Environmental Monitoring and Assessment

, Volume 184, Issue 12, pp 7141–7151 | Cite as

Environmental quality assessment combining sediment metal levels, biomarkers and macrobenthic communities: application to the Óbidos coastal lagoon (Portugal)

  • Patrícia Pereira
  • Susana Carvalho
  • Fábio Pereira
  • Hilda de Pablo
  • Miguel B. Gaspar
  • Mário Pacheco
  • Carlos Vale


Macroinvertebrate benthic communities are one of the key biological components considered for the assessment of benthic integrity in the context of the Water Framework Directive (WFD). However, under moderate contamination scenarios, the assessment of macrobenthic alterations at community level alone could be insufficient to discriminate the environmental quality of coastal and transitional waters. Keeping this in view, sediment quality of moderately contaminated sites in a coastal lagoon (Óbidos lagoon, Portugal) was assessed by the combination of sediment metal levels, Carcinus maenas biomarkers (accumulated metals and oxidative stress responses) and macrobenthic communities. Two sites were selected in confined inner branches (BS and BB) and a third one in the middle lagoon (ML). The site BB presented slightly higher levels of metals in sediment but biological variables calculated for macrobenthic data were not significantly different between sites. The biotic index M-AMBI that is being applied to assess environmental quality of transitional waters in the scope of the WFD pointed either to high (site ML) or good quality status (BS and BB) in the selected sites. However, crabs from BB site presented significantly higher levels of Ni in hepatopancreas than those from ML and macrobenthic community structure was significantly different between BB and ML. Additionally, spatial differences were obtained for oxidative stress parameters suggesting that BB site presented stressors for crabs (higher GST and lower GSHt at BB site). Factor analysis (PCA) integrating sediment contamination, biomarkers in crabs and macrobenthic data also distinguished BB site as the most environmentally disturbed. On the other hand, at ML site, some macrobenthic variables (equitability and polychaetes’ diversity) were found to be enhanced by current environmental conditions, suggesting the existence of a better sediment quality. Current results pointed to the usefulness of integrating macrobenthic community alterations with responses at organism level (bioaccumulation and biochemical endpoints) in order to increase the accuracy of environmental quality assessment in lagoon systems. Moreover, the application of different statistical methods was also found to be recommendable.


Sediment quality Metals Macrobenthic communities Carcinus maenas Oxidative stress Óbidos lagoon 



Patrícia Pereira (SFRH/BD/17616/2004) and Susana Carvalho (SFRH/BPD/26986/2006) benefit from Ph.D. and post-doctoral grants, respectively, awarded by Fundação para a Ciência e a Tecnologia” (FCT). Authors would like to thank to Dulce Subida for help with PERMANOVA analysis. This work was financially supported by the company “Águas do Oeste” within the project “Monitoring and modelling the Óbidos lagoon and the Foz do Arelho submarine outlet”. The manuscript was greatly improved by the comments of two anonymous reviewers.


  1. Accornero, A., Gnerre, R., & Manfra, L. (2008). Sediment concentrations of trace metals in the Berre Lagoon (France): an assessment of contamination. Archives of Environmental Contamination and Toxicology, 54, 372–385.CrossRefGoogle Scholar
  2. Allan, I. J., Vrana, B., Greenwood, R., Mills, G. A., Roig, B., & Gonzalez, C. (2006). A “toolbox” for biological and chemical monitoring of the European Union’s Water Framework Directive. Talanta, 69, 302–322.CrossRefGoogle Scholar
  3. Altun, O., Saçan, M. T., & Erdem, A. K. (2009). Water quality and heavy metal monitoring in water and sediment samples of the Küçükçekmece Lagoon, Turkey (2002–2003). Environmental Monitoring and Assessment, 151, 345–362.CrossRefGoogle Scholar
  4. Anderson, M. J., Gorley, R. N., & Clarke, K. R. (2008). PERMANOVA + for PRIMER: guide to statistical methods (p. 214). Plymouth: PRIMER-E.Google Scholar
  5. Blanchet, H., Lavesque, N., Ruellet, T., Dauvin, J. C., Sauriau, P. G., Desroy, N., Desclaux, C., Leconte, M., Bachelet, G., Janson, A.-L., Bessineton, C., Duhamel, S., Jourde, J., Mayot, S., Simon, S., & de Montaudouin, X. (2008). Use of biotic indices in semi-enclosed coastal ecosystems and transitional waters habitats—implications for the implementation of the European Water Framework Directive. Ecological Indicators, 8, 360–372.CrossRefGoogle Scholar
  6. Borja, A., Franco, J., & Pérez, V. (2000). A marine biotic index to establish the ecological quality of soft-bottom benthos within European estuarine and coastal environments. Marine Pollution Bulletin, 40, 1100–1114.CrossRefGoogle Scholar
  7. Carvalho, S., Moura, A., Gaspar, M. B., Pereira, P., Cancela da Fonseca, L., Falcão, M., Drago, T., Leitão, F., & Regala, J. (2005). Spatial and inter-annual variability of the macrobenthic communities within a coastal lagoon (Óbidos lagoon) and its relationship with environmental parameters. Acta Oecologica, 27, 143–159.CrossRefGoogle Scholar
  8. Carvalho, S., Gaspar, M. B., Moura, A., Vale, C., Antunes, P., Gil, O., Cancela da Fonseca, L., & Falcão, M. (2006). The use of the marine biotic index AMBI in the assessment of the ecological status of the Óbidos lagoon (Portugal). Marine Pollution Bulletin, 52, 1414–1424.CrossRefGoogle Scholar
  9. Carvalho, S., Pereira, P., Pereira, F., de Pablo, H., Vale, C., & Gaspar, M. B. (2011). Factors structuring temporal and spatial dynamics of macrobenthic communities in a eutrophic coastal lagoon (Óbidos lagoon, Portugal). Marine Environmental Research, 71, 97–110.CrossRefGoogle Scholar
  10. Choueri, R. B., Cesar, A., Torres, R. J., Abessa, D. M. S., Morais, R. D., Pereira, C. D. S., Nascimento, M. R. L., Mozeto, A. A., Riba, I., & DelValls, T. A. (2009). Integrated sediment quality assessment in Paranaguá Estuarine System, Southern Brazil. Ecotoxicology and Environmental Safety, 72, 1824–1831.CrossRefGoogle Scholar
  11. Claiborne, A. (1985). Catalase activity. In R. A. Greenwall (Ed.), CRC handbook of methods in oxygen radical research (pp. 283–284). Boca Raton, FL: CRC Press.Google Scholar
  12. Cohen, A. N., Carlton, J. T., & Fountain, M. C. (1995). Introduction, dispersal and potential impacts of the green crab Carcinus maenas in San Francisco Bay, California. Marine Biology, 122, 225–237.Google Scholar
  13. D’Adamo, R., Di Stasio, M., Fabbrocini, A., Petitto, F., Roselli, L., & Volpe, M. G. (2008). Migratory crustaceans as biomonitors of metal pollution in their nursery areas. The Lesina lagoon (SE Italy) as a case study. Environmental Monitoring and Assessment, 143, 15–24.CrossRefGoogle Scholar
  14. Depledge, M., & Galloway, T. S. (2005). Healthy animals, healthy ecosystems. Frontiers in Ecology and the Environment, 3, 251–258.CrossRefGoogle Scholar
  15. Elliott, M., & Quintino, V. (2007). The Estuarine Quality Paradox, Environmental Homeostasis and the difficulty of detecting anthropogenic stress in naturally stressed areas. Marine Pollution Bulletin, 54, 640–645.CrossRefGoogle Scholar
  16. Escobar, J. A., Rubio, M. A., & Lissi, E. A. (1996). SOD and catalase inactivation by singlet oxygen and peroxyl radicals. Free Radical Biology & Medicine, 20(3), 285–290.CrossRefGoogle Scholar
  17. Fernandes, C., Fontaínhas-Fernandes, A., Ferreira, M., & Salgado, M. A. (2008). Oxidative stress response in gill and liver of Liza saliens, from the Esmoriz-Paramos Coastal Lagoon, Portugal. Archives of Environmental Contamination and Toxicology, 55(2), 262–269.CrossRefGoogle Scholar
  18. Filho, D. W., Tribess, T., Gáspari, C., Cláudio, F. D., Torres, M. A., & Magalhães, A. R. M. (2001). Seasonal changes in antioxidant defences of the digestive gland of the brown mussel (Perna perna). Aquaculture, 203, 149–158.CrossRefGoogle Scholar
  19. Gamito, S. (2008). Three main stressors acting on the Ria Formosa lagoonal system (Southern Portugal): physical stress, organic matter pollution and the land-ocean gradient. Estuarine, Coastal and Shelf Science, 77, 710–720.CrossRefGoogle Scholar
  20. Gornall, A. C., Bardawill, C. J., & David, M. M. (1949). Determination of serum proteins by means of the biuret reaction. Journal of Biological Chemistry, 177, 751–766.Google Scholar
  21. Guilherme, S., Válega, M., Pereira, M. E., Santos, M. A., & Pacheco, M. (2008). Antioxidant and biotransformation responses in Liza aurata under environmental mercury exposure—relationship with mercury accumulation and implications for public health. Marine Pollution Bulletin, 56, 845–859.CrossRefGoogle Scholar
  22. Habig, W. H., Pabst, M. J., & Jakoby, W. B. (1974). Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 249, 7130–7139.Google Scholar
  23. Long, E. R., MacDonald, D. D., Smith, S. L., & Calder, F. D. (1995). Incidence of adverse biological effects within ranges of chemical concentrations in marine and estuarine sediments. Environmental Management, 19, 81–97.CrossRefGoogle Scholar
  24. Malhadas, M. S., Leitão, P. C., Silva, A., & Neves, R. (2009). Effect of coastal waves on sea level in Óbidos lagoon, Portugal. Continental Shelf Research, 29, 1240–1250.CrossRefGoogle Scholar
  25. Martín-Díaz, M. L., Blasco, J., Sales, D., & DelValls, T. A. (2007). Biomarkers study for sediment quality assessment in Spanish ports using the crab Carcinus maenas and the clam Ruditapes philippinarum. Archives of Environmental Contamination and Toxicology, 53, 66–76.CrossRefGoogle Scholar
  26. Martín-Díaz, M. L., Blasco, J., Sales, D., & DelValls, T. A. (2008). Field validation of a battery of biomarkers to assess sediment quality in Spanish ports. Environmental Pollution, 151, 631–640.CrossRefGoogle Scholar
  27. Mohandas, J., Marshall, J. J., Duggins, G. G., Horvath, J. S., & Tiller, D. (1984). Differential distribution of glutathione and glutathione related enzymes in rabbit kidney. Possible implications in analgesic neuropathy. Cancer Research, 44, 5086–5091.Google Scholar
  28. Morales-Caselles, C., Riba, I., Sarasquete, C., & DelValls, T. A. (2008). The application of a weight of evidence approach to compare the quality of coastal sediments affected by acute (Prestige 2002) and chronic (Bay of Algeciras) oil spills. Environmental Pollution, 156, 394–402.CrossRefGoogle Scholar
  29. Morales-Caselles, C., Riba, I., & DelValls, T. A. (2009). A weight of evidence approach for quality assessment of sediments impacted by an oil spill: the role of a set of biomarkers as a line of evidence. Marine Environmental Research, 67, 31–37.CrossRefGoogle Scholar
  30. Mucha, A. P., Bordalo, A. A., & Vasconcelos, M. T. S. D. (2004). Sediment quality in the Douro river estuary based on trace metal contents, macrobenthic community and elutriate sediment toxicity test (ESTT). Journal of Environmental Monitoring, 6, 585–592.CrossRefGoogle Scholar
  31. Muxika, I., Borja, A., & Bald, J. (2007). Using historical data, expert judgement and multivariate analysis in assessing reference conditions and benthic ecological status, according to the European Water Framework Directive. Marine Pollution Bulletin, 55, 16–29.CrossRefGoogle Scholar
  32. Nunes, M., Coelho, J. P., Cardoso, P. G., Pereira, M. E., Duarte, A. C., & Pardal, M. A. (2008). The macrobenthic community along a mercury contamination in a temperate estuarine system (Ria de Aveiro, Portugal). Science of the Total Environment, 405, 186–194.CrossRefGoogle Scholar
  33. Pedersen, S. N., & Lundebye, A.-K. (1996). Metallothionein and Stress Protein Levels in Shore Crabs (Carcinus maenas) along a Trace Metal Gradient in the Fal Estuary (UK). Marine Environmental Research, 42(1–4), 241–246.CrossRefGoogle Scholar
  34. Pereira, E., Abreu, S. N., Coelho, J. P., Lopes, C. B., Pardal, M. A., Vale, C., & Duarte, A. C. (2006). Seasonal fluctuations of tissue mercury contents in the European shore crab Carcinus maenas from low and high contamination areas (Ria de Aveiro, Portugal). Marine Pollution Bulletin, 52, 1450–1457.CrossRefGoogle Scholar
  35. Pereira, P., de Pablo, H., Subida, M. D., Vale, C., & Pacheco, M. (2009a). Biochemical responses of the shore crab (Carcinus maenas) in a eutrophic and metal-contaminated coastal system (Óbidos lagoon, Portugal). Ecotoxicology and Environmental Safety, 72, 1471–1480.CrossRefGoogle Scholar
  36. Pereira, P., de Pablo, H., Vale, C., Franco, V., & Nogueira, M. (2009b). Spatial and seasonal variation of water quality in an impacted coastal lagoon (Óbidos Lagoon, Portugal). Environmental Monitoring and Assessment, 153, 281–292.CrossRefGoogle Scholar
  37. Pereira, P., de Pablo, H., Vale, C., Rosa-Santos, F., & Cesário, R. (2009c). Metal and nutrient dynamics in a eutrophic coastal lagoon (Óbidos, Portugal): the importance of observations at different time scales. Environmental Monitoring and Assessment, 158, 405–418.CrossRefGoogle Scholar
  38. Pereira, P., de Pablo, H., Rosa-Santos, F., Vale, C., & Pacheco, M. (2009d). Metal accumulation and oxidative stress in Ulva sp. substantiated by responses integration into a general stress index. Aquatic Toxicology, 91, 336–345.CrossRefGoogle Scholar
  39. Pereira, P., de Pablo, H., Vale, C., & Pacheco, M. (2010a). Combined use of environmental data and biomarkers in fish (Liza aurata) inhabiting a eutrophic and metal-contaminated coastal system - gills reflect environmental contamination. Marine Environmental Research, 69, 53–62.CrossRefGoogle Scholar
  40. Pereira, P., de Pablo, H., Carvalho, S., Vale, C., & Pacheco, M. (2010b). Daily availability of nutrients and metals in a eutrophic meso-tidal coastal lagoon (Óbidos lagoon, Portugal). Marine Pollution Bulletin, 60, 1868–1872.CrossRefGoogle Scholar
  41. Pereira, P., de Pablo, H., Subida, M. D., Vale, C., & Pacheco, M. (2011). Bioaccumulation and biochemical markers in feral crab (Carcinus maenas) exposed to moderate environmental contamination—the impact of non-contamination-related variables. Environmental Toxicology, 26, 524–540.CrossRefGoogle Scholar
  42. Rosenberg, R., Blomqvist, M., Nilsson, H. C., Cederwall, H., & Dimming, A. (2004). Marine quality assessment by use of benthic species-abundance distributions: a proposed new protocol within the European Union Water Framework Directive. Marine Pollution Bulletin, 49, 728–739.CrossRefGoogle Scholar
  43. Salas, F., Neto, J. M., Borja, A., & Marques, J. C. (2004). Evaluation of the applicability of a marine biotic index to characterize the status of estuarine ecosystems: the case of Mondego estuary (Portugal). Ecological Indicators, 4, 215–225.CrossRefGoogle Scholar
  44. Specchiulli, A., Renzi, M., Scirocco, T., Cilenti, L., Florio, M., Breber, P., Focardi, S., & Bastianoni, S. (2010). Comparative study based on sediment characteristics and macrobenthic communities in two Italian lagoons. Environmental Monitoring and Assessment, 160, 237–256.CrossRefGoogle Scholar
  45. Wang, W., & Ballatori, N. (1998). Endogenous glutathione conjugates: occurrence and biological functions. Pharmacological Reviews, 50, 335–352.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Patrícia Pereira
    • 1
    • 3
  • Susana Carvalho
    • 2
  • Fábio Pereira
    • 2
  • Hilda de Pablo
    • 1
  • Miguel B. Gaspar
    • 2
  • Mário Pacheco
    • 3
  • Carlos Vale
    • 1
  1. 1.Instituto Nacional de Recursos Biológicos (INRB/IPIMAR)LisboaPortugal
  2. 2.Instituto Nacional de Recursos Biológicos (INRB/IPIMAR)OlhãoPortugal
  3. 3.Departamento de Biologia da Universidade de AveiroCESAMAveiroPortugal

Personalised recommendations