Skip to main content
Log in

Growth, stress tolerance and non-specific immune response of Japanese flounder Paralichthys olivaceus to probiotics in a closed recirculating system

  • Published:
Fisheries Science Aims and scope Submit manuscript

Abstract

Effects of probiotics on growth, stress tolerance and non-specific immune response in Japanese flounder Paralichthys olivaceus were evaluated in a closed recirculating system. Survival and growth of flounder treated by supplying commercial probiotics either in the diet (the probiotic diet group), or into the rearing water (the water supply group), were higher compared to the untreated group (the control group). Water quality parameters, pH, NH4−N, NO2−N and PO4−P showed lower concentration in the probiotic diet group compared with the control group and the supply group. Plasma lysozyme activity in the probiotic diet group and the water supply group was significantly higher (P<0.05) than that in the control group. In heat shock stress tests, flounder in the probiotics-treated groups showed greater heat tolerance (measured by 50% lethal time, LT50) than the control group. Pathogen challenge tests with Vibrio anguillarum (2×107 c.f.u./mL) resulted in significantly higher survival in the probiotics-treated groups than the control group. Results indicated that probiotics supplied in the rearing water and the diet of fish enhanced the stress tolerance and the non-specific immune system of Japanese flounder, providing them a higher resistance against stress conditions and pathogens.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Olafsen JA. Interactions between fish larvae and bacteria in marine aquaculture. Aquaculture 2001; 200: 223–247.

    Article  Google Scholar 

  2. Fuller R. Probiotics in man and animals. J. Appl. Bacteriol. 1989; 66: 365–378.

    PubMed  CAS  Google Scholar 

  3. Salminen S, Isolauri E, Salminen E. Clinical uses of probiotics for stabilizing the gut mucosal barrier: successful strains and future challenge. Antonie van leeuuwenboek 1997; 70: 347–358.

    Article  Google Scholar 

  4. Sakai M. Current research status of fish immunostimulants. Aquaculture 1998; 172: 63–92.

    Article  Google Scholar 

  5. Corre V Jr, Janeo RJ, Caipang AMA. Use of probiotics, reservoir with green water in shrimp farming in the Philippines. Proceed. Jpn. Soc. Promotion Sci. (JSPS) 2001; 30: 67–72.

    Google Scholar 

  6. Moriarty DJW. Control of luminous Vibrio species in penaeid aquaculture pond. Aquaculture 1998; 164: 351–358.

    Article  Google Scholar 

  7. Nogami K, Hamasaki K, Maeda M, Hirayama K. Biocontrol method in aquaculture for rearing the swimming crab larvae Portunus trituberculatus. Hydrobiologia 1997; 358: 291–295.

    Article  Google Scholar 

  8. Irianto A, Austin B. Probiotics in aquaculture. J. Fish. Dis. 2002; 25: 633–642.

    Article  Google Scholar 

  9. Rengpipat S, Phianphak W, Piyatiratitivorakul S, Menasveta P. Effects of a probiotic bacterium on black tiger shrimp Penaeus monodon survival and growth. Aquaculture 1998; 167: 301–313.

    Article  Google Scholar 

  10. Riquelme C, Araya R, Nelson V, Rojas A, Guaita M, Candia M. Potential probiotic strains in the culture of the Chilean scallop Argopecten purratus (Lamarck, 1819). Aquaculture 1997; 154: 17–26.

    Article  Google Scholar 

  11. Byun JW. Probiotic effect of Lactobacillus sp. Ds-12 in flounder. J. Gen. Appl. Microbiol. 1997; 43: 305–308.

    Article  PubMed  CAS  Google Scholar 

  12. Robertson PAW, O’Dowd C, Burrells C, Williams P, Austin B. Use of Carnobacterium sp. as a probiotic for Atlantic salmon (Salmo salar L.) and rainbow trout (Oncorynchus mykiss, Walbaum). Aquaculture 2000; 185: 235–243.

    Article  Google Scholar 

  13. Gatescope FJ. Lactic acid bacteria increase the resistance of turbot larvae, Scophthalmus maximus, against pathogenic Vibrio. Aquat. Living Resour. 1994; 7: 277–282.

    Article  Google Scholar 

  14. Sugita H, Tanaami H, Kobashi, T, Geguchi Y. Bacterial flora of coastal bivalves. Nippon Suisan Gakkaishi 1981 47: 655–661.

    Google Scholar 

  15. Yamanoi H, Muroga K, Maruyama K. A bacteriological investigation on the mass mortalities of red seabream Pagrus major larvae with intestinal swelling. Suisanzoshoku 1998; 36: 11–20.

    Google Scholar 

  16. Aranishi F, Nakane M. Epidermal protease of the Japanese eel. Fish Physiol. Biochem. 1997; 16: 471–478.

    Article  CAS  Google Scholar 

  17. Newell B, Morgan B, Cundy J. Determination of Urea in seawater. J. Mar. Res. 1967; 25: 201–202.

    CAS  Google Scholar 

  18. Strickland JDH, Parsons TA. Practical Hand Book of Seawater Analysis. Bull. Fish. Res. Ed. Can. 1972; 167: 1–311.

    Google Scholar 

  19. Association of Official Analytical Chemists (AOAC). Official Methods of Analysis, 16th edn. Association of Official Analytical Chemists, Arlington, VA. 1995.

    Google Scholar 

  20. Lowly OH, Rosebrough NJ, Fan AC, Rondall RT. Protein measurement with the folin phenol solution. J. Biol. Chem. 1951; 193: 265.

    Google Scholar 

  21. Takahashi Y, Itami T, Konegawa K. Enzymatic properties of partially lysozyme from the skin mucus of carp. Nippon Suisan Gakkaishi 1986; 52: 1209–1214.

    CAS  Google Scholar 

  22. Caruso D, Schlumberger O, Dahm C, Proteau JP. Plasma lysozyme levels in sheatfish Silurus glanis (L) subjected to stress and experimental infection with Edwardsiella tarda. Aquacult. Res. 2002; 33: 999–1008.

    Article  Google Scholar 

  23. Koshio S, Sakakura Y, Iida Y, Tsukamoto K, Kida T, Darbrowsky K. The effect of vitamin C intake on schooling behavior of amphidromus fish, Ayu Plecoglossus altivelis. Fish. Sci. 1997; 63: 619–624.

    CAS  Google Scholar 

  24. Austin B, Stuckey LF, Robertson PAW, Effendi I, Griffith DRW. A probiotic strain of Vibrio alginolyticus effective in reducing diseases caused by Aeromonous salmonicida, Vibrio anguillarum and Vibrio ordalii. J. Fish Dis. 1995; 18: 93–96.

    Article  Google Scholar 

  25. Chen CC, Chen SN. Water quality management with Bacillus spp. in the high-density culture of red-parrot fish Cichlasona citrinellum x C. sunspilum. North Am. J. Aquac. 2001; 63: 66–73.

    Article  Google Scholar 

  26. De Schrijver R, Ollevier F. Protein digestion in juvenile turbot (Scophthalmus maximus) and effects of dietary administration of Vibrio proteolyticus. Aquaculture 2000; 186: 107–116.

    Article  Google Scholar 

  27. Konsula Z, Liakopoulou-Kyriakides M. Hydrolysis of starches by the action of an α-amylase from Bacillus subtilis. Process Biochem. 2004; 39: 1745–1749.

    Article  CAS  Google Scholar 

  28. Ben Messaound E, Ben Ali M, Elleuch N, Fourati Masmoudi N, Bejar S. Purification and properties of a malthoheptaoseand maltohexaose forming amylase produced by Bacillus subtilis US116. Enzyme Microb. Technol. 2004; 34: 662–666.

    Article  Google Scholar 

  29. Ellouz Y, Bayoudh A, Kammoun S, Charsallah N, Nasri M. Productions of protease by Bacillus subtilis grown on sardinell heads and viscera. Bioresource Technol. 2001; 80; 49–51.

    Article  CAS  Google Scholar 

  30. Ellis AE. Techniques in fish immunology. In: Stolen JS, Fletcher TC, Anderson DP, Robertson BS, Van Muiswinkle WB (eds). Lysozyme Assays. SCS Publications, Fair Haven. 1990; 101–103.

    Google Scholar 

  31. Grinde B. Lysozyme from rainbow trout Salmo gairdneri Richardson as an anti bacterial agent against fish pathogens. J. Fish Dis. 1989; 12: 207–210.

    Article  Google Scholar 

  32. Haijji N, Sugita H, Ishii S, Deguchi Y. Serum bactericidal activity of carp (Cyprinus carpio) under supposed stressful rearing conditions. Bull. Coll. Agric. Vet. Med., Nihon Univ. 1990; 47: 50–54.

    Google Scholar 

  33. Mock A, Peters GS. Lysozyme activity in rainbow trout Oncorynchus mykiss (Walbaum) stressed by handling transport and water pollution. J. Fish Biol. 1990; 37: 873–885.

    Article  Google Scholar 

  34. Caruso D, Lazard J. Subordination stress in Nile tilapia and its effect on plasma lysozyme activity. J. Fish. Biol. 1999; 55: 451–454.

    Article  CAS  Google Scholar 

  35. Yehuda R, Yang R.-K, Guo SL, Makokine I, Singh B. Relationship between dexamethasone-inhibited lysozyme activity in peripheral mononuclear leukocytes and the cortisol and glucocorticoid receptor response to dexamethasone. J. Psychiatric Res. 2003; 37: 471–477.

    Article  Google Scholar 

  36. Demers NE, Bayne CJ. The immediate effects of stress on hormones and plasma lysozyme in rainbow trout. Dev. Comp. Immunol. 1997; 21: 363–373.

    Article  PubMed  CAS  Google Scholar 

  37. Kakuta I, Hisashi K, Nakamura H, Yamauchi K. Enhancement of the nonspecific defense activity of the skin mucus of red sea bream by oral administration of bovine lactoferin. Suisanzoshoku 1996; 44: 197–202.

    CAS  Google Scholar 

  38. Weyts FAA, Cohon N, Flik G, Verburg-Van Kemehande BMK. Interactions between the immune system and the hypothalamo-pituitary-interrenal axis in fish. Fish Shellfish Immunol. 1999; 9: 1–20.

    Article  Google Scholar 

  39. Joborn A, Olsson JC, Westerdahl A, Conway PL, Kjelleberg S. Colonization in the fish intestinal tract and production of inhibitory substances in intestinal mucus and faecal extracts by Carnobacterium sp. strain K1. J. Fish Dis. 1997; 20: 383–392.

    Article  Google Scholar 

  40. Rengpipat S, Rukpratanporn S, Piyatiratitivorakul S, Menasaveta P. Immunity enhancement in black tiger shirimp (Penaeus monodon) by a probiont bacterium (Bacillus S11). Aquaculture 2000; 191: 271–288.

    Article  CAS  Google Scholar 

  41. Nikoskelainen S, Ouwehand A, Salminen S, Bylund G. Protection of rainbow trout (Oncorynchus myliss) from frunculosis by Lactobacillus rhamnosus. Aquaculture 2001; 198: 229–236.

    Article  Google Scholar 

  42. Gildberg A, Mikkelsen H. Effects of supplementing the feed to Atlantic cod (Gadus morhua) fry with lactic acid bacteria and immuno-stimulating peptides during a challenge trial with Vibrio anguillarum. Aquaculture 1998; 167: 103–113.

    Article  CAS  Google Scholar 

  43. Gildberg A, Johansen A, Bogwald J. Growth and survival of Atlantic salmon (Salmo salar) fry given diets supplemented with fish protein hydrolysate and lactic acid bacteria during a challenge trial with Aeromonas salmonicida. Aquaculture 1995; 138: 23–34.

    Article  Google Scholar 

  44. Fevolden SE, Refstie T, Roed KH. Disease resistance in rainbow trout (Oncorhynchus mykiss) selected for stress response. Aquaculture 1992; 104: 19–29.

    Article  Google Scholar 

  45. Ringo E, Birkbeck TH, Munro DO, Vadstein O, Hielmeland K. The effect of early exposure to Vibrio pelagius on the aerobic bacterial flora of turbot Scophthalmus maximus (L) larvae. J. Appl. Bacteriol. 1996; 81: 207–211.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hiroto Maeda.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Taoka, Y., Maeda, H., Jo, JY. et al. Growth, stress tolerance and non-specific immune response of Japanese flounder Paralichthys olivaceus to probiotics in a closed recirculating system. Fish Sci 72, 310–321 (2006). https://doi.org/10.1111/j.1444-2906.2006.01152.x

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1111/j.1444-2906.2006.01152.x

Key Words

Navigation