Risks of seawater ozonation in recirculation aquaculture - Effects of oxidative stress on animal welfare of juvenile turbot (Psetta maxima, L.)

Aquatic Toxicology

Volumn 105, Issue 3-4, 2011, Pages 508-517

  Reiser, S ^a,b   Wuertz, S ^b,c   Schroeder, J P ^a,c   Kloas, W ^b,d   Hanel, R ^a,e  

^a GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

^b LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

^c Gesellschaft fuer Marine Aquakultur ^*  (Germany)

^d HUMBOLDT UNIVERSITY   (Germany)

^e INSTITUT FÜR SEEFISCHEREI   (Germany)

Author keywords

GST; Heat shock protein; Histology; HSP70; HSP90; Oxidative stress; Ozone; RAS; Turbot

Indexed keywords

BETA 2 MICROGLOBULIN; GLUTATHIONE TRANSFERASE; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; MESSENGER RNA; OZONE; SEA WATER;

BIOACCUMULATION; BIOMARKER; CONCENTRATION (COMPOSITION); DISINFECTION; FISH; GENE EXPRESSION; HISTOPATHOLOGY; JUVENILE; OXIDATION; OZONE; RECIRCULATING SYSTEM; RISK ASSESSMENT; RNA; SEAWATER; SUBLETHAL EFFECT; TOXICITY; WATER CHEMISTRY; WATER TREATMENT;

ANIMAL WELFARE; AQUACULTURE; ARTICLE; CONTROLLED STUDY; GILL; HISTOPATHOLOGY; HOUSEKEEPING GENE; HYPERPLASIA; HYPERTROPHY; LIVER; NECROSIS; NONHUMAN; OXIDATIVE STRESS; OZONATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSETTA MAXIMA; RISK FACTOR; SALINITY; TISSUE INJURY; TURBOT; WATER QUALITY;

ANIMALS; AQUACULTURE; BIOLOGICAL MARKERS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENTAL EXPOSURE; FLATFISHES; GILLS; GLUTATHIONE TRANSFERASE; HSP70 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; LIVER; OXIDANTS, PHOTOCHEMICAL; OXIDATIVE STRESS; OZONE; RANDOM ALLOCATION; REAL-TIME POLYMERASE CHAIN REACTION; SEAWATER; TOXICITY TESTS, CHRONIC;

ANIMALIA; SCOPHTHALMIDAE; SCOPHTHALMUS MAXIMUS;

EID: 80052541467     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2011.08.004     Document Type: Article

References (77)

1. American Public Health Association Standard Methods for the Examination of Water and Wastewater 1989, American Public Health Association, Washington, DC, USA, 1624pp. 17th ed.
2. Barton B.A., Morgan J.D., Vijayan M.M. Physiological and condition-related indicators of environmental stress in fish. Biological Indicators of Aquatic Ecosystem Stress 2002, 111-148. American Fisheries Society, Bethesda, USA. A.S. Marshall (Ed.).
3. Basu N., Todgham A.E., Ackerman P.A., Bibeau M.R., Nakano K., Schulte P.M., Iwama G.K. Heat shock protein genes and their functional significance in fish. Gene 2002, 295:173-183.
4. Block R.M., Burton D.T., Gullans S.R., Richardson L.B. Respiratory and osmoregulatory responses of white perch (Morone americana) exposed to chlo and ozone in estuarine waters. Water Chlorination: Environmental Impact and Health Effects 1978, 2:351-360. Arbor Science Publisher, Michigan, USA.
5. Blogoslawski W.J., Farrell L., Garceau R., Derrig P. Production of oxidants in ozonized sea water. Proceedings of the Second International Symposium on Ozone Technology 1976, 671-681. Ozone Press International, Jamesville, NY. R.G. Rice, P. Pichet, M.A. Vincent (Eds.).
6. Boone A.N., Vijayan M.M. Constitutive heat shock protein 70 (HSC70) expression in rainbow trout hepatocytes: effect of heat shock and heavy metal exposure. Comp. Biochem. Physiol. C 2002, 132:223-233.
7. Bouraoui Z., Banni M., Ghedira J., Clerandeau C., Guerbej H., Narbonne J.F., Boussetta H. Acute effects of cadmium on liver phase I and phase II enzymes and methallothionein accumulation on sea bream Sparus aurata. Fish Physiol. Biochem. 2008, 34:201-207.
8. Buchan K.A.H., Martin-Robichaud D.J., Benfey T.J. Measurement of dissolved ozone in seawater: a comparison of methods. Aquacult. Eng. 2005, 33:225-231.
9. Cerqueira C.C.C., Fernandes M.N. Gill tissue recovery after copper exposure and blood parameter responses in the tropical fish Prochilodus scrofa. Ecotoxicol. Environ. Safe. 2002, 52:83-91.
10. Crecelius E.A. Measurements of oxidants in ozonized seawater and some biological reactions. J. Fish. Res. Board Can. 1979, 36:1006-1008.
11. Crespo S., Sala R., Marlasca M.J. Different cell types in the gill epithelium of juvenile turbot Scophthalmus maximus. Aquaculture 1987, 67:216-217.
12. Cunha I., Neuparth T., Caeiro S., Costa M.H., Guilhermino L. Toxicity ranking of estuarine sediments on the basis of Sparus aurata biomarkers. Environ. Toxicol. Chem. 2007, 26:444-453.
13. Deane E.E., Woo N.Y.S. Impact of nitrite exposure in endocrine, osmoregulatory and cytoprotective functions in the marine teleost Sparus sarba. Aquat. Toxicol. 2007, 82:85-93.
14. Evans D.H. The fish gill: site of action and model for toxic effects of environmental pollutants. Environ. Health Perspect. 1987, 71:47-58.
15. Evans D.H., Piermarini P.M., Choe K.P. The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation and excretion of nitrogenous waste. Physiol. Rev. 2005, 85:97-117.
16. FAO, 2009. Psetta maxima (Linnaeus, 1758). Cultured aquatic species information programme. Fisheries and Aquaculture Department, Rome, Italy; www.fao.org/fishery/culturedspecies/Psetta_maxima/en.
17. Ferrari A., Venturino A., de D'angelo A.M.P. Effects of carbaryl and azinphos methyl on juvenile rainbow trout (Oncorhynchus mykiss) detoxifying enzymes. Pestic. Biochem. Physiol. 2007, 88:134-142.
18. Fink A.L., Goto Y. Molecular Chaperones in the Life Cycle of Proteins: Structure, Function, and Mode of Action 1998, Marcel Dekker, New York, USA, 626 pp.
19. Frances J., Allan G.L., Nowak B.F. The effects of nitrite on the short-term growth of silver perch (Bidyanus bidyanus). Aquaculture 1998, 163:63-72.
20. Fukunaga K., Suzuki T., Arita M., Suzuki S., Hara A., Yamauchi K., Shinriki N., Ishizaki K., Takama K. Acute toxicity of ozone against morphology of gill and erythrocytes of Japanese charr (Salvelinus leucomaenis). Comp. Biochem. Physiol. C 1992, 101:331-336.
21. Giese A.C., Christensen E. Effects of ozone on organisms. Physiol. Zool. 1954, 27:101-115.
22. Gisbert E., Rodriguez A., Cardona L., Huertas M., Gallardo M.A., Sarasquete C., Sala-Rabanal M., Ibarz A., Sánchez J., Castelló-Orvay F. Recovery of siberian sturgeon yearlings after an acute exposure to environmental nitrite: changes in the plasmatic ionic balance, Na+-K+ ATPase activity and gill histology. Aquaculture 2004, 239:141-154.
23. Gornati R., Papis E., Rimoldi S., Terova G., Saroglia M., Bernardini G. Rearing density influences the expression of stress-related genes in sea bass (Dicentrarchus labrax, L.). Gene 2004, 341:111-118.
24. Gornati R., Gualdoni S., Cavaliere R., Terova G., Saroglia M., Bernardini G. Molecular biology and fish welfare: a winning combination. Aquacult. Int. 2005, 13:51-55.
25. Haag W.R., Hoigné J. Kinetics and products of the reactions of ozone with various forms of chlorine and bromine in water. Ozone-Sci. Eng. 1984, 6:103-114.
26. Hall L.W., Burton D.T., Richardson L.D. Comparison of ozone and chlorine toxicity to the developmental stages of striped bass, Morone saxatilis. Can. J. Fish. Aquat. Sci. 1981, 38:752-757.
27. Halliwell B., Gutteridge J.M.C. Free Radicals in Biology and Medicine 1999, Oxford University Press, Oxford, UK, p. 704. third ed.
28. Hassanein H.M.A., Banhawy M.A., Soliman F.M., Abdel-Rehim S.A., Muller W.E.G., Schroder H.C. Induction of hsp70 by the herbicide oxyfluoren (goal) in the Egyptian Nile fish, Oreochromis niloticus. Arch. Environ. Contam. Toxicol. 1999, 37:78-84.
29. Hayes J.D., Pulford D.J. The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit. Rev. Biochem. Mol. Biol. 1995, 30:445-600.
30. Herwig R.P., Cordell J.R., Perrins J.C., Dinnel P.A., Gensemer R.W., Stubblefield W.A., Ruiz G.M., Kopp J.A., House M.L., Cooper W.J. Ozone treatment of ballast water on the oil tanker S/T Tonsina: chemistry, biology and toxicity. Mar. Ecol. Prog. Ser. 2006, 324:37-55.
31. Hoigné J., Bader H., Haag W.R., Staehelin J. Rate constant of reactions of ozone with organic and inorganic compounds in water-III. Water Res. 1985, 19:993-1004.
32. Hurlbert H.H. Pseudoreplication and the design of ecological field experiments. Ecol. Monogr. 1984, 54:187-211.
33. Iwama G.K., Thomas P.T., Forsyth R.B., Vijayan M.M. Heat shock protein expression in fish. Rev. Fish Biol. Fisher. 1998, 8:35-56.
34. Iwama G.K., Afonso L.O.B., Todgham A., Ackerman P., Nakano K. Are hsps suitable for indicating stressed states in fish?. J. Exp. Biol. 2004, 207:15-19.
35. Jiang G., Liu Y., Yang D., Lue Y. The toxicity of ozonated seawater to the Penaeus chinensis and Paralichthys olivaceus. Mar. Sci. 2001, 25:11-13.
36. Jones A.C., Gensemer R.W., Stubblefield W.A., van Genderen E., Dethloff G.M., Cooper W.J. Toxicity of ozonated seawater to marine organisms. Environ. Toxicol. Chem. 2006, 25:2683-2691.
37. Karan V., Vitorovic S., Tutundzic V., Poleskic V. Functional enzymes activity and gill histology of carp after copper sulphate exposure and recovery. Ecotoxicol. Environ. Safe. 1998, 40:49-55.
38. Kroupova H., Trubiroha A., Wuertz S., Kloas W. Stage dependent differences in RNA composition and content affect the outcome of expression profiling in roach (Rutilus rutilus) ovary. Comp. Biochem. Physiol. A 2011, 159:141-149.
39. Laurent P., Perry S.F. Environmental effects on fish gill morphology. Physiol. Zool. 1991, 64:4-25.
40. Lewis S., Handy R.D., Cordi B., Billinghurst Z., Depledge M.H. Stress proteins (HSP's): methods of detection and their use as an environmental biomarker. Ecotoxicology 1999, 8:351-368.
41. Liltved H., Hektoen H., Efraimsen H. Inactivation of bacterial and viral fish pathogens by ozonation or UV irradiation in water of different salinity. Aquacult. Eng. 1995, 14:107-122.
42. Livingstone D.R. Oxidative stress in aquatic organisms in relation to pollution and aquaculture. Rev. Med. Vet.-Toulouse 2003, 154:427-430.
43. Lovy J., Wright G.M., Speare D.J. Ultrastructural examination of the host inflammatory response within gills of netpen reared Chinook salmon (Oncorhynchus tshawytscha) with microsporidial gill disease. Fish Shellfish Immunol. 2007, 22:131-149.
44. Mallatt J. Fish gill structural changes induced by toxicants and other irritants: a statistical review. Can. J. Fish. Aquat. Sci. 1985, 42:630-648.
45. Martins C.I.M., Eding E.H., Verdegem M.C.J., Heinsbroek L.T.N., Schneider O., Blancheton J.P., Roque d'Orbcastel E., Verreth J.A.J. New developments in recirculating aquaculture systems in Europe: a perspective on environmental sustainability. Aquacult. Eng. 2010, 43:83-93.
46. Morgan M., Tovell P.W.A. The structure of the gill of the trout, Salmo gairdneri (Richardson). Z. Zellforsch. Mikrosk. Anat. 1973, 142:147-162.
47. Morita J., Suzuki T., Kimura S., Hara A., Takama K. Effect of low level ozone exposure on the serum TBA-reactive substance (TBA-RS) level and superoxide dismutase and catalse activities in rainbow trout. Fish. Sci. 1995, 61:890-891.
48. Oemcke D.J., van Leeuwen J. Potential of Ozone for Ballast Water Treatment 1998, CRC Reef Research Centre, James Cook University, Australia, 40 pp.
49. Paller M.H., Heidinger R.C. Mechanisms of delayed ozone toxicity to bluegill Lepomis macrochirus (Rafinesque). Environ. Pollut. A 1980, 22:229-239.
50. Pandey S., Parvez S., Ansari R.A., Ali M., Kaur M., Hayat F., Ahmad F., Raisuddin S. Effects of exposure to multiple trace metals on biochemical, histological and ultrastructural features of gills of a freshwater fish, Channa punctata Bloch. Chem. Biol. Interact. 2008, 174:183-192.
51. Perrins J.C., Cooper W.J., van Leeuwen J.H., Herwig R.P. Ozonation of seawater from different locations: formation and decay of total residual oxidants-implication for ballast water treatment. Mar. Pollut. Bull. 2006, 52:1023-1033.
52. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e36.
53. Pichavant K., Person-Le Ruyet J., Severe A., Le Roux A., Quemener L., Boeuf G. Effects of photopertiod on juvenile turbot (Psetta maxima): physiological status and growth. B. Fr. Peche. Piscic. 1998, 350-351:265-277.
54. Rabergh C.M.I., Airaksinen S., Soitamo A., Bjorklund H.V., Johansson T., Nikinmaa M., Sistonen J. Tissue-specific expression of zebrafish (Danio rerio) heat shock factor 1 mRNAS in response to heat stress. J. Exp. Biol. 2000, 203:1817-1824.
55. Reiser S., Schroeder J.P., Wuertz S., Kloas W., Hanel R. Histological and physiological alterations in juvenile turbot (Psetta maxima, L.) exposed to sublethal concentrations of ozone-produced oxidants in ozonated seawater. Aquaculture 2010, 307:157-164.
56. Richardson L.B., Burton D.T. Toxicity of ozonated estuarine water to juvenile blue crabs (Callinectes sapidus) and juvenile Atlantic menhaden (Brevoortia tyrannus). Bull. Environ. Contam. Toxicol. 1981, 26:171-178.
57. Richardson L.B., Burton D.T., Block R.M., Stavola A.M. Lethal and sublethal exposure and recovery effects of ozone-produced oxidants on adult white perch (Morone americana Gmelin). Water Res. 1983, 17:205-213.
58. Ritola O., Lyytikainen T., Pylkko P., Molsa H., Lindstrom-Seppa P. Glutathione-dependant defence system and monooxygenase enzyme activities in Arctic charr Salvelinus alpinus (L.) exposed to ozone. Aquaculture 2000, 185:219-233.
59. Ritola O., Peters L.D., Livingstone D.R., Lindstrom-Seppa P. Effects of in vitro exposure to ozone and/or hyperoxia on superoxide dismutase, catalase, glutathione and lipid peroxidation in red blood cells and plasma of rainbow trout, Oncorhynchus mykiss (Walbaum). Aquacult. Res. 2002, 33:165-175.
60. Ritola O., Livingstone D.R., Peters L.D., Lindstrom-Seppa P. Antioxidant processes are affected in juvenile rainbow trout (Oncorhynchus mykiss) exposed to ozone and oxygen-supersaturated water. Aquaculture 2002, 210:1-9.
61. Rosenthal H., Otte G. Ozonation in an intensive fish culture recycling system. Ozone-Sci. Eng. 1979, 1:319-327.
62. Salinas A.E., Wong M.G. Glutathione S-transferases - a review. Curr. Med. Chem. 1999, 6:279-309.
63. Schroeder J.P., Gärtner A., Waller U., Hanel R. The toxicity of ozone-produced oxidants to the Pacific white shrimp Litopenaeus vannamei. Aquaculture 2010, 305:6-11.
64. Smith T.R., Tremblay G.C., Bradley T.M. Characterization of the heat shock protein response of Atlantic salmon (Salmo salar). Fish Physiol. Biochem. 1999, 20:279-292.
65. Sokal R.R., Rohlf F.J. Biometry. The Principles and Practice of Statistics in Biological Research, second ed. 1995, WH Freeman & Co, New York, USA, 859 pp.
66. Sprague J.B. Measurement of pollutant toxicity to fish III. Sublethal effects and "safe" concentrations. Water Res. 1971, 5:245-266.
67. Sugita H., Asai T., Hayashi K., Mitsuya T., Amanuma K., Maruyama C., Deguchi Y. Application of ozone disinfection to remove Enterococcus seriolicida, Pasteurella piscicida, and Vibrio anguillarum from seawater. Appl. Environ. Microbiol. 1992, 58:4072-4075.
68. Summerfelt S.T., Hochheimer J.N. Review of ozone processes and applications as an oxidizing agent in aquaculture. Prog. Fish-Cult. 1997, 59:94-105.
69. Toner R.C., Brooks B. The effect of ozone on four species of phytoplankton, crab zoea and megalops and the Atlantic silverside Menidia menidia. Aquatic Applications of Ozone 1975, 154-160. International Ocean Institute, Stamford, Connecticut, USA. W.J. Blogoslawski, R.G. Rice (Eds.).
70. Trubiroha A., Wuertz S., Frank S.N., Sures B., Kloas W. Expression of gonadotropin subunits in roach (Rutilus rutilus, Cyprinidae) infected with plerocercoids of the tapeworm Ligula intestinalis (Cestoda). Int. J. Parasitol. 2009, 39:1465-1473.
71. van der Oost R., Beyer J., Vermeulen N.P.E. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ. Toxicol. Pharmacol. 2003, 13:57-149.
72. von Gunten U. Ozonation of drinking water: part II. Disinfection and by-product formation in presence of bromide, iodide or chlorine. Water Res. 2003, 37:1469-1487.
73. van Ham, E.H., 2003. The physiology of juvenile turbot (Scopthalmus maximus, Rafinesque) and Atlantic halibut (Hippoglossus hippoglossus, L.) under different stress conditions. PhD Thesis, University of Nijmegen, The Netherlands.
74. Waller U. Tank culture and recirculating systems. Environmental Impacts of Aquaculture 2000, 99-127. Sheffield Academic Press, Sheffield, UK. K.D. Black (Ed.).
75. Wedemeyer G.A., Nelson N.C., Yasutake W.I. Physiological and biochemical aspects of ozone toxicity to rainbow-trout (Salmo gairdneri). J. Fish. Res. Board Can. 1979, 36:605-614.
76. Wuertz, S., 2005. The paracrine IGF-I system and its role in the regulation of gonad maturation in sterlet, Acipenser ruthenus Linnaeus, 1758. PhD Thesis, dissertation.de, ISBN 3-86624-119-4.
77. Wuertz S., Gessner J., Kirschbaum F., Kloas W. Expression of IGF-I and IGF-I receptor in male and female sterlet, Acipenser ruthenus - Evidence for an important role in gonad maturation. Comp. Biochem. Physiol. A 2007, 147:223-230.