Estuaries and Coasts

, Volume 32, Issue 1, pp 111–122 | Cite as

Net Ecosystem Metabolism and Nonconservative Fluxes of Organic Matter in a Tropical Mangrove Estuary, Piauí River (NE of Brazil)

  • Marcelo F. L. Souza
  • Viviane R. Gomes
  • Simone S. Freitas
  • Regina C. B. Andrade
  • Bastiaan Knoppers


Net ecosystem metabolism (NEM) was measured in the Piauí River estuary, NE Brazil. A mass balance of C, N, and P was used to infer its sources and sinks. Dissolved inorganic carbon (DIC) concentrations and fluxes were measured over a year along this mangrove dominated estuary. DIC concentrations were high in all estuarine sections, particularly at the fluvial end member at the beginning of the rainy season. Carbon dioxide concentrations in the entire estuary were supersaturated throughout the year and highest in the upper estuarine compartment and freshwater, particularly at the rainy season, due to washout effects of carbonaceous soils and different organic anthropogenic effluents. The estuary served as a source of DIC to the atmosphere with an estimated flux of 13 mol CO2 m−2 year−1. Input from the river was 46 mol CO2 m−2 year−1. The metabolism of the system was heterotrophic, but short periods of autotrophy occurred in the lower more marine portions of the estuary. The pelagic system was more or less balanced between auto- and heterotrophy, whereas the benthic and intertidal mangrove region was heterotrophic. Estimated annual NEM yielded a total DIC production in the order of 18 mol CO2 m−2 year−1. The anthropogenic inputs of particulate C, N, and P, dissolved inorganic P (DIP), and DIC were significant. The fluvial loading of particulate organic carbon and dissolved inorganic nitrogen (DIN) was largely retained in two flow regulation and hydroelectric reservoirs, promoting a reduction of C:N and C:P particulate ratios in the estuary. The net nonconservative fluxes obtained by a mass balance approach revealed that the estuary acts as a source of DIP, DIN, and DIC, the latter one being almost equivalent to the losses to the atmosphere. Mangrove forests and tidal mudflats were responsible for most of NEM rates and are the main sites of organic decomposition to sustain net heterotrophy. The main sources for this organic matter are the fluvial and anthropogenic inputs. The mangrove areas are the highest estuarine sources of DIP, DIC, and DIN.


Autotrophy/heterotrophy Carbon dioxide fluxes Anthropogenic loading Mass balance 



We thank Dr. J. P. H. Alves for the laboratory support in the Departamento de Química/UFSE. We acknowledge Dr. E. C. G. Couto (Departamento de Ciências Biológicas/UESC) for the participation in field trips and for the important comments about biological features; Dr. S.V. Smith (CICESE) made several important contributions to the water and nutrient budgets that resulted in the data exposed in Table 3; people of the LOICZ IPO and the Instituto Argentino de Oceanografia, particularly Dr. Chris Crossland and Dr. Gerardo Perillo, for the opportunity to discuss these data and budgets during the South America Biogeochemical Budgeting Workshop held in Bahia Blanca, Argentina, in 1999. Dr. A. Raw (UESC) provided valuable critical and language review. Dr. C. A. Simenstad (University of Washington) reviewed a former version of the manuscript, resulting in several improvements. A. M. Fernandes, M. V. Carvalho, P. S. Lima, C. Assis, D. Assis, and E. Santos helped with field and laboratory assistance. Several field surveys were done in vessel of Brazilian Navy, for what we specially thank the Port Authority Cap. R. V. Dutra and Corporal F. Souza at CPSE. CNPq provided support for the work described in this paper in the form of a DCR research grant proc. no. 300.738/1995-1 (first author) and PQ grant proc. no. 300.772/2004-1 (last author).


  1. Abril, G., H. Etcheber, A.V. Borges, and M. Frankignoulle. 2000. Excess atmospheric carbon dioxide transported by rivers into the Scheldt estuary. Earth and Planetary Sciences 330: 761–768.Google Scholar
  2. Abril, G., M. Nogueira, H. Etcheber, G. Cabeçadas, E. Lemaire, and M.J. Brogueira. 2002. Behaviour of organic carbon in nine contrasting European estuaries. Estuarine, Coastal and Shelf Science 54: 241–262. doi: 10.1006/ecss.2001.0844.CrossRefGoogle Scholar
  3. Abril, G., M.-V. Commarieu, D. Maro, M. Fontagne, F. Guérin, and H. Etcheber. 2004. A massive dissolved inorganic carbon release at spring tide in a highly turbid estuary. Geophysical Research Letters 31: L09316. doi: 10.1029/2004GL019714.CrossRefGoogle Scholar
  4. Alongi, D.M. 1988. Bacterial productivity and microbial biomass in tropical mangrove sediments. Microbial Ecology 15: 59–79. doi: 10.1007/BF02012952.CrossRefGoogle Scholar
  5. Anesio, A.M., P.C. Abreu, and B.A. Biddanda. 2003. The role of free and attached microorganisms in the decomposition of estuarine macrophyte detritus. Estuarine, Coastal and Shelf Science 56: 197–201. doi: 10.1016/S0272-7714(02)00152-X.CrossRefGoogle Scholar
  6. Bano, N., M. Nisa, N. Khan, M. Saleem, P.J. Harrison, S.I. Ahmed, and 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. doi: 10.3354/meps157001.CrossRefGoogle Scholar
  7. Borges, A.V., L.-S. Schiettecatte, G. Abril, B. Delille, and F. Gazeau. 2006. Carbon dioxide in European coastal waters. Estuarine, Coastal and Shelf Science 70: 375–387. doi: 10.1016/j.ecss.2006.05.046.CrossRefGoogle Scholar
  8. Boto, K.G., and A.I. Robertson. 1990. The relationship between nitrogen fixation and tidal exports of nitrogen in a tropical mangrove system. Estuarine, Coastal and Shelf Science 31: 531–540. doi: 10.1016/0272–7714(90)90011-F.CrossRefGoogle Scholar
  9. Bouillon, S., M. Frankignoulle, F. Dehairs, B. Velimirov, A. Eiler, G. Abril, H. Etcheber, and A.V. Borges. 2003. Inorganic and organic carbon biogeochemistry in the Gautami Godavari estuary (Andhra Pradesh, India) during pre-monsoon: The local impact of extensive mangrove forests. Global Geochemical Cycles 17(4): 1114. doi: 10.1029/2002GB002026.CrossRefGoogle Scholar
  10. Bouillon, S., T. Moens, and F. Dehairs. 2004. Carbon sources supporting benthic mineralization in mangrove and adjacent seagrass sediments (Gazi Bay, Kenya). Biogeosciences 1: 71–78.Google Scholar
  11. Bouillon, S., J.J. Middleburg, F. Dehairs, A.V. Borges, G. Abril, M.R. Flindt, S. Ulomi, and E. Kristensen. 2007. Importance of intertidal sediment processes and porewater exchange on the water column biogeochemistry in a pristine mangrove creek (Ras Dege, Tanzania). Biogeosciences 4: 311–322.CrossRefGoogle Scholar
  12. Caffrey, J.M., J.E. Cloern, and C. Grenz. 1998. Changes in production and respiration during a spring phytoplankton bloom in San Francisco Bay, California, USA: implications for net ecosystem metabolism. Marine Ecology Progress Series 172: 1–12. doi: 10.3354/meps172001.CrossRefGoogle Scholar
  13. Cai, W.J., and Y. Wang. 1998. The chemistry, fluxes, and sources of carbon dioxide in the estuarine waters of the Satilla and Altamaha Rivers, Georgia. Limnology and Oceanography 43(4): 657–668.Google Scholar
  14. Cai, W.J., L.R. Pomeroy, M.A. Moran, and Y. Wang. 1999. Oxygen and carbon dioxide mass balance for the estuarine–intertidal marsh complex of five rivers in the southeastern U.S. Limnology and Oceanography 44(3): 639–649.Google Scholar
  15. Carmouze, J.P. 1994. O metabolismo dos ecossistemas aquáticos. In Fundamentos teóricos, métodos de estudo e análises químicas, ed. Edgard Blücher, 254. São Paulo: Fundação de Amparo à Pesquisa do Estado de São Paulo.Google Scholar
  16. Crump, B.C., and J.A. Baross. 2000. Characterization of the bacterially-active particle fraction in the Columbia River estuary. Marine Ecology Progress Series 206: 13–22. doi: 10.3354/meps206013.CrossRefGoogle Scholar
  17. Crump, B.C., J.A. Baross, and C.A. Simenstad. 1998. Dominance of particle-attached bacteria in the Columbia River estuary, USA. Aquatic Microbial Ecology 14(1): 7–18. doi: 10.3354/ame014007.CrossRefGoogle Scholar
  18. Dittmar, T., and R.J. Lara. 2001. Driving forces behind nutrient and organic matter dynamics in a mangrove tidal creek in North Brazil. Estuarine, Coastal and Shelf Science 52: 249–259. doi: 10.1006/ecss.2000.0743.CrossRefGoogle Scholar
  19. Dittmar, T., R.J. Lara, and G. Kattner. 2001. River or mangrove? Tracing major organic matter sources in tropical Brazilian coastal waters. Marine Chemistry 73: 253–271. doi: 10.1016/S0304-4203(00)00110-9.CrossRefGoogle Scholar
  20. Drever, J.I. 1982. The geochemistry of natural waters. Surface and groundwater environments. Upper Sadle River, New Jersey: Prentice-Hall.Google Scholar
  21. Frankignoulle, M., I. Bourge, and R. Wollast. 1996. Atmospheric CO2 fluxes in a highly polluted estuary (the Scheldt). Limnology and Oceanography 41: 365–369.CrossRefGoogle Scholar
  22. Furukawa, K., E. Wolanski, and H. Mueller. 1997. Currents and sediment transport in mangrove forests. Estuarine, Coastal and Shelf Science 44: 301–310. doi: 10.1006/ecss.1996.0120.CrossRefGoogle Scholar
  23. Gordon, D.C. Jr., P.R. Boudreau, K.H. Mann, J.-E. Ong, W.L. Silvert, S.V. Smith, G. Wattayakorn, F. Wulff, and T. Yanagi. 1996. LOICZ Biogeochemical Modelling Guidelines. LOICZ Reports & Studies No. 5., 2nd Edition. Texel, The Netherlands: LOICZ IPO, vi + 96 pp.Google Scholar
  24. Grasshoff, K., M. Ehrardt, and K. Kremling. 1983. Methods of seawater analysis. Weinhein: Verlag Chemie, 419 pp.Google Scholar
  25. Hall, C.A.S., and R. Moll. 1975. Methods of assessing aquatic primary productivity. In Primary productivity of the Biophere, eds. H. Lieth, , and R. H. Whittaker, 19–53. Berlin: Springer.Google Scholar
  26. Hopkinson, C.S., and J.J. Vallino. 1995. The relationship among man’s activities in watersheds and estuaries: a model of runoff effects on patterns of estuarine community metabolism. Estuaries 18(4): 598–621. doi: 10.2307/1352380.CrossRefGoogle Scholar
  27. Kempe, S. 1982. Long term records of CO2 pressure fluctuations in fresh waters. In Transport of carbon and minerals in major rivers. Part 1, ed. E.T. Degens, 91–332. Hamburg: Universitat Hamburg.Google Scholar
  28. Lanza, G., F.J. Flores-Verdugo, and F. Wulff. 1997. Teacapan-Agua Brava-Marismas Nacionales, Sinaloa and Nayarit. In Comparison of carbon, nitrogen and phosphorus fluxes in Mexican coastal lagoons. LOICZ Reports & Studies No. 10, eds. S.V. Smith, S. Ibarra-Orlando, P.R. Boudreau and V. Camacho-Ibar, 38–42. Texel, The Netherlands: LOICZ IPO, ii + 84 pp.Google Scholar
  29. Lee, S.Y. 1995. Mangrove outwelling: a review. In Asia-Pacific Symposium on mangrove ecosystems. Hydrobiologia 295, eds. Y.S. Wong and N.F.Y. Tam, 203–212. The Netherlands: Springer.Google Scholar
  30. Mukhopadhyay, S.K., H. Biswas, T.K. De, B.K. Sen, S. Sen, and T.K. Jana. 2002. Impact of Sundarban mangrove biosphere on the carbon dioxide and methane mixing ratios at the NE Coast of Bay of Bengal, India. Atmospheric Environment 36: 629–638. doi: 10.1016/S1352-2310(01)00521-0.CrossRefGoogle Scholar
  31. Mukhopadhyay, S.K., H. Biswas, T.K. Dea, and T.K. Jana. 2006. Fluxes of nutrients from the tropical River Hooghly at the land–ocean boundary of Sundarbans, NE Coast of Bay of Bengal, India. Journal of Marine Systems 62: 9–21. doi: 10.1016/j.jmarsys.2006.03.004.CrossRefGoogle Scholar
  32. Nixon, S.W., and M.E.Q. Pilson. 1984. Estuarine total system metabolism and organic exchange calculated from nutrient ratios: an example from Narragansett Bay. In The estuary as a filter, ed. V. S. Kennedy, , 261–290. Orlando: Academic.Google Scholar
  33. Odum, E.P., and E.J. Heald. 1975. The detritus bases food web of an estuarine mangrove community. In Estuarine research, ed. L. E. Cronin, , 265–286. New York: Academic.Google Scholar
  34. Smith, S.V., and M.J. Atkinson. 1994. Mass balance of nutrient fluxes in coastal lagoons. In: Coastal lagoon processes, ed. B. Kjerfve, 133–155. Amsterdam: Elsevier.CrossRefGoogle Scholar
  35. Smith, S.V., and J.T. Hollibaugh. 1997. Annual cycle and interannual variability of ecosystem metabolism in a temperate climate embayment. Ecological Monographs 67(4): 509–533.Google Scholar
  36. Smith, E.M., and W.M. Kemp. 2001. Size structure and the production/respiration balance in a coastal plankton community. Limnology and Oceanography 46(3): 473–485.Google Scholar
  37. Smith, E.M., and W.M. Kemp. 2003. Planktonic and bacterial respiration along an estuarine gradient: responses to carbon and nutrient enrichment. Aquatic Microbial Ecology 30(3): 251–261. doi: 10.3354/ame030251.CrossRefGoogle Scholar
  38. Souza, M.F.L. 1999. Metabolismo e balanço de massa do estuário do Rio Piauí, Sergipe. Ph.D. thesis, Universidade Federal Fluminense, Niterói, Brazil.Google Scholar
  39. Souza, M.F.L., and E.C.G. Couto. 1999. Short-term changes and longitudinal distribution of carbon metabolism in the Piauí River estuary (Sergipe, Brazil). Revista Brasileira de Biologia 59(2): 24–27. doi: 10.1590/S0034-71081999000200003.CrossRefGoogle Scholar
  40. Souza, M.F.L., V.R. Gomes, S.S. Freitas, R.C.B. Andrade, B.A. Knoppers, and S.V. Smith. 2000. Piaui River Estuary, Sergipe State. In Estuarine systems of the South American region: carbon, nitrogen and phosphorus fluxes. LOICZ Reports & Studies No. 15, eds. S.V. Smith, V. Dupra, J.I. Marshall Crossland, and C.J. Crossland, 10–17. Texel, The Netherlands: LOICZ, ii + 87 p.Google Scholar
  41. Strickland, J.D.H., and T.R. Parsons. 1972. A practical handbook of seawater analysis. Bulletin of Fisheries Research Board Canadian 167. The Quarterly Review of Biology 44(3): 327.Google Scholar
  42. Tam, N.F.Y. 1998. Effects of wastewater discharge on microbial populations and enzyme activities in mangrove soils. Environmental Pollution 102(2-3): 233–242. doi: 10.1016/S0269-7491(98)00084-0.CrossRefGoogle Scholar
  43. Teal, J.M. 1962. Energy flow in a salt marsh ecosystem of Georgia. Ecology 43: 614–624. doi: 10.2307/1933451.CrossRefGoogle Scholar
  44. Twilley, R.R. 1985. The exchange of organic carbon in a basin mangrove forests in a southwest Florida estuary. Estuarine, Coastal and Shelf Science 20: 543–557. doi: 10.1016/0272-7714(85)90106-4.CrossRefGoogle Scholar
  45. Wafar, S., A.G. Untawale, and M. Wafar. 1997. Litter fall and energy flux in a mangrove ecosystem. Estuarine, Coastal and Shelf Science 44: 111–124. doi: 10.1006/ecss.1996.0152.CrossRefGoogle Scholar
  46. Woitchik, A.F., B. Ohowa, J.M. Kazungu, R.G. Rao, L. Goyens, and F. Dehairs. 1997. Nitrogen enrichment during decomposition of mangrove leaf litter in an east African coastal lagoon (Kenya): relative importance of biological nitrogen fixation. Biogeochemistry 39: 15–35. doi: 10.1023/A:1005850032254.CrossRefGoogle Scholar
  47. Wong, C.H. 1984. Mangrove aquatic nutrients. In Proceedings of the Workshop on Productivity of the Mangrove Ecosystem: Management Implications, eds. J.-E. Ong and W.-K. Gong, 60–67.Google Scholar

Copyright information

© Coastal and Estuarine Research Federation 2008

Authors and Affiliations

  • Marcelo F. L. Souza
    • 1
    • 3
  • Viviane R. Gomes
    • 2
  • Simone S. Freitas
    • 2
  • Regina C. B. Andrade
    • 1
  • Bastiaan Knoppers
    • 1
  1. 1.Programa de Pós-graduação em Geoquímica, Departamento de GeoquímicaUniversidade Federal FluminenseNiteróiBrazil
  2. 2.Departamento de Engenharia QuímicaUniversidade Federal de SergipeSão CristóvãoBrazil
  3. 3.Laboratório de Oceanografia Química, PPGSAT, DCETUniversidade Estadual de Santa CruzIlhéusBrazil

Personalised recommendations