Advertisement

Macrobenthic assemblages, sediment characteristics and heavy metal concentrations in soft-bottom Ebre Delta bays (NW Mediterranean)

  • Esther JordanaEmail author
  • Susana Pinedo
  • Enric Ballesteros
Article

Abstract

The spatial distribution of soft-bottom macrofaunal assemblages and their relationship with sediment characteristics were examined in two semi-enclosed shallow-water bays (Alfacs Bay and Fangar Bay) in the Ebre Delta (Catalonia, NW Mediterranean) during 2006 and 2011. Three assemblages were identified: group 1, present in sediments that contain a high percentage of silt-clay, small median particle size and high organic matter content and located at the most external areas of both bays and in the central basin of Alfacs Bay; group 2, present in the shallow northern platform in Alfacs Bay and in both platforms in Fangar Bay, the locations which feature highly variable sediment characteristics; and group 3, present in the shallow areas of both bays, which are characterised by low silt-clay and organic matter content. In Alfacs Bay, the differentiation of these assemblages has persisted since 1987, independently of the increase in organic matter content and heavy metal concentrations and of the shift in macrofaunal composition that have occurred over the past 20 years, most likely the result of increased agricultural activity.

Keywords

Soft-bottoms Macroinvertebrates Heavy metals Ebre Delta bays Mediterranean Sea 

Notes

Acknowledgments

Funding was provided by Agència Catalana de l’Aigua (Departament de Medi Ambient i Habitatge, Generalitat de Catalunya) and INTRAMURAL-CSIC project (reference 201330E065). We are grateful to M. P. Satta for her help in field missions, sample sorting and physicochemical analysis. We thank J. Gil, N. Fernández, M. P. Satta and M. P. Mura for their contributions to species identification. Thanks are also due to M. de Torres for her constant support during this study. Finally, we are grateful to two anonymous reviewers for their useful comments on the manuscript.

References

  1. Anderson, M. J., Gorley, R. N., & Clarke, K. R. (2008). PERMANOVA+ for PRIMER: guide to software and statistical methods, Plymouth, UK.Google Scholar
  2. Blake, J. A. (2009). Redescription of Capitella capitata (Fabricius) from West Greenland and designation of a neotype (Polychaeta, Capitellidae). Zoosymposia, 2, 55–80.Google Scholar
  3. Bravo, I., Garcés, E., Diogène, J., Fraga, S., Sampedro, N., & Figueroa, I. (2006). Resting cysts of the toxigenic dinoflagellate genus Alexandrium in recent sediments from the Western Mediterranean coast, including first description of cysts of A. kutnerae and A. peruvianum. European Journal of Phycology, 41, 293–302.CrossRefGoogle Scholar
  4. Briant, N., Bancon-Montigny, C., Elbaz-Poulichet, F., Freydier, R., Delpoux, S., & Cossa, D. (2013). Trace elements in the sediments of a large Mediterranean marina (Port Camargue, France): levels and contamination history. Marine Pollution Bulletin, 73, 78–85.CrossRefGoogle Scholar
  5. Buchanan, J. B. (1963). The bottom fauna communities and their sediment relationships of the coast of Northumberland. Oikos, 14, 154–175.CrossRefGoogle Scholar
  6. Camp, J. (1994). Aproximaciones a la dinámica ecológica de una bahía estuárica mediterránea. PhD thesis, Universitat de Barcelona, Barcelona.Google Scholar
  7. Camp, J., & Delgado, M. (1987). Hidrografía de la bahías del Delta del Ebro. Investigación Pesquera, 51, 351–369.Google Scholar
  8. Carrasco, L., Díez, S., Soto, D. X., Catalan, J., & Bayona, J. M. (2008). Assessment of mercury and methylmercury pollution with zebra mussel (Dreissena polymorpha) in the Ebro River (NE Spain) impacted by industrial hazardous dumps. Science of The Total Environment, 407, 178–184.CrossRefGoogle Scholar
  9. Como, S., Magni, P., Casu, D., Floris, A., Giordani, G., Natale, S., Fenzi, G. A., Signa, G., & De Falco, G. (2007). Sediment characteristics and macrofauna distribution along a human-modified inlet in the Gulf of Oristano (Sardinia, Italy). Marine Pollution Bulletin, 54, 733–744.CrossRefGoogle Scholar
  10. Conde, A., Novais, J. M., & Domínguez, J. (2013). Intertidal macrofauna and environmental stress at a riverine-marine boundary. Marine Environmental Research, 92, 1–9.CrossRefGoogle Scholar
  11. Dauvin, J. C. (2008). Effects of heavy metal contamination on the macrobenthic fauna in estuaries: the case of the Seine estuary. Marine Pollution Bulletin, 57, 160–169.CrossRefGoogle Scholar
  12. Dauvin, J. C., & Ruellet, T. (2007). Polychaete/amphipod ratio revisited. Marine Pollution Bulletin, 55, 215–224.CrossRefGoogle Scholar
  13. Dauvin, J. C., & Ruellet, T. (2009). The estuarine quality paradox: is it possible to define an ecological quality status for specific modified and naturally stressed estuarine ecosystems? Marine Pollution Bulletin, 59, 38–47.CrossRefGoogle Scholar
  14. Day, J. W., Jr., Maltby, E., & Ibáñez, C. (2006). River basin management and delta sustainability: a commentary on the Ebro Delta and the Spanish National Hydrological Plan. Ecological Engineering, 26, 85–99.CrossRefGoogle Scholar
  15. Delgado, M. (1989). Abundance and distribution of microphytobenthos in the Bays of Ebro Delta (Spain). Estuarine, Coastal and Shelf Science, 29, 183–194.CrossRefGoogle Scholar
  16. Dutertre, M., Hamon, D., Chevalier, C., & Ehrhold, A. (2013). The use of the relationships between environmental factors and benthic macrofaunal distribution in the establishment of a baseline for coastal management. ICES Journal of Marine Science, 70, 294–308.CrossRefGoogle Scholar
  17. 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
  18. European Commission (2000). Water Framework Directive. Directive 2000/60/EC, p.72.Google Scholar
  19. Faria, M., Huertas, D., Soto, D. X., Grimalt, J. O., Catalan, J., Riva, M. C., & Barata, C. (2010). Contaminant accumulation and multi-biomarker responses in field collected zebra mussels (Dreissena polymorpha) and crayfish (Procambarus clarkii), to evaluate toxicological effects of industrial hazardous dumps in the Ebro river (NE Spain). Chemosphere, 78, 232–240.CrossRefGoogle Scholar
  20. Gambi, M. C., & Giangrande, A. (1986). Distribution of soft-bottom polychaetes in two coastal areas of the Tyrrhenian Sea (Italy): structural analysis. Estuarine, Coastal and Shelf Science, 23, 847–862.CrossRefGoogle Scholar
  21. Garcia-Orellana, J., Cañas, L., Masqué, P., Obrador, B., Olid, C., & Pretus, J. (2011). Chronological reconstruction of metal contamination in the Port of Maó (Minorca, Spain). Marine Pollution Bulletin, 62, 1632–1640.CrossRefGoogle Scholar
  22. Giangrande, A., & Gambi, M. (1985). Long term trends in the distribution of soft bottom polychaetes in the Sabaudia lagoon (Latina, Italy). Rapports de la Commission Internationale de la Mer Méditerranée, 29(4), 79–82.Google Scholar
  23. Giangrande, A., & Fraschetti, S. (1993). Life cycle, growth and secondary production in a brackish-water population of the polychaete N. latericeus (Capitellidae) in the Mediterranean Sea. Marine Ecology, 14, 313–327.CrossRefGoogle Scholar
  24. Giangrande, A., & Fraschetti, S. (1996). Effects of a short-term environmental change on a brackish-water polychaete community. Marine Ecology, 17, 321–332.CrossRefGoogle Scholar
  25. Gimeno-García, E., Andreu, V., & Boluda, R. (1996). Heavy metals in the application of inorganic fertilizers and pesticides to rice farming soils. Environmental Pollution, 92(1), 15–25.CrossRefGoogle Scholar
  26. Golterman, H. L., Sly, P. G., & Thomas, R. L. (1983). Study of the relationships between water quality and sediment transport. Technical papers in Hydrology, UNESCO, p. 231. Paris.Google Scholar
  27. Grémare, A., Sardá, R., Medernach, L., Jordana, E., Pinedo, S., Amouroux, J. M., Martin, D., Nozais, C., & Charles, F. (1998). On the dramatic increase of Ditrupa arietina O.F. Muller (Annelida: Polychaeta) along both the French and the Spanish Catalan coasts. Estuarine. Coastal and Shelf Science, 47, 447–457.CrossRefGoogle Scholar
  28. Guitart, R., Mañosa, S., & Mateo, R. (1998). El plumbisme en ocells aquàtics als països catalans: diagnosi d’una situació censurable. Butlletí de la Institució Catalana d’Història Natural, 66, 5–16.Google Scholar
  29. Ibàñez, C., Canicio, A., Day, J. W., & Curcó, A. (1997). Morphologic development, relative sea level rise and sustainable management of water and sediment in the Ebre Delta, Spain. Journal of Coastal Conservation, 3, 191–202.CrossRefGoogle Scholar
  30. Kikuchi, T. (1979). Some aspects of ecology, life cycle and taxonomy of the polychaete Capitella capitata, so called pollution indicator: a review. Benthos Research, 17(18), 33–51.CrossRefGoogle Scholar
  31. Köck, M., Farré, M., Martínez, E., Gajda-Schrantz, K., Ginebreda, A., Navarro, A., Alda, M. L. D., & Barceló, D. (2010). Integrated ecotoxicological and chemical approach for the assessment of pesticide pollution in the Ebro River delta (Spain). Journal of Hydrology, 383, 73–82.CrossRefGoogle Scholar
  32. Kolpin, D. W., Barbash, J. E., & Gilliom, R. J. (2000a). Pesticides in ground water of the United States, 1992-1996. Ground Water, 38(6), 859–863.CrossRefGoogle Scholar
  33. Kolpin, D. W., Thurman, E. M., & Linhart, S. M. (2000b). Finding minimal herbicides concentrations in ground water? Try looking for their degradates (2000). Science of the Total Environment, 248(2–3), 115–122.CrossRefGoogle Scholar
  34. Labrune, C., Grémare, A., Amouroux, J. M., Sardá, R., Gil, J., & Taboada, S. (2007). Assessment of soft-bottom polychaete assemblages in the Gulf of Lions (NW Mediterranean) based on a mesoscale survey. Estuarine, Coastal and Shelf Science, 71, 133–147.CrossRefGoogle Scholar
  35. Legendre, P., & Anderson, M. J. (1999). Erratum: distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments: (Ecological Monographs (1999) 69:1 (1-24)). Ecological Monographs, 69, 512.CrossRefGoogle Scholar
  36. Lenihan, H. S., Peterson, C. H., Kim, S. L., Conlan, K. E., Fairey, R., McDonald, C., Grabowski, J. H., & Oliver, J. S. (2003). Variation in marine benthic community composition allows discrimination of multiple stressors. Marine Ecology Progress Series, 261, 63–73.CrossRefGoogle Scholar
  37. Llagostera, I., Pérez, M., & Romero, J. (2011). Trace metal content in the seagrass Cymodocea nodosa: differential accumulation in plant organs. Aquatic Botany, 95, 124–128.CrossRefGoogle Scholar
  38. Llebot, C., Solé, J., Delgado, M., Fernández-Tejedor, M., Camp, J., & Estrada, M. (2011). Hydrographical forcing and phytoplankton variability in two semi-enclosed estuarine bays. Journal of Marine Systems, 86, 69–86.CrossRefGoogle Scholar
  39. Llebot, C., Rueda, F. J., Solé, J., Artigas, M. L., & Estrada, M. (2014). Hydrodynamic states in a wind-driven microtidal estuary (Alfacs Bay). Journal of Sea Research, 85, 263–276.CrossRefGoogle Scholar
  40. 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
  41. Maggiore, F., & Keppel, E. (2007). Biodiversity and distribution of polychaetes and molluscs along the Dese estuary (Lagoon of Venice, Italy). Hydrobiologia, 588, 189–203.CrossRefGoogle Scholar
  42. Mañosa, S., Mateo, R., & Guitart, R. (2001). A review of the effects of agricultural and industrial contamination on the Ebro delta biota and wildlife. Environmental Monitoring and Assessment, 71, 187–205.CrossRefGoogle Scholar
  43. Martin, D. (1991). Macroinfauna de una bahía mediterránea. Estudio de los niveles de organización de las poblaciones de anélidos poliquetos. PhD thesis, Universitat de Barcelona, Barcelona.Google Scholar
  44. Martin, D., & Grémare, A. (1997). Secondary production of Capitella sp. (Polychaeta: Capitellidae) inhabiting different organically enriched environments. Scientia Marina, 61, 99–109.Google Scholar
  45. Martin, D., Pinedo, S., & Sardá, R. (2000). Distribution patterns and trophic structure of soft-bottom polychaete assemblages in a north-western Mediterranean shallow-water bay. Ophelia, 53, 1–17.CrossRefGoogle Scholar
  46. Matschullat, J. (2000). Arsenic in the geosphere—a review. Science of The Total Environment, 249, 297–312.CrossRefGoogle Scholar
  47. Mayer-Pinto, M., Underwood, A. J., Tolhurst, T., & Coleman, R. A. (2010). Effects of metals on aquatic assemblages: what do we really know? Journal Experimental Marine Biology and Ecology, 39, 1–9.CrossRefGoogle Scholar
  48. McArdle, B. H., & Anderson, M. J. (2001). Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology, 82, 290–297.CrossRefGoogle Scholar
  49. McLusky, D. S., & Elliott, M. (2007). Transitional waters: a new approach, semantics or just muddying the waters? Estuarine, Coastal and Shelf Science, 71, 359–363.CrossRefGoogle Scholar
  50. Munari, C. (2013). Benthic community and biological trait composition in respect to artificial coast defence structures: a study case in the northern Adriatic Sea. Marine Environmental Research, 90, 47–54.CrossRefGoogle Scholar
  51. Munari, C., Manini, E., Pusceddu, A., Danovaro, R., & Mistri, M. (2009). Response of BITS (a benthic index based on taxonomic sufficiency) to water and sedimentary variables and comparison with other indices in three Adriatic lagoons. Marine Ecology, 30, 255–268.CrossRefGoogle Scholar
  52. Munari, C., & Mistri, M. (2010). Towards the application of the Water Framework Directive in Italy: assessing the potential of benthic tools in Adriatic coastal transitional ecosystems. Marine Pollution Bulletin, 60, 1040–1050.CrossRefGoogle Scholar
  53. Munday, B. W., & Keegan, B. F. (1992). Population dynamics of Amphiura chiajei (Echinodermata: Ophiuroidea) in Killary Harbour, on the west coast of Ireland. Marine Biology, 114, 595–605.CrossRefGoogle Scholar
  54. Muñoz, I., & Prat, N. (1989). The effects of regulation on the lower Ebro River (N.E. Spain). Regulated Rivers, 3, 345–354.CrossRefGoogle Scholar
  55. Ochoa, V., Riva, C., Faria, M., & Barata, C. (2013). Responses of B-esterase enzymes in oysters (Crassostrea gigas) transplanted to pesticide contaminated bays form the Ebro Delta (NE, Spain). Marine Pollution Bulletin, 66, 135–142.CrossRefGoogle Scholar
  56. Olla, B. L., Estelle, V. B., Swartz, R. C., Braun, G., & Studholme, A. L. (1988). Responses of polychaetes to cadmium contaminated sediment: comparison of uptake and behavior. Environmental Toxicology and Chemistry, 7, 587–592.Google Scholar
  57. Olsgard, F. (1999). Effects of copper contamination on recolonisation of subtidal marine soft sediments—an experimental field study. Marine Pollution Bulletin, 38, 448–462.CrossRefGoogle Scholar
  58. Palacín, C., Martin, D., & Gili, J. M. (1991). Features of spatial distribution of benthic infauna in a Mediterranean shallow-water bay. Marine Biology, 110, 315–321.CrossRefGoogle Scholar
  59. Palanques, A., Plana, F., & Maldonado, A. (1990). Recent influence of man on the Ebro margin sedimentation system, northwestern Mediterranean Sea. Marine Geology, 95, 247–263.CrossRefGoogle Scholar
  60. Palanques, A., Sánchez-Cabeza, J. A., Masqué, P., & León, L. (1998). Historical record of heavy metals in a highly contaminated Mediterranean deposit: the Besos prodelta. Marine Chemistry, 61, 209–217.CrossRefGoogle Scholar
  61. Palanques, A., Masqué, P., Puig, P., Sánchez-Cabeza, J. A., Frignani, M., & Alvisi, F. (2008). Anthropogenic trace metals in the sedimentary record of the Llobregat continental shelf and adjacent Foix submarine canyon (northwestern Mediterranean). Marine Geology, 248, 213–227.CrossRefGoogle Scholar
  62. Pearson, T. H., & Rosenberg, R. (1978). Macrobenthic succession in relation to organic enrichment and pollution of marine environment. Oceanography and Marine Biology: an Annual Review, 16, 229–311.Google Scholar
  63. Pérez, M., & Romero, J. (1994). Growth dynamics, production, and nutrient status of the seagrass Cymodocea nodosa in a Mediterranean semi-estuarine environment. Marine Ecology, 15, 51–64.CrossRefGoogle Scholar
  64. Pinedo, S., Sardá, R., Rey, C., & Bhaud, M. (2000). Effect of sediment particle size on recruitment of Owenia fusiformis in the Bay of Blanes (NW Mediterranean Sea): an experimental approach to explain field distribution. Marine Ecology Progress Series, 203, 205–213.CrossRefGoogle Scholar
  65. Pinedo, S., Jordana, E., Satta, M.P., Garcia, M., Torras, X., Weitzmann, B., & Ballesteros, E. (2012). Disseny, realització i suport del programa de vigilància de la qualitat de les aigües litorals de Catalunya en funció de les comunitats de macroinvertebrats que habiten els fons sedimentaris, segons la Directiva Marc de l’Aigua. Informe Tècnic. Agència Catalana de l’Aigua, Generalitat de Catalunya.Google Scholar
  66. Pinedo, S., Jordana, E., Flagella, M., & Ballesteros, E. (2014). Heavy metals contents in shallow marine sediments from Catalonia (Northwestern Mediterranean Sea). Water, Air and Soil Pollution, 225(9), 2084.CrossRefGoogle Scholar
  67. Ponti, M., Casselli, C., & Abbiati, M. (2011). Anthropogenic disturbance and spatial heterogeneity of macrobenthic invertebrate assemblages in coastal lagoons: the study case of Pialassa Baiona (northern Adriatic Sea). Helgoland Marine Research, 65, 25–42.CrossRefGoogle Scholar
  68. Prat, N., Muñoz, I., Camp, J., Comín, F. A., Lucena, J. R., Romero, J., & Vidal, M. (1988). Seasonal changes in particulate organic carbon and nitrogen in the river and drainage channels of the Ebro Delta (N.E. Spain). Verhandlungen des Internationalen Verein Limnologie, 23, 1344–1349.Google Scholar
  69. Puig, P., Palanques, A., Sánchez-Cabeza, J. A., & Masqué, P. (1999). Heavy metals in particulate matter and sediments in the southern Barcelona sedimentation system (North-western Mediterranean). Marine Chemistry, 63, 311–329.CrossRefGoogle Scholar
  70. Ranasinghe, J. A., Weisberg, S. B., Montagne, D. E., Thompson, B., Oakden, J. M., Huff, D. D., Cadien, D. B., Velarde, R. G., & Ritter, K. J. (2009). Calibration and evaluation of five indicators of benthic community condition in two California bay and estuary habitats. Marine Pollution Bulletin, 59, 5–13.CrossRefGoogle Scholar
  71. Ritter, K. J., Bay, S. M., Smith, R. W., Vidal-Dorsch, D. E., & Filed, L. J. (2011). Development and evaluation of sediments quality guidelines based on benthic macrofauna responses. Integrated Environmental Assessment and Management, 8, 610–624.CrossRefGoogle Scholar
  72. Roberts, D. A., Johnston, E. L., & Poore, A. G. B. (2008). Contamination of marine biogenic habitats and effects upon associated epifauna. Marine Pollution Bulletin, 56, 1057–1065.CrossRefGoogle Scholar
  73. Rodrigues, A. M., Meireles, S., Pereira, T., Gama, A., & Quintino, V. (2006). Spatial patterns of benthic macroinvertebrates in intertidal areas of a Southern European estuary: the Tagus, Portugal. Hydrobiologia, 555, 99–113.CrossRefGoogle Scholar
  74. Rodrigues, A. M., Quintino, V., Sampaio, L., Freitas, R., & Neves, R. (2011). Benthic biodiversity patterns in Ria de Aveiro, Western Portugal: environmental-biological relationships. Estuarine, Coastal and Shelf Science, 95, 338–348.CrossRefGoogle Scholar
  75. Rodríguez-Martín, J. A., Arias, M. L., & Grau Corbí, J. M. (2006). Heavy metals contents in agricultural topsoils in the Ebro basin (Spain). Application of the multivariate geoestatistical methods to study spatial variations. Environmental Pollution, 144, 1001–1012.CrossRefGoogle Scholar
  76. Rossi, F., Castelli, A., & Lardicci, C. (2006). Distribution of macrobenthic assemblages along a marine gradient in Mediterranean eutrophic coastal lagoons. Marine Ecology, 27, 66–75.CrossRefGoogle Scholar
  77. Ryu, J., Khim, J. S., Kang, S., Kang, D., Lee, C., & Koh, C. (2011). The impact of heavy metal gradients in sediments on benthic macrofauna at population and community levels. Environmental Pollution, 159, 2622–2629.CrossRefGoogle Scholar
  78. Sanchiz, C., García-Carrascosa, A. M., & Pastor, A. (2000). Heavy metal contents in soft-bottom marine macrophytes and sediments along the Mediterranean Coast of Spain. Marine Ecology, 21, 1–16.CrossRefGoogle Scholar
  79. Sardá, R., & Martin, D. (1993). Populations of Streblospio (Polychaeta, Spionidae) in temperate zones: demography and production. Journal of Marine Biological Association U. K., 73, 769–784.CrossRefGoogle Scholar
  80. Satta, C. T., Anglès, S., Lugliè, A., Guillén, J., Sechi, N., Camp, J., & Garcés, E. (2013). Studies on dinoflagellate cyst assemblages in two estuarine Mediterranean bays: a useful tool for the discovery and mapping of harmful algal species. Harmful Algae, 24, 65–79.CrossRefGoogle Scholar
  81. Schirosi, R., Musco, L., & Giangrande, A. (2010). Benthic assemblage of Acquatina Lake (South Adriatic Sea): present state and long-term faunistic changes. Scientia Marina, 74, 235–246.CrossRefGoogle Scholar
  82. Schuhmacher, M., Domingo, J. L., Llobet, J. M., & Corbella, J. (1993). Evaluation of the effect of temperature, pH, and bioproduction on Hg concentration in sediments, water, molluscs and algae of the delta of the Ebro River. Science of The Total Environment, 134, 117–125.CrossRefGoogle Scholar
  83. Schuhmacher, M., Batiste, J., Bosque, M. A., Domingo, J. L., & Corbella, J. (1994). Mercury concentrations in marine species from the coastal area of Tarragona Province, Spain. Dietary intake of mercury through fish and seafood consumption. Science of The Total Environment, 156, 269–273.CrossRefGoogle Scholar
  84. Schuhmacher, M., Domingo, J. L., Llobet, J. M., & Corbella, J. (1995). Variations of heavy metals in water, sediments, and biota from the delta of Ebro river, Spain. Journal of Environmental Science and Health A, 30, 1361–1372.Google Scholar
  85. Self, R. F. L., & Jumars, P. A. (1988). Cross-phyletic patterns of particle selection by deposit feeders. Journal of Marine Research, 46, 119–143.CrossRefGoogle Scholar
  86. Serrano, O., Mateo, M. A., Dueñas-Bohórquez, A., Renom, P., López-Sáez, J. A., & Martínez Cortizas, A. (2011). The Posidonia oceanica marine sedimentary record: a Holocene archive of heavy metal pollution. Science of The Total Environment, 409, 4831–4840.CrossRefGoogle Scholar
  87. Simboura, N., Nicolaidou, A., & Thessalou-Legaki, M. (2000). Polychaete communities of Greece: an ecological overview. Marine Ecology, 21, 129–144.CrossRefGoogle Scholar
  88. Suárez-Serrano, A., Alcaraz, C., Ibáñez, C., Trobajo, R., & Barata, C. (2010). Procambarus clarkii as a bioindicator of heavy metal pollution sources in the lower Ebro River and Delta. Ecotoxicology and Environmental Safety, 73, 280–286.CrossRefGoogle Scholar
  89. Tagliapietra, D., Sigovini, M., & Ghirardini, A. V. (2009). A review of terms and definitions to categorise estuaries, lagoons and associated environments. Marine and Freshwater Research, 60, 497–509.CrossRefGoogle Scholar
  90. Terrado, M., Kuster, M., Raldúa, D., Lopez De Alda, M., Barceló, D., & Tauler, R. (2007). Use of chemometric and geostatistical methods to evaluate pesticide pollution in the irrigation and drainage channels of the Ebro river delta during the rice-growing season. Analytical and Bioanalytical Chemistry, 387, 1479–1488.CrossRefGoogle Scholar
  91. Tsutsumi, H. (1990). Population persistence of Capitella sp. (Polychaeta; Capitellidae) on a mud flat subject to environmental disturbance by organic enrichment. Marine Ecology Progress Series, 63, 147–156.CrossRefGoogle Scholar
  92. Vidal, M., & Morguí, J. A. (2000). Close and delayed benthic-pelagic coupling in coastal ecosystems: the role of physical constraints. Hydrobiologia, 429, 105–113.CrossRefGoogle Scholar
  93. Wu, B., Song, J., & Li, X. (2014). Linking the toxic metals to benthic community alteration: a case study of ecological status in the Bohai Bay. Marine Pollution Bulletin, 83, 116–126.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Esther Jordana
    • 1
    Email author
  • Susana Pinedo
    • 1
  • Enric Ballesteros
    • 1
  1. 1.Centre d’Estudis Avançats de Blanes (CSIC)BlanesSpain

Personalised recommendations