Ecotoxicology

, Volume 22, Issue 6, pp 996–1011 | Cite as

Integrated ecotoxicological assessment of marine sediments affected by land-based marine fish farm effluents: physicochemical, acute toxicity and benthic community analyses

  • C. Silva
  • E. Yáñez
  • M. L. Martín-Díaz
  • I. Riba
  • T. A. DelValls
Article

Abstract

An integrated ecotoxicological assessment of marine sediments affected by land-based marine fish farm effluents was developed using physicochemical and benthic community structure analyses and standardised laboratory bioassays with bacteria (Vibrio fischeri), amphipods (Ampelisca brevicornis) and sea urchin larvae (Paracentrotus lividus). Intertidal sediment samples were collected at five sites of the Rio San Pedro (RSP) creek, from the aquaculture effluent to a clean site. The effective concentration (EC50) from bacterial bioluminescence and A. brevicornis survival on whole sediments and P. lividus larval developmental success on sediment elutriates were assessed. Numbers of species, abundance and Shannon diversity were the biodiversity indicators measured in benthic fauna of sediment samples. In parallel, redox potential, pH, organic matter and metal levels (Cd, Cu, Ni, Pb and Zn) in the sediment and dissolved oxygen in the interstitial water were measured in situ. Water and sediment physicochemical analysis revealed the exhibition of a spatial gradient in the RSP, evidenced by hypoxia/anoxia, reduced and acidic conditions, high organic enrichment and metal concentrations at the most contaminated sites. Whereas, the benthic fauna biodiversity decreased the bioassays depicted decreases in EC50, A. brevicornis survival, P. lividus larval success at sampling sites closer to the studied fish farms. This study demonstrates that the sediments polluted by fish farm effluents may lead to alterations of the biodiversity of the exposed organisms.

Keywords

Sediment organic enrichment Microtox Amphipod survival Sea urchin larval development Benthic fauna Aquaculture effluents 

References

  1. Alvarez-Guerra M, Viguri JR, Voulvoulis N (2009) A multicriteria-based methodology for site prioritisation in sediment management. Environ Int 35:920–930CrossRefGoogle Scholar
  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust J Ecol 26:32–46Google Scholar
  3. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: guide to software and statistical methods. PRIMER-E, PlymouthGoogle Scholar
  4. Antunes P, Gil O (2004) PCB and DDT contamination in cultivated and wild sea bass from Ria de Aveiro, Portugal. Chemosphere 54(10):1503–1507CrossRefGoogle Scholar
  5. Araújo CVM, Diz FR, Laiz I, Lubián LM, Blasco J, Moreno- Garrido I (2009) Sediment integrative assessment of the Bay of Cádiz (Spain): an ecotoxicological and chemical approach. Environ Int 35(6):831–841CrossRefGoogle Scholar
  6. Azur Environmental (1998) Microtox acute toxicity basic test procedures. Azur Environmental, Carlsbad, CAGoogle Scholar
  7. Beiras R (2002) Comparison of methods to obtain a liquid phase in marine sediment toxicity bioassays with Paracentrotus lividus sea urchin embryos. Arch Environ Contam Toxicol 42:23–28CrossRefGoogle Scholar
  8. Beiras R, Fernández N, Bellas J, Besada V, González-Quijano A, Nunes T (2003) Integrative assessment of marine pollution in Galician estuaries using sediment chemistry, mussel bioaccumulation, and embryo-larval toxicity bioassays. Chemosphere 52:1209–1224CrossRefGoogle Scholar
  9. Blasco J, Gomes T, García-Barrera T, Rodriguez-Romero A, González-Rey M, Morán-Roldán F, Trombini C, Miotk M, Gómez-Ariza JL, Bebianno M (2010) Trace metal concentrations in sediments from the southwest of the Iberian Peninsula. Sci Mar 74S1:99–106CrossRefGoogle Scholar
  10. 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. Mar Poll Bull 40:1100–1114CrossRefGoogle Scholar
  11. Brooks KM, Mahnken C, Nash C (2002) Environmental effects associated with marine net pen waste with emphasis on salmon farming in the Pacific Northwest. In: Stickney RR, McVey JP (eds) Responsible marine aquaculture. World aquaculture society. CABI Publishing, Wallingford, p 391Google Scholar
  12. Cabello FC (2006) Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol 8(7):1137–1144CrossRefGoogle Scholar
  13. Carballeira C, De Orte MR, VianaI IG, Carballeira A (2011a) Implementation of a minimal biological test set for assessment of ecotoxic effect of effluents from land-based fish farms. Ecotox Environ Safe 78:148–161CrossRefGoogle Scholar
  14. Carballeira C, Martín-Díaz L, DelValls TA (2011b) Influence of salinity on fertilization and larval development toxicity tests with two species of sea urchin. Mar Environ Res 72:196–203CrossRefGoogle Scholar
  15. Carballeira C, Ramos-Gómez J, Martín-Díaz L, DelValls TA (2012) Identification of specific malformations of sea urchin larvae for toxicity assessment: application to marine pisciculture effluents. Mar Environ Res 77:12–22CrossRefGoogle Scholar
  16. Casado-Martínez MC, Campisi T, Díaz A, Lo Re R, Obispo R, Postma JF, Riba I, Sneekes AC, Buceta JL, DelValls TA (2006a) Interlaboratory assessment of marine bioassays to evaluate the environmental quality of coastal sediments in Spain. II. Bioluminescence inhibition test for rapid sediment toxicity assessment. Cienc Mar 32:129–138Google Scholar
  17. Casado-Martínez MC, Beiras R, Belzunce MJ, González-Castromil MA, Marin-Guirao L, Postma JF, Riba I, DelValls TA (2006b) Interlaboratory assessment of marine bioassays to evaluate the environmental quality of coastal sediments in Spain. IV. Whole sediment toxicity test using crustacean amphipods. Cienc Mar 32:149–157Google Scholar
  18. Casado-Martínez MC, Fernández N, Lloret J, Marín A, Martínez-Gómez C, Riba I, Beiras R, Saco-Álvarez L, DelValls TA (2006c) Interlaboratory assessment of marine bioassays to evaluate the environmental quality of coastal sediments in Spain. III. Bioassay using embryos of the sea urchin Paracentrotus lividus. Cienc Mar 32:139–147Google Scholar
  19. Cesar A, Marín A, Marín-Guirao L, Vita R (2004) Amphipod and sea urchin tests to assess the toxicity of Mediterranean sediments: the case of Portman Bay. Sci Mar 68:205–213CrossRefGoogle Scholar
  20. Cesar A, Marín A, Marin-Guirao L, Vita R, Lloret J, DelValls TA (2009) Integrative ecotoxicological assessment of sediment in Portmán Bay (southeast Spain). Ecotox Environ Safe 72:1832–1841CrossRefGoogle Scholar
  21. Chapman PM (1996) Presentation and interpretation of sediment quality triad data. Ecotoxicology 5:327–339CrossRefGoogle Scholar
  22. Chapman PM (2007) Determining when contamination is pollution — weight of evidence determinations for sediments and effluents. Environ Int 33(4):492–501CrossRefGoogle Scholar
  23. Chapman PM, Hollert H (2006) Should the sediment quality triad become a tetrad, a pentad, or possibly even a hexad? J Soils Sediments 6(1):4–8CrossRefGoogle Scholar
  24. Chapman PM, McDonald BG, Lawrence GS (2002) Weight of evidence frameworks for sediment quality and other assessments. Hum Ecol Risk Assess 8:1489–1515CrossRefGoogle Scholar
  25. Choueri RB, Cesar A, Abessa DMS, Torres RJ, Morais RD, Riba I, Pereira CDS, Nascimento MRL, Mozeto A, DelValls TA (2009) Development of site-specific sediment quality guidelines for North and South Atlantic littoral zones: comparison against national and international sediment quality benchmarks. J Hazard Mat 170:320–331CrossRefGoogle Scholar
  26. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E Ltd. Plymouth Marine Laboratory, PlymouthGoogle Scholar
  27. Comreys AL (1973) A first course in factor analysis. Academic, New YorkGoogle Scholar
  28. De la Paz M, Gómez-Parra A, Forja JM (2008a) Variability of the partial pressure of CO2 on a daily-to-seasonal time scale in a shallow coastal system affected by intensive aquaculture activities (Bay of Cadiz, SW Iberian Peninsula). Mar Chem 110:195–204CrossRefGoogle Scholar
  29. De la Paz M, Gómez-Parra A, Forja JM (2008b) Tidal-to-seasonal variability in the parameters of the carbonate system in a shallow tidal creek influenced by anthropogenic inputs, Río San Pedro (SW Iberian Peninsula). Cont Shelf Res 28:1394–1404CrossRefGoogle Scholar
  30. DelValls TA, Forja JM, González-Mazo E, Gómez-Parra A (1998a) Determining contamination sources in marine sediments using multivariate analysis. Trends Anal Chem 17(4):181–192CrossRefGoogle Scholar
  31. DelValls TA, Conradi M, García-Adiego E, Forja JM, Gómez-Parra A (1998b) Analysis of macrobenthic community structure in relation to different environmental sources of contamination in two littoral ecosystems from the Gulf of Cádiz (SW Spain). Hydrobiologia 385:59–70CrossRefGoogle Scholar
  32. DelValls TA, Forja JM, Gómez-Parra A (1999) An integrative study of environmental quality of sediments from the Bay of Cadiz. Ecotoxicol Environ Res 2:26–33Google Scholar
  33. DelValls TA, Andres A, Belzunce MJ, Buceta JL, Casado-Martinez MC, Castro R, Riba I, Viguri JR, Blasco J (2004) Chemical and ecotoxicological guidelines for managing disposal of dredged material. Trends Anal Chem 23:819–828CrossRefGoogle Scholar
  34. Environment Canada (1992a) Biological test method: acute test for sediment toxicity using marine or estuarine amphipods. Environmental Protection Service, Ottawa, ON, Report EPS 1/RM/26, p 111Google Scholar
  35. Environment Canada (1992b) Biological test method: fertilization assay using echinoids (sea urchins and sand dollars). Environmental Protection Service, Ottawa, ON, Report EPS 1/RM/27, p 97Google Scholar
  36. Environment Canada (2002) Biological test method: reference method for determining the toxicity of sediment using luminescent bacteria in a solid-phase test. Environmental Protection Service, Ottawa, ON, Report EPS 1/RM/42, p 83Google Scholar
  37. Ferrón S, Ortega T, Forja JM (2009) Benthic fluxes in a tidal salt marsh creek affected by fish farm activities: Río San Pedro (Bay of Cadiz, SW Spain). Mar Chem 113:50–62CrossRefGoogle Scholar
  38. França S, Vinagre C, Pardal MA, Cabral HN (2009) Spatial and temporal patterns of benthic invertebrates in the Tagus estuary (Portugal): comparison between subtidal and intertidal mudflat. Sci Mar 73:307–318CrossRefGoogle Scholar
  39. Heilskov AC, Alperin M, Holmer M (2006) Benthic fauna bio-irrigation effects on nutrient regeneration in fish farm sediments. J Exp Mar Biol Ecol 339:204–225CrossRefGoogle Scholar
  40. Hernando MD, De Vettori S, Martínez Bueno MJ, Fernández-Alba AR (2007) Toxicity evaluation with Vibrio fischeri test of organic chemicals used in aquaculture. Chemosphere 68:724–730CrossRefGoogle Scholar
  41. Holmer M (2010) Environmental issues of fish farming in offshore waters: perspectives, concerns and research needs. Aquac Environ Interact 1:57–70CrossRefGoogle Scholar
  42. Holmer M, Wildish D, Hargrave BT (2005) Organic enrichment from marine finfish aquaculture and effects on sediment biogeochemical processes. In: Hargrave BT (ed) Environmental effects of marine finfish aquaculture. Springer, Berlin, pp 181–206CrossRefGoogle Scholar
  43. Isidori M, Lavorgna M, Nardelli A, Pascarella L, Parrella A (2005) Toxic and genotoxic evaluation of six antibiotics on non-target organisms. Sci Total Environ 346:87–98CrossRefGoogle Scholar
  44. ISO11466 (1995) Soil quality—extraction of trace elements soluble in aqua regia. International Organization for Standardization, SwitzerlandGoogle Scholar
  45. Kalantzi I, Karakassis I (2006) Benthic impacts of fish farming: meta-analysis of community and geochemical data. Mar Pollut Bull 52:479–483CrossRefGoogle Scholar
  46. Karakassis I, Tsapakis M, Smith CJ, Rumohr H (2002) Fish farming impacts in the Mediterranean studied through sediment profiling imagery. Mar Ecol Prog Series 227:125–133CrossRefGoogle Scholar
  47. Lalumera GM, Calamari D, Galli P, Castiglioni S, Crosa G, Fanelli R (2004) Preliminary investigation on the environmental occurrence and effects of antibiotics used in aquaculture in Italy. Chemosphere 54:661–668CrossRefGoogle Scholar
  48. Long ER, Morgan LG (1990) The potential for biological effects of sediment-sorbed contaminants tested in the National Status and Trends Program. National Oceanic and Atmospheric Administration Technical Memorandum NOS OMA 52, USA, p 175Google Scholar
  49. Macken A, Giltrap M, Foley B, McGovern E, McHugh B, Davoren M (2008) An integrated approach to the toxicity assessment of Irish marine sediments: validation of established marine bioassays for the monitoring of Irish marine sediments. Environ Int 34(7):1023–1032CrossRefGoogle Scholar
  50. Macleod CK, Crawford CM, Moltschaniwskyj NA (2004) Assessment of long term change in sediment condition after organic enrichment: defining recovery. Mar Pollut Bull 49:79–88CrossRefGoogle Scholar
  51. Mantzavrakos E, Kornaros M, Lyberatos G, Kaspiris P (2007) Impacts of a marine fish farm in Argolikos Gulf (Greece) on the water column and the sediment. Desalination 210:110–124CrossRefGoogle Scholar
  52. Marín A, Montoya S, Vita R, Marín-Guirao L, Lloret J, Aguado F (2007) Utility of sea urchin embryo-larval bioassays for assessing the environmental impact of marine fish cage farming. Aquaculture 271:286–297CrossRefGoogle Scholar
  53. Martín-Díaz ML, Blasco J, Sales D, DelValls A (2008) Field validation of a battery of biomarkers to assess sediment quality in Spanish ports. Environ Pollut 20:1–10Google Scholar
  54. McPherson C, Chapman PM, deBruyn AMH, Cooper L (2008) The importance of benthos in weight of evidence sediment assessments—a case study. Sci Total Environ 394(2–3):252–264CrossRefGoogle Scholar
  55. Mendiguchía C, Moreno C, Mánuel-Vez MP, García-Vargas M (2006) Preliminary investigation on the enrichment of heavy metals in marine sediments originated from intensive aquaculture effluents. Aquaculture 254:317–325CrossRefGoogle Scholar
  56. Montero N, Belzunce-Segarra MJ, Del Campo A, Garmendia JM, Ferrer L, Larreta J (2011) Integrative environmental assessment of the impact of Pasaia harbour activities on the Oiartzun estuary (southeastern Bay of Biscay). J Mar Syst (in press). doi:10.1016/j.jmarsys.2011.06.002
  57. Morales-Caselles C, Kalman J, Riba I, DelValls TA (2007) Comparing sediment quality in Spanish littoral areas affected by acute (Prestige, 2002) and chronic (Bay Of Algeciras) oil spills. Environ Pollut 146:233–240CrossRefGoogle Scholar
  58. 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. Mar Poll Bull 55:16–29CrossRefGoogle Scholar
  59. Ocaña-Martín A, Sanchez-Tocino LL, López-González S, Viciana JF (2000) Guía Submarina de invertebrados no artrópodos, 2nd edn. Granada, Comares, p 512Google Scholar
  60. Papageorgiou N, Sigala K, Karakassis I (2009) Changes of macrofaunal functional composition at sedimentary habitats in the vicinity of fish farms. Estuar Coast Shelf Sci 83:561–568CrossRefGoogle Scholar
  61. Pearson TH, Black KD (2001) The environmental impacts of marine fish cage culture. In: Black KD (ed) Environmental impacts of aquaculture. Academic, Sheffield, pp 1–27Google Scholar
  62. Pearson TH, Rosemberg R (1978) Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanogr Mar Biol 16:229–311Google Scholar
  63. Pérez E, Blasco J, Solé M (2004) Biomarker responses to pollution in two invertebrate species: Scrobicularia plana and Nereis diversicolor from the Cadiz bay. Mar Environ Res 58:275–279CrossRefGoogle Scholar
  64. Peters C, Becker S, Noack U, Pfitzner S, Bülow W, Barz K, Ahlf W, Berghahn R (2002) A marine bioassay test set to assess marine water and sediment quality-its need, the approach and first results. Ecotoxicology 11:379–383CrossRefGoogle Scholar
  65. Pusceddu A, Fraschetti S, Mirto S, Holmer M, Danovaro R (2007) Effects of intensive mariculture on sediment biochemistry. Ecol Appl 17:1366–1378CrossRefGoogle Scholar
  66. Ramos-Gómez J, Martín-Díaz ML, DelValls TA (2009) Acute toxicity measured in the amphipod Ampelisca brevicornis after exposure to contaminated sediments from Spanish littoral. Ecotoxicology 18:1068–1076CrossRefGoogle Scholar
  67. Read P, Fernandes T (2003) Management of environmental impacts of marine aquaculture in Europe. Aquaculture 226:139–163CrossRefGoogle Scholar
  68. Riba I, DelValls TA, Forja JM, Gómez-Parra A (2003) Comparative toxicity of contaminated sediment from a mining spill using two amphipods species: Corophium volutator (Pallas, 1776) and Ampelisca brevicornis (A. Costa, 1853). Bull Environ Contam Toxicol 71:1061–1068CrossRefGoogle Scholar
  69. Riba I, Casado-Martínez C, Forja JM, DelValls TA (2004) Sediment quality in the Atlantic coast of Spain. Environ Toxicol Chem 23(2):271–282CrossRefGoogle Scholar
  70. Riedl R (1986) Fauna y flora del mar Mediterráneo. Omega, Barcelona, p 858Google Scholar
  71. Rodrigues AM, 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 555:99–113CrossRefGoogle Scholar
  72. Sapkota A, Sapkota AR, Kucharski M, Burke J, McKenzie S, Walker P, Lawrence R (2008) Aquaculture practices and potential human health risks: current knowledge and future priorities. Environ Int 34:1215–1226CrossRefGoogle Scholar
  73. SEPA (2005) Scottish Environment Protection Agency. Regulation and monitoring of marine cage fish farming in Scotland. A manual of Procedures. Standard Monitoring Survey. Version 1.6. http://www.sepa.org.uk/guidance/fishfarmmanual/manual.asp
  74. Shannon CE, Weaver W (1949) The mathematical theory of communication. The University of Illinois Press, UrbanaGoogle Scholar
  75. Solan M, Cardinale BJ, Dowing AL, Engelhardt KAM, Ruesink JL, Srivastava DS (2004) Extinction and ecosystem function in the marine benthos. Science 306:1177–1180CrossRefGoogle Scholar
  76. Solé M, Kopecka-Pilarczyk J, Blasco J (2009) Pollution biomarkers in two estuarine invertebrates, Nereis diversicolor and Scrobicularia plana, from a Marsh ecosystem in SW Spain. Environ Int 35:523–531CrossRefGoogle Scholar
  77. Tello A, Corner RA, Telfer TC (2010) How do land-based salmonid farms affect stream ecology? Environ Pollut 158:1147–1158CrossRefGoogle Scholar
  78. Thorson G (1957) Bottom communities (sublittoral or shallow shelf). In: de Hedgpeth JH (ed) Treatise on marine ecology and paleoecology, vol 1. Ecology Mem Geol Soc Am 67:461–534Google Scholar
  79. Tomassetti P, Porrello S (2005) Polychaetes as indicators of marine fish farm organic enrichment. Aquac Int 13:109–128CrossRefGoogle Scholar
  80. Tomassetti P, Persia E, Mercatali I, Vani D, Marussso V, Porrello S (2009) Effects of mariculture on macrobenthic assemblages in a western mediterranean site. Mar Pollut Bull 58:533–541CrossRefGoogle Scholar
  81. Tovar A, Moreno C, Mánuel-vez MP, García-Vargas M (2000a) Environmental impacts of intensive aquaculture in marine waters. Water Res 34:334–342CrossRefGoogle Scholar
  82. Tovar A, Moreno C, Mánuel-vez MP, García-Vargas M (2000b) Environmental implications of intensive marine aquaculture in earthen ponds. Mar Pollut Bull 40:981–988CrossRefGoogle Scholar
  83. US, EPA (United States Environmental Protection Agency) (1994) Methods for assessing the toxicity of sediment-associated contaminants with estuarine and marine amphipods (EPA/600/R-94/025). Office of Water, WashingtonGoogle Scholar
  84. Usero J, Morillo J, El Bakouri H (2008) A general integrated ecotoxicological method for marine sediment quality assessment: application to sediments from littoral ecosystems on Southern Spain’s Atlantic coast. Mar Pollut Bull 56:2027–2036CrossRefGoogle Scholar
  85. Vezzulli L, Moreno M, Marin V, Pezzati E, Bartoli M, Fabiano M (2008) Organic waste impact of captured-based Atlantic bluefin tuna aquaculture at an exposed site in the Mediterranean Sea. Estuar Coast Shelf Sci 78:369–384CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • C. Silva
    • 1
    • 2
    • 3
  • E. Yáñez
    • 3
  • M. L. Martín-Díaz
    • 1
    • 2
  • I. Riba
    • 1
  • T. A. DelValls
    • 1
  1. 1.UNITWIN/UNESCO/WiCoP, Physical Chemical Department, Campus de Excelencia Internacional del Mar (CEIMAR)University of CádizCádizSpain
  2. 2.Andalusian Center of Marine Science and Technology (CACYTMAR), CEIMARUniversity of CádizCádizSpain
  3. 3.School of Marine SciencePontificia Universidad Católica de ValparaísoValparaísoChile

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