of phosphate and consumption of inorganic nitrogen predominate throughout in the system. Fluxes and therefore export of DIN and eespecially of DIP are higher in the rainy season. Stoichiometric estimates based on the C:N:P ratios of the reacting particulate organic matter (mangrove and plankton detritus) suggest that net denitrification predominates all over the bay, with values between -24.3 and -10.6 x 10(6) mol N year-1. Estimated seaward outflows had little effect upon the fate of the phyto- and zooplankton biomass in different sectors of the bay. This is exemplified by the low net export of algal production from the upper to the middle sectors of the estuary.

Mass balance; DIN and DIP budgets; Plankton dynamics; Paranaguá Bay; Brazil

Um esforço global de modelagem foi proposto pelo Programa LOICZ (Land-Ocean Interactions in the Coastal Zone) para promover a aquisição de dados comparáveis sobre fluxos continente-oceano em ecossistemas estuarinos e de plataforma em todos os continentes. Como parte do componente sulamericano desta iniciativa, apresentamos neste trabalho estimativas de fluxo de água, sal, fósforo inorgânico dissolvido (DIP), nitrogênio inorgânico dissolvido (DIN) e plâncton para o sistema estuarino da Baía de Paranaguá, obtidas a partir da aplicação de modelos sugeridos pelo programa LOICZ. Este sistema é fortemente influenciado por um ciclo meteorológico sazonal, representado pelos períodos chuvosos de verão e secos de inverno. As marés semidiurnas, com variação de até 2,7 m, são responsáveis pela dinâmica estuarina de curta escala temporal. Nossos resultados indicam uma exportação potencial de água para a área costeira adjacente de até 7 x 10(6) m³ d-1 no período seco e mais de 28 x 10(6) m³ d-1 no período chuvoso. O sistema exibe variações sazonais e espaciais nos fluxos de DIP e DIN. O "DIP atingiu +2.3 x 10(6) mol P ano-1 e o "DIN to -2.7 x 10(6) mol N ano-1, sugerindo que a produção líquida de fosfato e o consumo de nitrogênio inorgânico predominam em todo o sistema. Os fluxos e, portanto, a exportação de DIN e principalmente de DIP são altos no período chuvoso. Estimativas estequiométricas baseadas nas razões C:N:P da matéria orgânica particulada reativa (detritos de origem planctônica e do manguezal) sugerem que o processo de denitrificação predomina em toda a baía, com valores entre -24.3 e -10.6 x 10(6) mol N ano-1. Os fluxos estimados em direção à área costeira adjacente tiveram pouco efeito sobre o destino da biomassa do fito- e zooplâncton nos diferentes setores da baía.

Balanço de massa; Fluxos de nitrogênio e fósforo dissolvidos; Dinâmica do plâncton; Baía de Paranaguá; Brasil

Björnberg, T. K. S. 1972. Developmental stages of some tropical and subtropical planktonic marine copepods. Stud. Fauna Cur. Other Carib. Is., 40:1-185.
Björnberg, T. K. S. 1981. Copepoda. In: Boltovskoy D (ed) Atlas del zooplancton del Atlántico Sudoccidental y métodos de trabajo com el zooplancton marino. Mar del Plata, INIDEP, p. 587-679.
Brandini, F. P. 1985a. Seasonal succession of the phytoplankton in the Bay of Paranaguá (Paraná State - Brazil). Rev. Brasil. Biol., 45(4):687-694.
Brandini, F. P. 1985b. Ecological studies in the Bay of Paranaguá. I. Horizontal distribution and seasonal dynamics of the phytoplankton. Bolm Inst. oceanogr., S Paulo, 33:139-147.
Brandini, F. P. & Thamm, C. A. C. 1994. Variações diárias e sazonais do fitoplâncton e parâmetros ambientais na Baía de Paranaguá. Nerítica, 8(1-2):55-72.
Brandini, F. P.; Thamm, C. A. & Ventura, I. 1988. Ecological studies in the Bay of Paranaguá. III. Seasonal and spatial variations of nutrients and chlorophyll-a. Nerítica, 3(1):1-30.
Camacho-Ibar, V. F.; Dupra, V.; Marshall-Crossland, J. I.; Wulff, F.; Smith, S. V. & Crossland, C. J. eds. 2002. Estuarine Systems of the Latin American Region (Regional Workshop V), and estuarine systems of the Arctic Region: carbon, nitrogen and phosphorus fluxes. LOICZ Reports and Studies No. 23, 96 p.
Chisholm, L. A. & Roff, J. C. 1990. Size-weight relationships and biomass of tropical neritic copepods off Kingston, Jamaica. Mar. Biol., 104:71-77.
Costa, J. E.; Howes, B. L.; Janik, D.; Aubrey, D.; Gunn, E. & Giblin, A. E. 1999. Managing anthropogenic nitrogen inputs to coastal embayments: Technical basis of a management strategy adopted for Buzzards Bay. Buzzards Bay Project Technical Report, 62 p.
Christian, R. R. & Thomas, C. R. 2000. Neuse River Estuary modeling and monitoring project Stage 1: Network analysis for evaluating the consequences of nitrogen loading. Water Resources Research Institute of The University of North Carolina Report No. 325-F. Raleigh, NC.
Dam, H. G. & Peterson, W. T. 1993. Seasonal contrasts in the diel vertical distribution, feeding behaviour, and grazing impact of the copepod Temora longicornis in Long Island Sound. J. Mar. Res., 51:561-594.
Day, J. W.; Smith, W. G.; Wagner, P. R. & Stowe, W. 1973. Community structure and carbon budget of a salt marsh and shallow bay estuarine system in Louisiana. Center for Wetland Resources, Louisiana State University, Baton Rouge, Publ. LUS-SG-72-04.
Deibel, D. 1985. Clearance rates of the salp Thalia democratica fed naturally occurring particles. Mar. Biol., 86:47-54.
Deibel, D. 1988. Filter feeding by Oikopleura vanhoeffeni: grazing impact on suspended particles in cold ocean waters. Mar. Biol., 99:177-186.
FEEMA. 1987. Qualidade das águas do estado do Rio de Janeiro. Rio de Janeiro: FEEMA, 86 p. v. 2.
Feigenbaum, D. 1979. Daily ration and specific daily ration of the chaetognath Sagitta enflata Mar. Biol., 54:75-82.
Gordon Jr., D. C.; Boudreau, P. R.; Mann, K. H.; Ong, J.-E., Silvert, W. L.; Smith, S. V.; Wattayakorn, G.; Wullf, F. & Yanagi, T. 1996. LOICZ Biogeochemical Modelling Guidelines. LOICZ Reports and Studies No 5, 1-96.
Ikeda, T. 1985. Metabolic rates of epipelagic marine zooplankton as a function of body mass and temperature. Mar. Biol., 85:1-11.
IPARDES, 1989. Zoneamento do Litoral Paranaense. Instituto Paranaense de Desenvolvimento Econômico e Social. Fund. Édison Vieira. Curitiba, Julho de 1989. 176 pp.
Jørgensen, S. E. 1994. Fundamentals of ecological modelling (2^nd edition). Developments in Environmental Modelling, 19, New York, 628 p.
Kelly, J. R. 1998. Quantification and potential role of ocean nutrient loading to Boston Harbor, Massachusetts, USA. Marine Ecology Progress Series.173:53-65.
Knoppers, B. A.; Brandini, F. P. & Thamm, C. A. 1987. Ecological studies in the Bay of Paranaguá. II. some physical and chemical characteristics. Nerítica 2(1):1-36.
Kuypers, M. M. M.; Sliekers, A. O.; Lavik, G.; Schmid, M.; Jørgensen, B. B.; Kuenen, J. G.; Damste, J. S. S.; Strous, M.; Mike, S. M. & Jetten, M. S. M. 2003. Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature, 422:608-611.
Lana, P. C.; Marone, E.; Lopes, R. M. & Machado, E. C. 2000. The subtropical estuarine complex of Paranaguá Bay, Brazil. In: Coastal Marine Ecosystems of Latin America, Seeliger, U., Lacerda, L.D. & Kjerfve, B. (eds.), Springer Verlag, NY, USA, 467pp.
Lopes, R. M. 1997. Zooplâncton da Baía de Paranaguá: distribuição espacial, variação temporal e interações tróficas. Thesis, Zoology Dept., UFPR, 145p.
Lopes, R. M.; Vale, R. & Brandini, F. P. 1998. Composição, abundância e distribuição espacial do zooplâncton no complexo estuarino de Paranaguá durante o inverno de 1993 e o verão de 1994. Rev. Bras. Oceanogr., 46:195-211.
Machado, E. C.; Daniel, C. B.; Brandini, N. & Queiroz, R. L. V. 1997. Temporal and spatial dynamics of nutrients and particulate suspended matter in Paranaguá Bay, PR, Brazil. Nerítica, 11:15-34.
Marone, E. & Camargo, R. 1994. Efeitos de maré meteorológica na Baía de Paranaguá, PR. Neritica, 8(1-2):73-85.
Marone, E.; Guimarães, M. R.; Prata Jr., V. P.; Klingenfuss, M. S. & Camargo, R. 1995. Caracterização Física das Condições Oceanográficas, Meteorológicas e Costeiras das Zonas Estuarinas da Baía de Paranaguá, PR. Anales del VI Congreso Latinoamericano de Ciencias del Mar. Mar del Plata, Argentina, 57-61p.
Marone, E.; Mantovanelli, A.; Klingenfuss, M. S.; Lautert, L. F. C. & Prata Jr., V. P. 1997. Transporte de material particulado em suspensão, água, sal e calor na Gamboa do Perequê num evento de maré de sizígia. Anales del VII Congreso Latinoamericano de Ciencias del Mar. Santos, Brazil, 132-135p.
Montú, M. & Cordeiro, T. A. 1988. Zooplancton del complejo estuarial de la Bahia de Paranaguá. I. Composición, dinámica de las especies, ritmos reproductivos y acción de los factores ambientales sobre la comunidad. Nerítica 3:61-83.
Nowicki, B. L.; Kelly, J. R.; Requintina, E. & Van Keuren, D. 1997. Nitrogen losses through sediment denitrification in Boston Harbor and Massachusetts Bay. Estuaries 20:626-639.
Paffenhöfer, G.-A. 1976. On the biology of Appendicularia of the southeastern North Sea. In: Persoone, G. & Jaspers, E. eds. 10^thEuropean Symposium on Marine Biology. Vol. 2, Universa Press, Belgium, p. 437-455.
Pearre, S. 1982. Feeding by Chaetognatha: aspects of inter- and intra-specific predation. Mar. Ecol. Prog. Ser., 7:33-45.
Rebello, J. & Brandini, F. P. 1990. Variação temporal de parâmetros hidrográficos e material particulado em suspensão em dois pontos fixos da Baía de Paranaguá, Paraná (junho/87 - fevereiro/88). Nerítica 5(1):95-111.
Rezende, K. R. V. 1995. Dinâmica temporal do fitoplâncton de zona de arrebentação da Praia de Pontal do Sul (Paraná). M.Sc. Dissertation, Inst. Oceanogr., Univ. S. Paulo, 130 p.
San Diego-Mcglone, M. L.; Smith, S.V. & Nicolas, V. 1999. Stoichiometric Interpretations of C:N:P Ratios in Organic Waste Materials. Marine Pollution Bulletin 40: 325-330.
Seitzinger, S. P. 1988. Denitrification in freshwater and coastal marine ecosystems: ecological and geochemical significance. Limnol. Oceanog. 33:702-724.
Smith, S. V.; Ibarra-Obando, S.; Boudreau, P. R. & Camacho-Ibar, V. F. 1997. Comparison of Carbon, Nitrogen and Phosphorus Fluxes in Mexican Coastal Lagoons, LOICZ Reports & Studies No. 10, ii + 84 pp. Texel, The Netherlands.
Soares, C. R. & Marone,E.1997. Relatório Consolidado - Convênio APPA-CEM. Curitiba. 580 p.
Teixeira, C.; Tundisi, J. & Santoro, J. Y. 1969. Plankton studies in a mangrove environment. VI. Primary production, zooplankton standing-stock and some environmental factors. Int. rev. ges. Hydrobiol., 53:289-301.
UNESCO United Nations Educacional, Scientific and Cultural Organization. 1985. The International System of Units (SI) in oceanography. IAPSO Publication Scientifique, Paris, 32:1-124.
Webber, M. K. & Roff, J. C. 1995. Annual biomass and production of the oceanic copepod community off Discovery Bay, Jamaica. Mar. Biol., 123:481-495.
Wiebe, P. H.; Boyd, S. & Cox, J. L. 1975. Relationships between zooplankton displacement volume, wet weight, dry weight and carbon. Fish. Bull., 73(4): 777-786.
Wollast, R. 1993. Interactions of carbon and nitrogen cycles in the coastal zone. In: Interactions of C, N, P and S Biogeochemical Cycles and Global Change (R. Wollast, F. T. Mackenzie & L. Chou, eds.). Springer- Verlag Berlin Heidelberg. NATO ASI Series I (4):401-445.
Zehrl, J. P & Ward, B. B. 2002. Nitrogen Cycling in the Ocean: New Perspectives on Processes and Paradigms. Applied and Environmental Microbiology: 1015-1024.

Publication Dates

Publication in this collection
08 July 2009
Date of issue
Dec 2005

History

Accepted
03 Dec 2005
Reviewed
22 Sept 2005
Received
04 Mar 2004

This work is licensed under a Creative Commons Attribution 4.0 International License.

[1] Björnberg, T. K. S. 1972. Developmental stages of some tropical and subtropical planktonic marine copepods. Stud. Fauna Cur. Other Carib. Is., 40:1-185.

[2] Björnberg, T. K. S. 1981. Copepoda. In: Boltovskoy D (ed) Atlas del zooplancton del Atlántico Sudoccidental y métodos de trabajo com el zooplancton marino. Mar del Plata, INIDEP, p. 587-679.

[3] Brandini, F. P. 1985a. Seasonal succession of the phytoplankton in the Bay of Paranaguá (Paraná State - Brazil). Rev. Brasil. Biol., 45(4):687-694.

[4] Brandini, F. P. 1985b. Ecological studies in the Bay of Paranaguá. I. Horizontal distribution and seasonal dynamics of the phytoplankton. Bolm Inst. oceanogr., S Paulo, 33:139-147.

[5] Brandini, F. P. & Thamm, C. A. C. 1994. Variações diárias e sazonais do fitoplâncton e parâmetros ambientais na Baía de Paranaguá. Nerítica, 8(1-2):55-72.

[6] Brandini, F. P.; Thamm, C. A. & Ventura, I. 1988. Ecological studies in the Bay of Paranaguá. III. Seasonal and spatial variations of nutrients and chlorophyll-a. Nerítica, 3(1):1-30.

[7] Camacho-Ibar, V. F.; Dupra, V.; Marshall-Crossland, J. I.; Wulff, F.; Smith, S. V. & Crossland, C. J. eds. 2002. Estuarine Systems of the Latin American Region (Regional Workshop V), and estuarine systems of the Arctic Region: carbon, nitrogen and phosphorus fluxes. LOICZ Reports and Studies No. 23, 96 p.

[8] Chisholm, L. A. & Roff, J. C. 1990. Size-weight relationships and biomass of tropical neritic copepods off Kingston, Jamaica. Mar. Biol., 104:71-77.

[9] Costa, J. E.; Howes, B. L.; Janik, D.; Aubrey, D.; Gunn, E. & Giblin, A. E. 1999. Managing anthropogenic nitrogen inputs to coastal embayments: Technical basis of a management strategy adopted for Buzzards Bay. Buzzards Bay Project Technical Report, 62 p.

[10] Christian, R. R. & Thomas, C. R. 2000. Neuse River Estuary modeling and monitoring project Stage 1: Network analysis for evaluating the consequences of nitrogen loading. Water Resources Research Institute of The University of North Carolina Report No. 325-F. Raleigh, NC.

[11] Dam, H. G. & Peterson, W. T. 1993. Seasonal contrasts in the diel vertical distribution, feeding behaviour, and grazing impact of the copepod Temora longicornis in Long Island Sound. J. Mar. Res., 51:561-594.

[12] Day, J. W.; Smith, W. G.; Wagner, P. R. & Stowe, W. 1973. Community structure and carbon budget of a salt marsh and shallow bay estuarine system in Louisiana. Center for Wetland Resources, Louisiana State University, Baton Rouge, Publ. LUS-SG-72-04.

[13] Deibel, D. 1985. Clearance rates of the salp Thalia democratica fed naturally occurring particles. Mar. Biol., 86:47-54.

[14] Deibel, D. 1988. Filter feeding by Oikopleura vanhoeffeni: grazing impact on suspended particles in cold ocean waters. Mar. Biol., 99:177-186.

[15] FEEMA. 1987. Qualidade das águas do estado do Rio de Janeiro. Rio de Janeiro: FEEMA, 86 p. v. 2.

[16] Feigenbaum, D. 1979. Daily ration and specific daily ration of the chaetognath Sagitta enflata Mar. Biol., 54:75-82.

[17] Gordon Jr., D. C.; Boudreau, P. R.; Mann, K. H.; Ong, J.-E., Silvert, W. L.; Smith, S. V.; Wattayakorn, G.; Wullf, F. & Yanagi, T. 1996. LOICZ Biogeochemical Modelling Guidelines. LOICZ Reports and Studies No 5, 1-96.

[18] Ikeda, T. 1985. Metabolic rates of epipelagic marine zooplankton as a function of body mass and temperature. Mar. Biol., 85:1-11.

[19] IPARDES, 1989. Zoneamento do Litoral Paranaense. Instituto Paranaense de Desenvolvimento Econômico e Social. Fund. Édison Vieira. Curitiba, Julho de 1989. 176 pp.

[20] Jørgensen, S. E. 1994. Fundamentals of ecological modelling (2^nd edition). Developments in Environmental Modelling, 19, New York, 628 p.

[21] Kelly, J. R. 1998. Quantification and potential role of ocean nutrient loading to Boston Harbor, Massachusetts, USA. Marine Ecology Progress Series.173:53-65.

[22] Knoppers, B. A.; Brandini, F. P. & Thamm, C. A. 1987. Ecological studies in the Bay of Paranaguá. II. some physical and chemical characteristics. Nerítica 2(1):1-36.

[23] Kuypers, M. M. M.; Sliekers, A. O.; Lavik, G.; Schmid, M.; Jørgensen, B. B.; Kuenen, J. G.; Damste, J. S. S.; Strous, M.; Mike, S. M. & Jetten, M. S. M. 2003. Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature, 422:608-611.

[24] Lana, P. C.; Marone, E.; Lopes, R. M. & Machado, E. C. 2000. The subtropical estuarine complex of Paranaguá Bay, Brazil. In: Coastal Marine Ecosystems of Latin America, Seeliger, U., Lacerda, L.D. & Kjerfve, B. (eds.), Springer Verlag, NY, USA, 467pp.

[25] Lopes, R. M. 1997. Zooplâncton da Baía de Paranaguá: distribuição espacial, variação temporal e interações tróficas. Thesis, Zoology Dept., UFPR, 145p.

[26] Lopes, R. M.; Vale, R. & Brandini, F. P. 1998. Composição, abundância e distribuição espacial do zooplâncton no complexo estuarino de Paranaguá durante o inverno de 1993 e o verão de 1994. Rev. Bras. Oceanogr., 46:195-211.

[27] Machado, E. C.; Daniel, C. B.; Brandini, N. & Queiroz, R. L. V. 1997. Temporal and spatial dynamics of nutrients and particulate suspended matter in Paranaguá Bay, PR, Brazil. Nerítica, 11:15-34.

[28] Marone, E. & Camargo, R. 1994. Efeitos de maré meteorológica na Baía de Paranaguá, PR. Neritica, 8(1-2):73-85.

[29] Marone, E.; Guimarães, M. R.; Prata Jr., V. P.; Klingenfuss, M. S. & Camargo, R. 1995. Caracterização Física das Condições Oceanográficas, Meteorológicas e Costeiras das Zonas Estuarinas da Baía de Paranaguá, PR. Anales del VI Congreso Latinoamericano de Ciencias del Mar. Mar del Plata, Argentina, 57-61p.

[30] Marone, E.; Mantovanelli, A.; Klingenfuss, M. S.; Lautert, L. F. C. & Prata Jr., V. P. 1997. Transporte de material particulado em suspensão, água, sal e calor na Gamboa do Perequê num evento de maré de sizígia. Anales del VII Congreso Latinoamericano de Ciencias del Mar. Santos, Brazil, 132-135p.

[31] Montú, M. & Cordeiro, T. A. 1988. Zooplancton del complejo estuarial de la Bahia de Paranaguá. I. Composición, dinámica de las especies, ritmos reproductivos y acción de los factores ambientales sobre la comunidad. Nerítica 3:61-83.

[32] Nowicki, B. L.; Kelly, J. R.; Requintina, E. & Van Keuren, D. 1997. Nitrogen losses through sediment denitrification in Boston Harbor and Massachusetts Bay. Estuaries 20:626-639.

[33] Paffenhöfer, G.-A. 1976. On the biology of Appendicularia of the southeastern North Sea. In: Persoone, G. & Jaspers, E. eds. 10^thEuropean Symposium on Marine Biology. Vol. 2, Universa Press, Belgium, p. 437-455.

[34] Pearre, S. 1982. Feeding by Chaetognatha: aspects of inter- and intra-specific predation. Mar. Ecol. Prog. Ser., 7:33-45.

[35] Rebello, J. & Brandini, F. P. 1990. Variação temporal de parâmetros hidrográficos e material particulado em suspensão em dois pontos fixos da Baía de Paranaguá, Paraná (junho/87 - fevereiro/88). Nerítica 5(1):95-111.

[36] Rezende, K. R. V. 1995. Dinâmica temporal do fitoplâncton de zona de arrebentação da Praia de Pontal do Sul (Paraná). M.Sc. Dissertation, Inst. Oceanogr., Univ. S. Paulo, 130 p.

[37] San Diego-Mcglone, M. L.; Smith, S.V. & Nicolas, V. 1999. Stoichiometric Interpretations of C:N:P Ratios in Organic Waste Materials. Marine Pollution Bulletin 40: 325-330.

[38] Seitzinger, S. P. 1988. Denitrification in freshwater and coastal marine ecosystems: ecological and geochemical significance. Limnol. Oceanog. 33:702-724.

[39] Smith, S. V.; Ibarra-Obando, S.; Boudreau, P. R. & Camacho-Ibar, V. F. 1997. Comparison of Carbon, Nitrogen and Phosphorus Fluxes in Mexican Coastal Lagoons, LOICZ Reports & Studies No. 10, ii + 84 pp. Texel, The Netherlands.

[40] Soares, C. R. & Marone,E.1997. Relatório Consolidado - Convênio APPA-CEM. Curitiba. 580 p.

[41] Teixeira, C.; Tundisi, J. & Santoro, J. Y. 1969. Plankton studies in a mangrove environment. VI. Primary production, zooplankton standing-stock and some environmental factors. Int. rev. ges. Hydrobiol., 53:289-301.

[42] UNESCO United Nations Educacional, Scientific and Cultural Organization. 1985. The International System of Units (SI) in oceanography. IAPSO Publication Scientifique, Paris, 32:1-124.

[43] Webber, M. K. & Roff, J. C. 1995. Annual biomass and production of the oceanic copepod community off Discovery Bay, Jamaica. Mar. Biol., 123:481-495.

[44] Wiebe, P. H.; Boyd, S. & Cox, J. L. 1975. Relationships between zooplankton displacement volume, wet weight, dry weight and carbon. Fish. Bull., 73(4): 777-786.

[45] Wollast, R. 1993. Interactions of carbon and nitrogen cycles in the coastal zone. In: Interactions of C, N, P and S Biogeochemical Cycles and Global Change (R. Wollast, F. T. Mackenzie & L. Chou, eds.). Springer- Verlag Berlin Heidelberg. NATO ASI Series I (4):401-445.

[46] Zehrl, J. P & Ward, B. B. 2002. Nitrogen Cycling in the Ocean: New Perspectives on Processes and Paradigms. Applied and Environmental Microbiology: 1015-1024.