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Environmental Science and Pollution Research

, Volume 21, Issue 3, pp 1680–1690 | Cite as

Temperature enhanced effects of chlorine exposure on the health status of the sentinel organism Mytilus galloprovincialis

  • Cristina López-Galindo
  • Ignacio Ruiz-Jarabo
  • Daniel Rubio
  • Enrique Nebot
  • Montserrat Solé
  • Juan M. Mancera
Research Article

Abstract

It now is widely recognised that the global temperature is rising, a phenomenon which could alter the effects of pollution on wildlife. In order to assess the role of temperature and exposure to chlorine due to cooling water discharges, a battery of metabolic, oxidative stress and histological parameters were evaluated in Mytilus galloprovincialis after 15 and 30 days at 15 °C and at two increased temperatures (+5 and +10 °C). Diverse gill pathologies such as haemolymphatic sinus dilatation, an increased number of mucocytes and granulocytes as well as a lower number of cilia were observed after 30 days exposure at higher temperatures. Protein, amino acid, triglyceride and fatty acid levels decreased when the temperature increased, as a consequence of higher energetic demand. Similarly, acetylcholinesterase, catalase and glutathione S-transferase activities showed an inhibition at higher temperatures, although gill lipid peroxidation levels remained unaffected. Our results suggest that increased temperatures induce deterioration in the health status of the mussels and in their defensive capacity against a polluted environment.

Keywords

Chlorine Mytilus galloprovincialis Gill histopathology Metabolic parameters Oxidative stress biomarkers Temperature 

Notes

Acknowledgements

The authors are grateful to power plant “Nueva Generadora del Sur” (San Roque, Cádiz, Spain) for providing their facilities and help and to Agustin Santos Alvarez for his valuable laboratory support. This research work was funded by grant CTM2009-09527 and CSD2007-0055 to E.N.

References

  1. Akaishi FM, St-Jean SD, Bishay F, Clarke J, Rabitto IS, Oliveira Ribeiro CA (2007) Immunological responses, histopathological finding and disease resistance of blue mussel (Mytilus edulis) exposed to treated and untreated municipal wastewater. Aquat Toxicol 82:1–14CrossRefGoogle Scholar
  2. Bebianno MJ, Lopes B, Guerra L, Hoarau P, Ferreira AM (2007) Glutathione S-transferases and cytochrome P450 activities in Mytilus galloprovincialis from the South coast of Portugal: effect of abiotic factors. Environ Int 33:550–558CrossRefGoogle Scholar
  3. Bocchetti R, Fattorini D, Pisanelli B, Macchia S, Oliviero L, Pilato F, Pellegrini D, Regoli F (2008) Contaminant accumulation and biomarker responses in caged mussels, Mytilus galloprovincialis, to evaluate bioavailability and toxicological effects of remobilized chemicals during dredging and disposal operations in harbour areas. Aquat Toxicol 89:257–266CrossRefGoogle Scholar
  4. Borković SS, Šaponjić JS, Pavlović SZ, Blagojević DP, Milošević SM, Kovačević TB, Radojičić RM, Spasić MB, Žikić RV, Saičić ZS (2005) The activity of antioxidant defenses enzymes in the mussel Mytilus galloprovincialis from the Adriatic Sea. Comp Biochem Physiol, Part C: Pharmacol Toxicol Endocrinol 141:366–374CrossRefGoogle Scholar
  5. Cajaraville MP, Bebiano MJ, Blasco J, Porte C, Sarasquete C, Viarengo A (2000) The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a practical approach. Sci Total Environ 247:295–311CrossRefGoogle Scholar
  6. Characklis WG (1991) Biofouling: effects and control. In: Flemming HC, Geesey GG (eds) Biofouling and biocorrosion in industrial water systems. Springer, Berlin–Heidelberg, pp pp 7–27CrossRefGoogle Scholar
  7. Coles JA, Fairly SR, Pipe RK (1994) The effects of fluoranthene on the immunocompetence of the common marine mussel Mytilus edulis. Aquat Toxicol 30:367–379CrossRefGoogle Scholar
  8. Cooke SJ, Schreer JF (2001) Additive effects of chlorinated biocides and water temperature on fish in thermal effluents with emphasis on the Great Lakes. Rev Fish Sci 9(2):69–113CrossRefGoogle Scholar
  9. Davies MS, Hawkins J (1998) Mucus from marine molluscs. Adv Mar Biol 34:1–71CrossRefGoogle Scholar
  10. Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008 establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive).Google Scholar
  11. Engel RH, Neat MJ, Hillman RE (1970) Sublethal chronic effects of DDT and Lindane on glycolytic and gluconeogenic enzymes of the quahog, Mercenaria mercenaria. FAO technical conference on marine pollution and its effects on living resources and fishing. In: Ruivo M, Sahrhage D, Andren L, Angelescu V, Tomczak G (ed) Marine pollution and sea life. Fishing News (Books), London, pp 257–259.Google Scholar
  12. Erk M, Ivanković D, Želijka S (2011) Cellular energy allocation in mussels (Mytilus galloprovincialis) from the stratified estuary as a physiological biomarker. Mar Pollut Bull 62:1124–1129CrossRefGoogle Scholar
  13. Escartín E, Porte C (1997) The use of cholinesterase and carboxylesterase activities from Mytilus galloprovincialis in pollution monitoring. Environ Toxicol Chem 16:2090–2095Google Scholar
  14. Giarratano E, Duarte CA, Amin OA (2010) Biomarkers and heavy metal bioaccumulation in mussels trasplanted to coastal waters of the Beagle Channel. Ecotoxicol Environ Saf 73:270–279CrossRefGoogle Scholar
  15. Giarratano E, Gil MN, Malanga G (2011) Seasonal and pollution-induced variations in biomarkers of transplanted mussels within the Beagle Channel. Mar Pollut Bull 62:1337–344CrossRefGoogle Scholar
  16. Grasso D (ed.) (1996) Wastewater disinfection. Manual of practice FD-10. Water Environment Federation, Alexandria.Google Scholar
  17. ICES (2007) Report of the Working Group on Biological Effects of Contaminants (WGBEC), Alessandria, Italy, 19–23 Mar 2007, CM 2007/MHC:03.129 ppGoogle Scholar
  18. IPCC (2007) In: Core Writing Team, Pachauri RK, Reisinger A (eds) Climate change 2007: synthesis report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, p 104 ppGoogle Scholar
  19. Jenner HA, Taylor CJL, Van Donk M, Khalanski M (1997) Chlorination by-products in chlorinated cooling water of some European coastal power stations. Mar Environ Res 43:279–293CrossRefGoogle Scholar
  20. Keppler D, Decker K (1974) Glycogen determination with amyloglucosidase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic, New York, pp 1127–1131Google Scholar
  21. Leiniö S, Lehtonen KK (2005) Seasonal variability in biomarkers in the bivalves Mytilus edulis and Macoma balthica from the northern Baltic Sea. Comp Biochem Physiol, Part C: Pharmacol Toxicol Endocrinol 140:408–421Google Scholar
  22. Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42:656–666CrossRefGoogle Scholar
  23. López-Galindo C, Vargas-Chacoff L, Nebot E, Casanueva JF, Rubio D, Solé M, Mancera JM (2010a) Biomarker responses in Solea senegalensis exposed to sodium hypochlorite used as antifouling. Chemosphere 78:885–893CrossRefGoogle Scholar
  24. López-Galindo C, Vargas-Chacoff L, Nebot E, Casanueva JF, Rubio D, Mancera JM, Solé M (2010b) Sublethal responses of the common mussel (Mytilus galloprovincialis) exposed to the antifouling compounds, sodium hypochlorite and Mexel®432. Ecotoxicol Environ Saf 73:825–834CrossRefGoogle Scholar
  25. McManus JFA (1948) Histological and histochemical uses of periodic acid. Biotech Histochem 23:99–108.Google Scholar
  26. Manduzio H, Monsinjon T, Galap C, Leboulenger F, Rocher B (2004) Seasonal variations in antioxidant defences in blue mussels Mytilus edulis collected from a polluted area: major contributions in gills of an inducible isoform of Cu/Zn-superoxide dismutase and of glutathione S-transferase. Aquat Toxicol 70:83–93CrossRefGoogle Scholar
  27. Moore S (1968) Amino acid analysis: aqueous dimethyl sulfoxide as solvent for the ninhydrin reaction. J Biol Chem 243(23):6281–6283Google Scholar
  28. Noyes PM, McElwee MK, Miller HD, Clark BW, Van Tiem LA, Walcott KC, Erwwin KN, Levin ED (2009) The toxicology of climate change: environmental contaminants in a warming world. Environ Int 35:971–986CrossRefGoogle Scholar
  29. Oliveira David JA, Salaroli RB, Fontanetti CS (2008) Fine structure of Mytella falcata (Bivalvia) gill filaments. Micron 39:329–336CrossRefGoogle Scholar
  30. Parry HE, Pipe RK (2004) Interactive effects of temperature and copper on immunocompetence and disease susceptibility in mussels (Mytilus edulis). Aquat Toxicol 69:311–325CrossRefGoogle Scholar
  31. Pfeifer S, Schiedek D, Dippner JW (2005) Effect of temperature and salinity on acetylcholinesterase activity, a common pollution biomarker, in Mytilus sp. from the south-western Baltic Sea. J Exp Mar Biol Ecol 320:93–103CrossRefGoogle Scholar
  32. Porte C, Solé M, Borghi V, Martinez M, Chamorro J, Torreblanca A, Ortiz M, Orbea A, Soto M, Cajaraville MP (2001) Chemical, biochemical and cellular responses in the digestive gland of mussel Mytilus galloprovincialis from the Spanish Mediterranean coast. Biomarkers 6:335–350CrossRefGoogle Scholar
  33. Power A, Sheehan D (1996) Seasonal variation in the antioxidant defence systems of gill and digestive gland of the blue mussel, Mytilus edulis. Comp Biochem Physiol, Part C: Pharmacol Toxicol Endocrinol 114:99–103Google Scholar
  34. Roméo M, Hoarau P, Garello G, Gnassia-Barelli M, Girard JP (2003) Mussel transplantation and biomarkers as useful tools for assessing water quality in the NW Mediterranean. Environ Pollut 122:369–378CrossRefGoogle Scholar
  35. Schiedek D, Bagdonas E, Balk L, Baršiene J, Broeg K, Gercken J, Koehler A, Lehtonen KK, Pfeifer S, Šyvokiene J, Schneider R (2003) Biomarker responses in the blue mussel (Mytilus edulis) and in eelpout (Zoarces viviparus) in the Western Baltic Sea. CM-International Council for the Exploration of the Sea 2003/M:07, 1–17.Google Scholar
  36. Soldatov AA, Gostyukhina OL, Golovina IV (2007) Antioxidant enzyme complex of tissues of the bivalve Mytilus galloprovincialis Lam. under normal and oxidative-stress conditions: a review. Appl Biochem Micro 43:556–562CrossRefGoogle Scholar
  37. Sunila I (1986) Chronic histopathological effects of short-term copper and cadmium exposure on the gill of the mussel, Mytilus edulis. J Invertebr Pathol 47:125–142CrossRefGoogle Scholar
  38. Taylor CJL (2006) The effects of biological fouling control at coastal and estuarine power stations. Mar Poll Bull 53:30–48CrossRefGoogle Scholar
  39. Vargas-Chacoff L, Arjona FJ, Polakof S, Martin del Río MP, Soengas JL, Mancera JM (2009) Interactive effects of environmental salinity and temperature on metabolic responses of gilthead sea bream Sparus aurata. Comp Biochem Physiol, Part A: Mol Integr Physiol 154:417–424CrossRefGoogle Scholar
  40. Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149CrossRefGoogle Scholar
  41. Verma AK, Pal AK, Manush SM, Das T, Dalvi RS, Chandrachoodan PP, Ravi PM, Apte SK (2007) Persistent sub-lethal chlorine exposure elicits the temperature induced stress responses in Cyprinus carpio early fingerlings. Pestic Biochem Physiol 87:229–237CrossRefGoogle Scholar
  42. Viarengo A, Canesi L (1991) Mussels as biological indicators of pollution. Aquaculture 94:225–243CrossRefGoogle Scholar
  43. Viarengo A, Lowe D, Bolognesi C, Fabbri E, Koehler A (2007) The use of biomarkers in biomonitoring: a 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Comp Biochem Physiol, Part C: Pharmacol Toxicol Endocrinol 146:281–300Google Scholar
  44. Zandee DI, Kluytmans JH, Zurburg W (1980) Seasonal variations in biochemical composition of Mytilus edulis with reference to energy metabolism and gametogenesis. Neth J Sea Res 14:1–29CrossRefGoogle Scholar
  45. Zwaan A, Wijsman TCM (1976) Anaerobic metabolism in bivalvia (Mollusca) characteristic of anaerobic metabolism. Comp Biochem Physiol, Part B: Biochem Mol Biol 54:313–324CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Cristina López-Galindo
    • 1
  • Ignacio Ruiz-Jarabo
    • 2
  • Daniel Rubio
    • 1
  • Enrique Nebot
    • 1
  • Montserrat Solé
    • 3
  • Juan M. Mancera
    • 2
  1. 1.Departamento de Tecnologías del Medio Ambiente, Centro Andaluz de Ciencia y Tecnología Marina (CACYTMAR)Universidad de CádizCadizSpain
  2. 2.Departamento de Biología, Facultad de Ciencias del Mar y AmbientalesUniversidad de CádizCadizSpain
  3. 3.Institut de Ciencies del MarICM-CSICBarcelonaSpain

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