Fish Physiology and Biochemistry

, Volume 43, Issue 6, pp 1501–1515 | Cite as

Influence of immunostimulant polysaccharides, nucleic acids, and Bacillus strains on the innate immune and acute stress response in turbots (Scophthalmus maximus) fed soy bean- and wheat-based diets

  • V. I. Fuchs
  • J. Schmidt
  • M. J. Slater
  • B. H. Buck
  • D. Steinhagen
Article

Abstract

Immunostimulants are widely applied in aquaculture practice and may have beneficial effects on the immune system and physical functions allowing higher tolerance to stress. In the current study, the impact of four (i–iv) dietary active ingredients on the immune and stress response of turbot was examined in two experiments (I and II). A basal low fish meal (FM; 32%) diet was formulated and supplemented with (i) yeast β-glucan and mannan oligosaccharide (GM), (ii) alginic acid (AC), (iii) yeast nucleotides and RNA (NR), or (iv) Bacillus strains (BS). The basal diet (C-LF) and a high FM (59%) control (C-HF) were maintained. All six diets were fed to juvenile turbots for 84 days in experiment I and for additional 28 days prior to experiment II. Immunological and hematological parameters were determined in experiment I. In experiment II, physical stress response to a typical short-term (<1 day) aquaculture handling procedure (combination of capture, netting/transfer, and crowding) was investigated. For this, turbot blood was sampled before and at 0.5, 1, 4, and 24 h post stress. Plasma lysozyme activity, neutrophil reactive oxygen species (ROS) production, and total plasma protein levels did not significantly differ between treatment groups; however, plasma cholesterol increased significantly in fish fed GM, AC, NR, and C-HF compared to C-LF (I). A significant increase in plasma glucose and triglyceride was observed in GM and NR treatments, while glucose levels were significantly higher in C-HF compared to C-LF. Moreover, the immunostimulant-supplemented diets exhibited significantly lower cortisol levels compared to controls C-LF (at 0.5 h) and C-HF (at 1 h) post stress, respectively (II). According to our findings, FM substitution did not modulate the innate immune response but was associated with reduced levels of cholesterol. Dietary immunostimulants were not effective enough to boost the immune response, but we believe they might be helpful to trigger metabolic advantages during stressful handling events on fish farms.

Keywords

Turbot Scophthalmus maximus Fish meal reduction Immunostimulants Lysozyme activity Reactive oxygen species Cortisol 

Notes

Acknowledgements

Sincere thanks to Michael Lutz (Köster Marine Proteins) and Matthias Seidel (J. Müller Weser) for supporting this study. Furthermore, special thanks to the scientific and technical staff of AWI and TiHo for the helpful work during the project. The authors wish to thank the anonymous reviewers for their constructive help in improving the manuscript.

Compliance with ethical standards

Funding

This study was funded by the Federal Ministry of Food and Agriculture (BMEL, “Programm Innovationsförderung”) via the Federal Office for Agriculture and Food (BLE; no. 2817304110).

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Ai Q, Xu H, Mai K, Xu W, Wang J, Zhang W (2011) Effects of dietary supplementation of Bacillus subtilis and fructooligosaccharide on growth performance, survival, non-specific immune response and disease resistance of juvenile large yellow croaker, Larimichthys crocea. Aquaculture 317:155–161CrossRefGoogle Scholar
  2. Ainsworth AJ (1994) A β-glucan inhibitable zymosan receptor on channel catfish neutrophils. Vet Immunol Immunopathol 41:141–152CrossRefPubMedGoogle Scholar
  3. Anderson DP (1992) Immunostimulants, adjuvants, and vaccine carriers in fish: applications to aquaculture. Annu Rev Fish Dis 2:281–307CrossRefGoogle Scholar
  4. Arends R, Mancera J, Munoz J, Wendelaar Bonga S, Flik G (1999) The stress response of the gilthead sea bream (Sparus aurata L.) to air exposure and confinement. J Endocrinol 163:149–157CrossRefPubMedGoogle Scholar
  5. Ashley PJ (2007) Fish welfare: current issues in aquaculture. Appl Anim Behav Sci 104:199–235CrossRefGoogle Scholar
  6. Bagni M, Romano N, Finoia MG, Abelli L, Scapigliati G, Tiscar PG, Sarti M, Marino G (2005) Short- and long-term effects of a dietary yeast β-glucan (Macrogard) and alginic acid (Ergosan) preparation on immune response in sea bass (Dicentrarchus labrax). Fish Shellfish Immunol 18:311–325CrossRefPubMedGoogle Scholar
  7. Balcázar JL, Blas I, Ruiz-Zarzuela I, Cunningham D, Vendrell D, Múzquiz JL (2006) The role of probiotics in aquaculture. Vet Microbiol 114:173–186CrossRefPubMedGoogle Scholar
  8. Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517–525CrossRefPubMedGoogle Scholar
  9. Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annu Rev Fish Dis 1:3–26CrossRefGoogle Scholar
  10. Bonaldo A, Thompson KD, Manfrin A, Adams A, Murano E, Mordenti AL, Gatta PP (2007) The influence of dietary β-glucans on the adaptive and innate immune responses of European sea bass (Dicentrarchus labrax) vaccinated against vibriosis. Ital J Anim Sci 6:151–164CrossRefGoogle Scholar
  11. Bonaldo A, Parma L, Mandrioli L, Sirri R, Fontanillas R, Badiani A, Gatta PP (2011) Increasing dietary plant proteins affects growth performance and ammonia excretion but not digestibility and gut histology in turbot (Psetta maxima) juveniles. Aquaculture 318:101–108CrossRefGoogle Scholar
  12. Bonaldo A, Di Marco P, Petochi T, Marino G, Parma L, Fontanillas R, Koppe W, Mongile F, Finoia MG, Gatta PP (2014) Feeding turbot juveniles Psetta maxima L. with increasing dietary plant protein levels affects growth performance and fish welfare. Aquac Nutr 21:401–413CrossRefGoogle Scholar
  13. Bransden MP, Carter CG, Nowak BF (2001) Effects of dietary protein source on growth, immune function, blood chemistry and disease resistance of Atlantic salmon (Salmo salar L.) parr. Anim Sci 73:105–113CrossRefGoogle Scholar
  14. Bridle AR, Carter CG, Morrison RN, Nowak BF (2005) The effect of β-glucan administration on macrophage respiratory burst activity and Atlantic salmon, Salmo salar L., challenged with amoebic gill disease—evidence of inherent resistance. J Fish Dis 28:347–356CrossRefPubMedGoogle Scholar
  15. Burrells C, Williams PD, Southgate PJ, Crampton VO (1999) Immunological, physiological and pathological responses of rainbow trout (Oncorhynchus mykiss) to increasing dietary concentrations of soybean proteins. Vet Immunol Immunopathol 72:277–288CrossRefPubMedGoogle Scholar
  16. Burrells C, Williams PD, Forno PF (2001a) Dietary nucleotides: a novel supplement in fish feeds: 1. Effects on resistance to disease in salmonids. Aquaculture 199:159–169CrossRefGoogle Scholar
  17. Burrells C, Williams PD, Southgate PJ, Wadsworth SL (2001b) Dietary nucleotides: a novel supplement in fish feeds: 2. Effects on vaccination, salt water transfer, growth rates and physiology of Atlantic salmon (Salmo salar L.) Aquaculture 199:171–184CrossRefGoogle Scholar
  18. Caipang C, Lazado C, Berg I, Brinchmann M, Kiron V (2011) Influence of alginic acid and fucoidan on the immune responses of head kidney leukocytes in cod. Fish Physiol Biochem 37:603–612CrossRefPubMedGoogle Scholar
  19. Carver JD, Walker WA (1995) The role of nucleotides in human nutrition. J Nutr Biochem 6:58–72CrossRefGoogle Scholar
  20. Castro R, Couso N, Obach A, Lamas J (1999) Effect of different β-glucans on the respiratory burst of turbot (Psetta maxima) and gilthead seabream (Sparus aurata) phagocytes. Fish Shellfish Immunol 9:529–541CrossRefGoogle Scholar
  21. Castro R, Zarra I, Lamas J (2004) Water-soluble seaweed extracts modulate the respiratory burst activity of turbot phagocytes. Aquaculture 229:67–78CrossRefGoogle Scholar
  22. Cerdá-Reverter JM, Zanuy S, Carrillo M, Madrid JA (1998) Time-course studies on plasma glucose, insulin, and cortisol in sea bass (Dicentrarchus labrax) held under different photoperiodic regimes. Physiol Behav 64:245–250CrossRefPubMedGoogle Scholar
  23. Cheng Z, Buentello A, Gatlin Iii DM (2011) Dietary nucleotides influence immune responses and intestinal morphology of red drum Sciaenops ocellatus. Fish Shellfish Immunol 30:143–147CrossRefPubMedGoogle Scholar
  24. Choudhury D, Pal AK, Sahu NP, Kumar S, Das SS, Mukherjee SC (2005) Dietary yeast RNA supplementation reduces mortality by Aeromonas hydrophila in rohu (Labeo rohita L.) juveniles. Fish Shellfish Immunol 19:281–291CrossRefPubMedGoogle Scholar
  25. Costas B, Rêgo PCNP, Conceição LEC, Dias J, Afonso A (2013) Dietary arginine supplementation decreases plasma cortisol levels and modulates immune mechanisms in chronically stressed turbot (Scophthalmus maximus). Aquac Nutr 19:25–38CrossRefGoogle Scholar
  26. Dalmo RA, Bøgwald J (2008) β-Glucans as conductors of immune symphonies. Fish Shellfish Immunol 25:384–396CrossRefPubMedGoogle Scholar
  27. Davis KB (2004) Temperature affects physiological stress responses to acute confinement in sunshine bass (Morone chrysops×Morone saxatilis). Comp Biochem Physiol A Mol Integr Physiol 139:433–440CrossRefPubMedGoogle Scholar
  28. Dietz C, Kroeckel S, Schulz C, Susenbeth A (2012) Energy requirement for maintenance and efficiency of energy utilization for growth in juvenile turbot (Psetta maxima, L.): the effect of strain and replacement of dietary fish meal by wheat gluten. Aquaculture 358–359:98–107CrossRefGoogle Scholar
  29. El-Boshy ME, El-Ashram AM, AbdelHamid FM, Gadalla HA (2010) Immunomodulatory effect of dietary Saccharomyces cerevisiae, β-glucan and laminaran in mercuric chloride treated Nile tilapia (Oreochromis niloticus) and experimentally infected with Aeromonas hydrophila. Fish Shellfish Immunol 28:802–808CrossRefPubMedGoogle Scholar
  30. Engstad RE, Robertsen B (1993) Recognition of yeast cell wall glucan by Atlantic salmon (Salmo salar L.) macrophages. Dev Comp Immunol 17:319–330CrossRefPubMedGoogle Scholar
  31. Ferrari S, Millot S, Leguay D, Chatain B, Bégout M-L (2015) Consistency in European seabass coping styles: a life-history approach. Appl Anim Behav Sci 167:74–88CrossRefGoogle Scholar
  32. Figueras A, Santarém M, Novoa B (1998) Influence of the sequence of administration of β-glucans and a Vibrio damsela vaccine on the immune response of turbot (Scophthalmus maximus L.) Vet Immunol Immunopathol 64:59–68CrossRefPubMedGoogle Scholar
  33. Focardi S, Corsi I, Franchi E (2005) Safety issues and sustainable development of European aquaculture: new tools for environmentally sound aquaculture. Aquacult Int 13:3–17CrossRefGoogle Scholar
  34. Fuchs VI, Schmidt J, Slater MJ, Zentek J, Buck BH, Steinhagen D (2015) The effect of supplementation with polysaccharides, nucleotides, acidifiers and Bacillus strains in fish meal and soy bean based diets on growth performance in juvenile turbot (Scophthalmus maximus). Aquaculture 437:243–251CrossRefGoogle Scholar
  35. Gabrielsen BO, Austreng E (1998) Growth, product quality and immune status of Atlantic salmon, Salmo salar L., fed wet feed with alginate. Aquac Res 29:397–401CrossRefGoogle Scholar
  36. Ganga R, Montero D, Bell JG, Atalah E, Ganuza E, Vega-Orellana O, Tort L, Acerete L, Afonso JM, Benitez-Sanatana T, Fernández Vaquero A, Izquierdo M (2011) Stress response in sea bream (Sparus aurata) held under crowded conditions and fed diets containing linseed and/or soybean oil. Aquaculture 311:215–223CrossRefGoogle Scholar
  37. Gioacchini G, Smith P, Carnevali O (2008) Effects of Ergosan on the expression of cytokine genes in the liver of juvenile rainbow trout (Oncorhynchus mykiss) exposed to enteric red mouth vaccine. Vet Immunol Immunopathol 123:215–222CrossRefPubMedGoogle Scholar
  38. Gregory TR, Wood CM (1999) The effects of chronic plasma cortisol elevation on the feeding behaviour, growth, competitive ability, and swimming performance of juvenile rainbow trout. Physiol Biochem Zool 72:286–295CrossRefPubMedGoogle Scholar
  39. Gudding R, Lillehaug A, Evensen Ø (1999) Recent developments in fish vaccinology. Vet Immunol Immunopathol 72:203–212CrossRefPubMedGoogle Scholar
  40. Guerreiro I, Pérez-Jiménez A, Costas B, Oliva-Teles A (2014) Effect of temperature and short chain fructooligosaccharides supplementation on the hepatic oxidative status and immune response of turbot (Scophthalmus maximus). Fish Shellfish Immunol 40:570–576CrossRefPubMedGoogle Scholar
  41. Heidarieh M, Soltani M, Tamimi AH, Toluei MH (2011) Comparative effect of raw fiber (Vitacel) and alginic acid (Ergosan) on growth performance, immunocompetent cell population and plasma lysozyme content of giant sturgeon (Huso huso). Turkish J Fish Aquat Sci 11:445–450Google Scholar
  42. Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597CrossRefGoogle Scholar
  43. Horne MT (1997) Technical aspects of the administration of vaccines. Dev Biol Stand 90:79–89PubMedGoogle Scholar
  44. Huntingford FA, Adams C, Braithwaite VA, Kadri S, Pottinger TG, Sandøe P, Turnbull JF (2006) Current issues in fish welfare. J Fish Biol 68:332–372CrossRefGoogle Scholar
  45. Hutchinson TH, Manning MJ (1996) Seasonal trends in serum lysozyme activity and total protein concentration in dab (Limanda limanda L.) sampled from Lyme Bay, UK. Fish Shellfish Immunol 6:473–482CrossRefGoogle Scholar
  46. Jung-Schroers V, Adamek M, Jung A, Harris S, Dóza ÖS, Baumer A, Steinhagen D (2015) Feeding of β-1,3/1,6-glucan increases the diversity of the intestinal microflora of carp (Cyprinus carpio). Aquac Nutr. doi: 10.1111/anu.12320
  47. Kesarcodi-Watson A, Kaspar H, Lategan MJ, Gibson L (2008) Probiotics in aquaculture: the need, principles and mechanisms of action and screening processes. Aquaculture 274:1–14CrossRefGoogle Scholar
  48. Khosravi S, Rahimnejad S, Herault M, Fournier V, Lee C-R, Dio Bui HT, Jeong J-B, Lee K-J (2015) Effects of protein hydrolysates supplementation in low fish meal diets on growth performance, innate immunity and disease resistance of red sea bream Pagrus major. Fish Shellfish Immunol 45:858–868CrossRefPubMedGoogle Scholar
  49. Kiron V (2012) Fish immune system and its nutritional modulation for preventive health care. Anim Feed Sci Technol 173:111–133CrossRefGoogle Scholar
  50. Kokou F, Rigos G, Henry M, Kentouri M, Alexis M (2012) Growth performance, feed utilization and non-specific immune response of gilthead sea bream (Sparus aurata L.) fed graded levels of a bioprocessed soybean meal. Aquaculture 364–365:74–81CrossRefGoogle Scholar
  51. Krogdahl Å, Bakke-Mckellep AM, RØed KH, Baeverfjord G (2000) Feeding Atlantic salmon Salmo salar L. soybean products: effects on disease resistance (furunculosis), and lysozyme and IgM levels in the intestinal mucosa. Aquac Nutr 6:77–84CrossRefGoogle Scholar
  52. Laiz-Carrión R, Martín Del Río MP, Miguez JM, Mancera JM, Soengas JL (2003) Influence of cortisol on osmoregulation and energy metabolism in gilthead seabream Sparus aurata. J Exp Zool Part A: Comp Exp Biol 298A:105–118CrossRefGoogle Scholar
  53. Leonardi M, Sandino AM, Klempau A (2003) Effect of a nucleotide-enriched diet on the immune system, plasma cortisol levels and resistance to infectious pancreatic necrosis (IPN) in juvenile rainbow trout (Oncorhynchus mykiss). Arch Bull Eur Assoc Fish Pathol 23:52–59Google Scholar
  54. Li P, Lewis DH, Gatlin Iii DM (2004) Dietary oligonucleotides from yeast RNA influence immune responses and resistance of hybrid striped bass (Morone chrysops × Morone saxatilis) to Streptococcus iniae infection. Fish Shellfish Immunol 16:561–569CrossRefPubMedGoogle Scholar
  55. Li Y, Wang YJ, Wang L, Jiang KY (2008) Influence of several non-nutrient additives on nonspecific immunity and growth of juvenile turbot, Scophthalmus maximus L. Aquac Nutr 14:387–395CrossRefGoogle Scholar
  56. Lillehaug A (1989) A cost-effectiveness study of three different methods of vaccination against vibriosis in salmonids. Aquaculture 83:227–236CrossRefGoogle Scholar
  57. Magnadóttir B (2006) Innate immunity of fish (overview). Fish Shellfish Immunol 20:137–151CrossRefPubMedGoogle Scholar
  58. Meng Y, Ma R, Ma J, Han D, Xu W, Zhang W, Mai K (2016) Dietary nucleotides improve the growth performance, antioxidative capacity and intestinal morphology of turbot (Scophthalmus maximus). Aquac Nutr. doi: 10.1111/anu.12425:n/a-n/a
  59. Merrifield DL, Dimitroglou A, Foey A, Davies SJ, Baker RTM, Bøgwald J, Castex M, Ringø E (2010) The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture 302:1–18CrossRefGoogle Scholar
  60. Merrifield DL, Harper GM, Mustafa S, Carnevali O, Picchietti S, Davies SJ (2011) Effect of dietary alginic acid on juvenile tilapia (Oreochromis niloticus) intestinal microbial balance, intestinal histology and growth performance. Cell Tissue Res 344:135–146CrossRefPubMedGoogle Scholar
  61. Mommsen T, Vijayan M, Moon T (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268CrossRefGoogle Scholar
  62. Montoya A, López-Olmeda JF, Garayzar ABS, Sánchez-Vázquez FJ (2010) Synchronization of daily rhythms of locomotor activity and plasma glucose, cortisol and thyroid hormones to feeding in gilthead seabream (Sparus aurata) under a light–dark cycle. Physiol Behav 101:101–107CrossRefPubMedGoogle Scholar
  63. Mugnier C, Fostier A, Guezou S, Gaignon J-L, Quemener L (1998) Effect of some repetitive factors on turbot stress response. Aquacult Int 6:33–45CrossRefGoogle Scholar
  64. Naylor RL, Goldburg RJ, Primavera JH, Kautsky N, Beveridge MCM, Clay J, Folke C, Lubchenco J, Mooney H, Troell M (2000) Effect of aquaculture on world fish supplies. Nature 405:1017–1024CrossRefPubMedGoogle Scholar
  65. Neiffer DL, Stamper MA (2009) Fish sedation, anesthesia, analgesia, and euthanasia: considerations, methods, and types of drugs. ILAR J 50:343–360CrossRefPubMedGoogle Scholar
  66. Ogier de Baulny M, Quentel C, Fournier V, Lamour F, Le Gouvello R (1996) Effect of long-term oral administration of β-glucan as an immunostimulant or an adjuvant on some non-specific parameters of the immune response of turbot Scophthalmus maximus. Dis Aquat Org 26:139–147CrossRefGoogle Scholar
  67. Oliveira CV, Aparício R, Blanco-Vives B, Chereguini O, Martín I, Javier Sánchez-Vazquez F (2013) Endocrine (plasma cortisol and glucose) and behavioral (locomotor and self-feeding activity) circadian rhythms in Senegalese sole (Solea senegalensis Kaup 1858) exposed to light/dark cycles or constant light. Fish Physiol Biochem 39:479–487CrossRefPubMedGoogle Scholar
  68. Palermo FA, Cardinaletti G, Cocci P, Tibaldi E, Polzonetti-Magni A, Mosconi G (2013) Effects of dietary nucleotides on acute stress response and cannabinoid receptor 1 mRNAs in sole, Solea solea. Comp Biochem Physiol A Mol Integr Physiol 164:477–482CrossRefPubMedGoogle Scholar
  69. Parry RM, Chandan RC, Shahani KM (1965) A rapid and sensitive assay of muramidase. Proc Soc Exp Biol Med 119:384–386CrossRefPubMedGoogle Scholar
  70. Peddie S, Zou J, Secombes CJ (2002) Immunostimulation in the rainbow trout (Oncorhynchus mykiss) following intraperitoneal administration of Ergosan. Vet Immunol Immunopathol 86:101–113CrossRefPubMedGoogle Scholar
  71. Peng M, Xu W, Ai Q, Mai K, Liufu Z, Zhang K (2013) Effects of nucleotide supplementation on growth, immune responses and intestinal morphology in juvenile turbot fed diets with graded levels of soybean meal (Scophthalmus maximus L.) Aquaculture 392–395:51–58CrossRefGoogle Scholar
  72. Pick E, Charon J, Mizel D (1981) A rapid densitometric microassay for nitroblue tetrazolium reduction and application of the microassay to macrophages. J Reticuloendothel Soc 30:581–593PubMedGoogle Scholar
  73. Pickering AD, Pottinger TG (1989) Stress responses and disease resistance in salmonid fish: effects of chronic elevation of plasma cortisol. Fish Physiol Biochem 7:253–258CrossRefPubMedGoogle Scholar
  74. Regost C, Arzel J, Kaushik SJ (1999) Partial or total replacement of fish meal by corn gluten meal in diet for turbot (Psetta maxima). Aquaculture 180:99–117CrossRefGoogle Scholar
  75. Reiser S, Schroeder JP, Wuertz S, Kloas W, Hanel R (2010) Histological and physiological alterations in juvenile turbot (Psetta maxima, L.) exposed to sublethal concentrations of ozone-produced oxidants in ozonated seawater. Aquaculture 307:157–164CrossRefGoogle Scholar
  76. Ringø E, Olsen RE, Gifstad TØ, Dalmo RA, Amlund H, Hemre GI, Bakke AM (2010) Prebiotics in aquaculture: a review. Aquac Nutr 16:117–136CrossRefGoogle Scholar
  77. Ringø E, Olsen RE, Vecino JLG, Wadsworth S, Song SK (2012) Use of immunostimulants and nucleotides in aquaculture: a review. J Marine Sci Res Dev 1:104. doi: 10.4172/2155-9910.1000104 Google Scholar
  78. Rook GAW, Steele J, Umar S, Dockrell HM (1985) A simple method for the solubilisation of reduced NBT, and its use as a colorimetric assay for activation of human macrophages by γ-interferon. J Immunol Methods 82:161–167CrossRefPubMedGoogle Scholar
  79. Sakai M (1999) Current research status of fish immunostimulants. Aquaculture 172:63–92CrossRefGoogle Scholar
  80. Sakai M, Taniguchi K, Mamoto K, Ogawa H, Tabata M (2001) Immunostimulant effects of nucleotide isolated from yeast RNA on carp, Cyprinus carpio L. J Fish Dis 24:433–438CrossRefGoogle Scholar
  81. Segner H, Sundh H, Buchmann K, Douxfils J, Sundell K, Mathieu C, Ruane N, Jutfelt F, Toften H, Vaughan L (2012) Health of farmed fish: its relation to fish welfare and its utility as welfare indicator. Fish Physiol Biochem 38:85–105CrossRefPubMedGoogle Scholar
  82. Selvaraj V, Sampath K, Sekar V (2005) Administration of yeast glucan enhances survival and some non-specific and specific immune parameters in carp (Cyprinus carpio) infected with Aeromonas hydrophila. Fish Shellfish Immunol 19:293–306CrossRefPubMedGoogle Scholar
  83. Sitjà-Bobadilla A, Peña-Llopis S, Gómez-Requeni P, Médale F, Kaushik S, Pérez-Sánchez J (2005) Effect of fish meal replacement by plant protein sources on non-specific defence mechanisms and oxidative stress in gilthead sea bream (Sparus aurata). Aquaculture 249:387–400CrossRefGoogle Scholar
  84. Skouras A, Steinhagen D (2003) Measuring some flounder (Platichthys flesus L.) innate immune responses to be incorporated in effect biomonitoring concepts. Helgol Mar Res 57:199–205CrossRefGoogle Scholar
  85. Skouras A, Broeg K, Dizer H, von Westernhagen H, Hansen P-D, Steinhagen D (2003) The use of innate immune responses as biomarkers in a programme of integrated biological effects monitoring on flounder (Platichthys flesus) from the southern North Sea. Helgol Mar Res 57:190–198CrossRefGoogle Scholar
  86. Staykov Y, Spring P, Denev S, Sweetman J (2007) Effect of a mannan oligosaccharide on the growth performance and immune status of rainbow trout (Oncorhynchus mykiss). Aquacult Int 15:153–161CrossRefGoogle Scholar
  87. Sun G, Li M, Wang J, Liu Y (2016) Effects of flow rate on growth performance and welfare of juvenile turbot (Scophthalmus maximus L.) in recirculating aquaculture systems. Aquac Res 47:1341–1352CrossRefGoogle Scholar
  88. Tahmasebi-Kohyani A, Keyvanshokooh S, Nematollahi A, Mahmoudi N, Pasha-Zanoosi H (2012) Effects of dietary nucleotides supplementation on rainbow trout (Oncorhynchus mykiss) performance and acute stress response. Fish Physiol Biochem 38:431–440CrossRefPubMedGoogle Scholar
  89. Thorarinsson R, Powell DB (2006) Effects of disease risk, vaccine efficacy, and market price on the economics of fish vaccination. Aquaculture 256:42–49CrossRefGoogle Scholar
  90. Torrecillas S, Makol A, Caballero MJ, Montero D, Dhanasiri AKS, Sweetman J, Izquierdo M (2012) Effects on mortality and stress response in European sea bass, Dicentrarchus labrax (L.), fed mannan oligosaccharides (MOS) after Vibrio anguillarum exposure. J Fish Dis 35:591–602CrossRefPubMedGoogle Scholar
  91. Tort L (2011) Stress and immune modulation in fish. Dev Comp Immunol 35:1366–1375CrossRefPubMedGoogle Scholar
  92. Urán PA, Schrama JW, Rombout JHWM, Obach A, Jensen L, Koppe W, Verreth JAJ (2008) Soybean meal-induced enteritis in Atlantic salmon (Salmo salar L.) at different temperatures. Aquac Nutr 14:324–330CrossRefGoogle Scholar
  93. Van Ham EH, Van Anholt RD, Kruitwagen G, Imsland AK, Foss A, Sveinsbø BO, FitzGerald R, Parpoura AC, Stefansson SO, Wendelaar Bonga SE (2003) Environment affects stress in exercised turbot. Comp Biochem Physiol A Mol Integr Physiol 136:525–538CrossRefPubMedGoogle Scholar
  94. Verburg-van Kemenade BML, Daly JG, Groeneveld A, Wiegertjes GF (1996) Multiple regulation of carp (Cyprinus carpio L.) macrophages and neutrophilic granulocytes by serum factors: influence of infection with atypical Aeromonas salmonicida. Vet Immunol Immunopathol 51:189–200CrossRefPubMedGoogle Scholar
  95. Verburg-Van Kemenade BML, Stolte EH, Metz JR, Chadzinska M (2009) Chapter 7: Neuroendocrine–immune interactions in teleost fish. In: Bernier NJ, Kraak GVD, Farrell AP, Colin JB (eds) Fish physiology. Academic, pp 313–364Google Scholar
  96. Waring CP, Stagg RM, Poxton MG (1992) The effects of handling on flounder (Platichthys flesus L.) and Atlantic salmon (Salmo salar L.) J Fish Biol 41:131–144CrossRefGoogle Scholar
  97. Waring CP, Stagg RM, Poxton MG (1996) Physiological responses to handling in the turbot. J Fish Biol 48:161–173CrossRefGoogle Scholar
  98. Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625PubMedGoogle Scholar
  99. Whyte SK (2007) The innate immune response of finfish—a review of current knowledge. Fish Shellfish Immunol 23:1127–1151CrossRefPubMedGoogle Scholar
  100. Yoo G, Lee S, Kim YC, Okorie OE, Park GJ, Han YO, Choi S-M, Kang J-C, Sun M, Bai SC (2007) Effects of dietary β-1,3 glucan and feed stimulants in juvenile olive flounder, Paralichthys olivaceus. J World Aquacult Soc 38:138–145CrossRefGoogle Scholar
  101. Zheng K, Liang M, Yao H, Wang J, Chang Q (2013) Effect of size-fractionated fish protein hydrolysate on growth and feed utilization of turbot (Scophthalmus maximus L.) Aquac Res 44:895–902CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • V. I. Fuchs
    • 1
    • 2
  • J. Schmidt
    • 2
  • M. J. Slater
    • 2
  • B. H. Buck
    • 2
    • 3
  • D. Steinhagen
    • 1
  1. 1.Fish Disease Research UnitUniversity of Veterinary Medicine HannoverHannoverGermany
  2. 2.Helmholtz Center for Polar and Marine ResearchBremerhavenGermany
  3. 3.University of Applied Sciences BremerhavenBremerhavenGermany

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