Advertisement

The Blood Indicators of Siberian Sturgeon Welfare

  • Rémy Simide
  • Sandrine Gaillard
  • Simone Richard
Chapter

Abstract

Animal welfare science is expanding rapidly. The use of physiological indicators is one of the most investigated ways in which to evaluate welfare. Blood samples are minimally invasive; they enable successive sampling of the same individuals and provide access to a large range of indicators from numerous physiological functions. Thus, they provide all the useful features for welfare research. The welfare of Siberian sturgeon is a very recent consideration. This chapter gathers together indicators from bibliography and our analysis which have been or could be used to assess this. The current research on stress responses and health status in Siberian sturgeon aids in the collation of this extensive information. Blood samples enable monitoring of hormonal response, biochemical and hydromineral indicators, oxidative stress parameters, immune status, hematological markers, and molecular indicators. The integration of these numerous physiological parameters in the context of welfare assessment is discussed throughout this chapter. Measuring physiological indicators from blood samples analyzed by multivariate analysis could be one of the future standards in the monitoring of fish welfare.

Keywords

Welfare Acipenser baerii Blood sampling Physiological functions Multivariate analysis 

Notes

Acknowledgments

We particularly thank S. Coupé and N. Prévot-D’Alvise for their advice, the PACA which funded this study, and Sturgeon SCEA for generously providing sturgeon.

References

  1. Adams CE, Turnbull JF, Bell A, Bron JE, Huntingford FA (2007) Multiple determinants of welfare in farmed fish: stocking density, disturbance, and aggression in Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 64:336–344CrossRefGoogle Scholar
  2. Ahmdifar E, Akrami R, Ghelichi A, Zarejabad AM (2011) Effects of different dietary prebiotic inulin levels on blood serum enzymes, hematologic, and biochemical parameters of great sturgeon (Huso huso) juveniles. Comp Clin Pathol 20:447–451CrossRefGoogle Scholar
  3. Alexander JB, Ingram GA (1992) Noncellular nonspecific defence mechanisms of fish. Annu Rev Fish Dis 2:249–279CrossRefGoogle Scholar
  4. Allen PJ, Cech JJ (2007) Age/size effects on juvenile green sturgeon, Acipenser medirostris, oxygen consumption, growth, and osmoregulation in saline environments. Environ Biol Fish 79:211–229CrossRefGoogle Scholar
  5. Allen PJ, Barth CC, Peake SJ, Abrahams MV, Anderson WG (2009) Cohesive social behaviour shortens the stress response: the effects of conspecifics on the stress response in lake sturgeon Acipenser fulvescens. J Fish Biol 74:90–104PubMedCrossRefGoogle Scholar
  6. Asadi F, Halajian A, Pourkabir M, Asadian P, Jadidizadeh F (2006a) Serum biochemical parameters of Huso huso. Comp Clin Pathol 15:245–248CrossRefGoogle Scholar
  7. Asadi F, Masoudifard M, Vajhi A, Lee K, Pourkabir M, Khazraeinia P (2006b) Serum biochemical parameters of Acipenser persicus. Fish Physiol Biochem 32:43–47PubMedCrossRefGoogle Scholar
  8. Ashley PJ (2007) Fish welfare: current issues in aquaculture. Appl Anim Behav Sci 104:199–235CrossRefGoogle Scholar
  9. Bahmani M, Kazemi R, Donskaya P (2001) A comparative study of some hematological features in young reared sturgeons (Acipenser persicus and Huso huso). Fish Physiol Biochem 24:135–140CrossRefGoogle Scholar
  10. Baker DW, Peake SJ, Kieffer JD (2008) The effect of capture, handling, and tagging on hematological variables in wild adult lake sturgeon. N Am J Fish Manag 28:296–300CrossRefGoogle Scholar
  11. Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517–525PubMedCrossRefGoogle Scholar
  12. Barton BA, Bollig H, Hauskins BL, Jansen CR (2000) Juvenile pallid (Scaphirhynchus albus) and hybrid pallid × shovelnose (S. albus×platorynchus) sturgeons exhibit low physiological responses to acute handling and severe confinement. Comp Biochem Physiol, Part A: Mol Integr Physiol 126:125–134CrossRefGoogle Scholar
  13. Barton BA, Morgan JD, Vijayan MM (2002) Physiological and condition-related indicators of environmental stress in fish. Biol Indic Aquat Ecosyst Stress:111–148Google Scholar
  14. Basu N, Todgham AE, Ackerman PA, Bibeau MR, Nakano K, Schulte PM, Iwama GK (2002) Heat shock protein genes and their functional significance in fish. Gene 295:173–183PubMedCrossRefGoogle Scholar
  15. Bayunova L, Barannikova I, Semenkova T (2002) Sturgeon stress reactions in aquaculture. J Appl Ichthyol 18:397–404CrossRefGoogle Scholar
  16. Belanger JM, Son JH, Laugero KD, Moberg GP, Doroshov SI, Lankford SE, Cech JJ Jr (2001) Effects of short-term management stress and ACTH injections on plasma cortisol levels in cultured white sturgeon, Acipenser transmontanus. Aquaculture 203:165–176CrossRefGoogle Scholar
  17. Bœuf G, Payan P (2001) How should salinity influence fish growth? Comp Biochem Physiol, Part C: Toxicol Pharmacol 130:411–423Google Scholar
  18. Bols NC, Brubacher JL, Ganassin RC, Lee LEJ (2001) Ecotoxicology and innate immunity in fish. Dev Comp Immunol 25:853–873PubMedCrossRefGoogle Scholar
  19. Brown C (2015) Fish intelligence, sentience and ethics. Anim Cogn 18:1–17PubMedCrossRefGoogle Scholar
  20. Cataldi E, Di Marco P, Mandich A, Cataudella S (1998) Serum parameters of Adriatic sturgeon Acipenser naccarii (Pisces: Acipenseriformes): effects of temperature and stress. Comp Biochem Physiol, Part A: Mol Integr Physiol 121:351–354CrossRefGoogle Scholar
  21. Costantini D, Verhulst S (2009) Does high antioxidant capacity indicate low oxidative stress? Funct Ecol 23:506–509CrossRefGoogle Scholar
  22. Costantini D, Rowe M, Butler MW, McGraw KJ (2010) From molecules to living systems: historical and contemporary issues in oxidative stress and antioxidant ecology. Funct Ecol 24:950–959CrossRefGoogle Scholar
  23. Davis AK, Maney DL, Maerz JC (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22:760–772CrossRefGoogle Scholar
  24. Deane EE, Woo NY (2009) Modulation of fish growth hormone levels by salinity, temperature, pollutants and aquaculture related stress: a review. Rev Fish Biol Fish 19:97–120CrossRefGoogle Scholar
  25. Deane EE, Woo NY (2011) Advances and perspectives on the regulation and expression of piscine heat shock proteins. Rev Fish Biol Fish 21:153–185CrossRefGoogle Scholar
  26. Di Marco P, DJ MK, Mandich A, Bronzi P, Cataldi E, Cataudella S (1999) Influence of sampling conditions on blood chemistry values of Adriatic sturgeon Acipenser naccarii (Bonaparte, 1836). J Appl Ichthyol 15:73–77CrossRefGoogle Scholar
  27. Di Marco P, Priori A, Finoia MG, Massari A, Mandich A, Marino G (2008) Physiological responses of European sea bass Dicentrarchus labrax to different stocking densities and acute stress challenge. Aquaculture 275:319–328CrossRefGoogle Scholar
  28. Di Marco P, Priori A, Finoia MG, Petochi T, Longobardi A, Donadelli V, Marino G (2011) Assessment of blood chemistry reference values for cultured sturgeon hybrids (Acipenser naccarii female × Acipenser baerii male). J Appl Ichthyol 27:584–590CrossRefGoogle Scholar
  29. Díaz ME, Furné M, Trenzado CE, García-Gallego M, Domezain A, Sanz A (2010) Antioxidant defences in the first life phases of the sturgeon Acipenser naccarii. Aquaculture 307:123–129CrossRefGoogle Scholar
  30. DiVincenti L, Wyatt J, Priest H, Dittman D, Klindt R, Gordon D, Preston A, Smith T, Bowman C (2012) Reference intervals for select hematologic and plasma biochemical analytes of wild Lake Sturgeon (Acipenser fulvescens) from the St. Lawrence River in New York. Vet Clin Pathol 42:19–26PubMedCrossRefGoogle Scholar
  31. Duncan IJH (2005) Science-based assessment of animal welfare: farm animals. Rev Sci Tech 24:483PubMedCrossRefGoogle Scholar
  32. Elia AC, Abete MC, Pacini N, Dörr AJM, Scanzio T, Prearo M (2014) Antioxidant biomarker survey ensuing long-term selenium withdrawal in Acipenser baeri fed se-cysteine diets. Environ Toxicol Pharmacol 37:1131–1139PubMedCrossRefGoogle Scholar
  33. Ellis T, Yildiz HY, López-Olmeda J, Spedicato MT, Tort L, Øverli Ø, Martins CIM (2012) Cortisol and finfish welfare. Fish Physiol Biochem 38:163–188PubMedCrossRefGoogle Scholar
  34. Eslamloo K, Falahatkar B (2014) Variations of some physiological and immunological parameters in Siberian sturgeon (Acipenser baerii, Brandt, 1869) subjected to an acute stressor. J Appl Anim Welf Sci 17:29–42PubMedCrossRefGoogle Scholar
  35. Eslamloo K, Falahatkar B, Yokoyama S (2012) Effects of dietary bovine lactoferrin on growth, physiological performance, iron metabolism and non-specific immune responses of Siberian sturgeon Acipenser baeri. Fish Shellfish Immunol 32:976–985CrossRefPubMedGoogle Scholar
  36. Falahatkar B, Eslamloo K, Yokoyama S (2014) Suppression of stress responses in siberian sturgeon, Acipenser baeri, juveniles by the dietary administration of bovine lactoferrin. J World Aquacult Soc 45:699–708CrossRefGoogle Scholar
  37. Feng G, Zhuang P, Zhang L, Kynard B, Shi X, Duan M, Liu J, Huang X (2011) Effect of anaesthetics MS-222 and clove oil on blood biochemical parameters of juvenile Siberian sturgeon (Acipenser baerii). J Appl Ichthyol 27:595–599CrossRefGoogle Scholar
  38. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247PubMedCrossRefGoogle Scholar
  39. Fontagné S, Bazin D, Brèque J, Vachot C, Bernarde C, Rouault T, Bergot P (2006) Effects of dietary oxidized lipid and vitamin a on the early development and antioxidant status of Siberian sturgeon (Acipenser baeri) larvae. Aquaculture 257:400–411CrossRefGoogle Scholar
  40. Gallo VP, Accordi F, Ohlberger J, Civinini A (2004) The chromaffin system of the beluga sturgeon Huso huso (Chondrostei): histological, immunohistochemical and ultrastructural study. Ital J Zool 71:279–285CrossRefGoogle Scholar
  41. Geraylou Z, Souffreau C, Rurangwa E, D’Hondt S, Callewaert L, Courtin CM, Delcour JA, Buyse J, Ollevier F (2012) Effects of arabinoxylan-oligosaccharides (AXOS) on juvenile Siberian sturgeon (Acipenser baerii) performance, immune responses and gastrointestinal microbial community. Fish Shellfish Immunol 33:718–724PubMedPubMedCentralCrossRefGoogle Scholar
  42. Geraylou Z, Souffreau C, Rurangwa E, De Meester L, Courtin CM, Delcour JA, Buyse J, Ollevier F (2013) Effects of dietary arabinoxylan-oligosaccharides (AXOS) and endogenous probiotics on the growth performance, non-specific immunity and gut microbiota of juvenile Siberian sturgeon (Acipenser baerii). Fish Shellfish Immunol 35:766–775PubMedPubMedCentralCrossRefGoogle Scholar
  43. Gisbert E, Rodrgı́uez A, Cardona L, Huertas M, Gallardo MA, Sarasquete C, Sala-Rabanal M, Ibarz A, Sánchez J, Castelló-Orvay F (2004) 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 239:141–154CrossRefGoogle Scholar
  44. Gomulka P, Własow T, Velíšek J, Svobodová Z, Chmielinska E (2008) Effects of Eugenol and MS-222 Anaesthesia on Siberian sturgeon Acipenser baerii Brandt. Acta Vet Brno 77:447–453CrossRefGoogle Scholar
  45. Hamlin HJ, Moore BC, Edwards TM, Larkin ILV, Boggs A, High WJ, Main KL, Guillette LJ Jr (2008) Nitrate-induced elevations in circulating sex steroid concentrations in female Siberian sturgeon (Acipenser baeri) in commercial aquaculture. Aquaculture 281:118–125CrossRefGoogle Scholar
  46. Han D, Huang SSY, Wang W-F, Deng D-F, Hung SSO (2012) Starvation reduces the heat shock protein responses in white sturgeon larvae. Environ Biol Fish 93:333–342CrossRefGoogle Scholar
  47. Harris J, Bird DJ (2000) Modulation of the fish immune system by hormones. Vet Immunol Immunopathol 77:163–176PubMedCrossRefGoogle Scholar
  48. He X, Zhuang P, Zhang L, Xie C (2009) Osmoregulation in juvenile Chinese sturgeon (Acipenser sinensis gray) during brackish water adaptation. Fish Physiol Biochem 35:223–230PubMedCrossRefGoogle Scholar
  49. Huntingford FA, Kadri S (2009) Taking account of fish welfare: lessons from aquaculture. J Fish Biol 75:2862–2867PubMedCrossRefGoogle Scholar
  50. Huntingford F, Kadri S (2014) Defining, assessing and promoting the welfare of farmed fish. Rev Sci Tech 33:233–244PubMedCrossRefGoogle Scholar
  51. 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
  52. Jeney G, Jeney Z (2002) Application of immunostimulants for modulation of the non-specific defense mechanisms in sturgeon hybrid: Acipenser ruthenus × A. baerii. J Appl Ichthyol 18:416–419CrossRefGoogle Scholar
  53. Johnson JL, Hintz WD, Garvey JE, Phelps QE, Tripp SJ (2014) Evaluating growth, survival and swimming performance to determine the feasibility of telemetry for age-0 pallid sturgeon (Scaphirhynchus albus). Am Midl Nat 171:68–77CrossRefGoogle Scholar
  54. Jollès P, Jollès J (1984) What’s new in lysozyme research? Mol Cell Biochem 63:165–189PubMedCrossRefGoogle Scholar
  55. Jolliffe I (2014) Principal component analysis. Wiley Stats Ref: Statistics Reference OnlineGoogle Scholar
  56. Kalmar B, Greensmith L (2009) Induction of heat shock proteins for protection against oxidative stress. Adv Drug Deliv Rev 61:310–318PubMedCrossRefGoogle Scholar
  57. Khoshbavar-Rostami HA, Soltani M, Hassan HMD (2007) Immune responses of great sturgeon Huso huso to Aeromonas hydrophila bacterin. J Fish Biol 70:1931–1938CrossRefGoogle Scholar
  58. Kita J, Itazawa Y (1990) Effects of adrenaline on the blood flow through the spleen of rainbow trout (Salmo gairdneri). Comp Biochem Physiol, Part A: Physiol 95:591–595CrossRefGoogle Scholar
  59. Knowles S, Hrubec TC, Smith SA, Bakal RS (2006) Hematology and plasma chemistry reference intervals for cultured shortnose sturgeon (Acipenser brevirostrum). Vet Clin Pathol 35:434–440PubMedCrossRefGoogle Scholar
  60. Kolman H (2001) The humoral effects of epin in Siberian sturgeon (Acipenser baeri Brandt). Arch Pol Fish 9:61–69Google Scholar
  61. Kolman H (2002) Primary humoral response in Siberian sturgeon after exposure to anti-furunculosis bacterin. Cz J Anim Sci 47:183–188Google Scholar
  62. Kolman H, Kolman R, Siwicki AK (1999a) Influence of bacterial antigens on specific and non-specific immune response in bester (Huso huso x Acipenser ruthenus) fry F3. Cz J Anim Sci 7:93–102Google Scholar
  63. Kolman I, Siwicki AK, Kolman R (1999b) Influence of O-antigen Aeromonas salmonicida on non specific and specific immune response in siberian sturgeon Acipenser baeri Brandt. Arch Pol Fish 7:93–102Google Scholar
  64. Kolman H, Kolman R, Siwicki AK (2000) Non-specific defence mechanisms of Russian sturgeon (Acipenser gueldenstaedti Brandt) reared in cages. Arch Pol Fish 8:181–192Google Scholar
  65. Korte SM, Olivier B, Koolhaas JM (2007) A new animal welfare concept based on allostasis. Physiol Behav 92:422–428PubMedCrossRefGoogle Scholar
  66. Kynard B, Horgan M (2002) Ontogenetic behavior and migration of atlantic sturgeon, Acipenser oxyrinchus oxyrinchus, and shortnose sturgeon, A. brevirostrum, with notes on social behavior. Environ Biol Fish 63:137–150CrossRefGoogle Scholar
  67. Lankford SE, Adams TE, Cech JJ (2003) Time of day and water temperature modify the physiological stress response in green sturgeon, Acipenser medirostris. Comp Biochem Physiol, Part A: Mol Integr Physiol 135:291–302CrossRefGoogle Scholar
  68. LeBlanc S, Höglund E, Gilmour KM, Currie S (2012) Hormonal modulation of the heat shock response: insights from fish with divergent cortisol stress responses. Am J Phys Regul Integr Comp Phys 302:R184–R192Google Scholar
  69. Lewis JM, Hori TS, Rise ML, Walsh PJ, Currie S (2010) Transcriptome responses to heat stress in the nucleated red blood cells of the rainbow trout (Oncorhynchus mykiss). Physiol Genomics 42:361–373PubMedCrossRefGoogle Scholar
  70. Linares-Casenave J, Werner I, Van Eenennaam JP, Doroshov SI (2013) Temperature stress induces notochord abnormalities and heat shock proteins expression in larval green sturgeon (Acipenser medirostris Ayres 1854). J Appl Ichthyol 29:958–967CrossRefGoogle Scholar
  71. Magnadóttir B (2006) Innate immunity of fish (overview). Fish Shellfish Immunol 20:137–151PubMedPubMedCentralCrossRefGoogle Scholar
  72. Martin I, Grotewiel MS (2006) Oxidative damage and age-related functional declines. Mech Ageing Dev 127:411–423PubMedCrossRefGoogle Scholar
  73. Martínez-Álvarez RM, Hidalgo MC, Domezain A, Morales AE, García-Gallego M, Sanz A (2002) Physiological changes of sturgeon Acipenser naccarii caused by increasing environmental salinity. J Exp Biol 205:3699–3706PubMedGoogle Scholar
  74. Martínez-Porchas M, Martínez-Córdova LR, Ramos-Enriquez R (2009) Cortisol and glucose: reliable indicators of fish stress. Pan-Am J Aquat Sci 4:158–178Google Scholar
  75. Martins CI, Galhardo L, Noble C, Damsgård B, Spedicato MT, Zupa W, Beauchaud M, Kulczykowska E, Massabuau J-C, Carter T et al (2012) Behavioural indicators of welfare in farmed fish. Fish Physiol Biochem 38:17–41PubMedCrossRefGoogle Scholar
  76. Matsche MA (2011) Evaluation of tricaine methanesulfonate (MS-222) as a surgical anesthetic for Atlantic sturgeon Acipenser oxyrinchus oxyrinchus. J Appl Ichthyol 27:600–610CrossRefGoogle Scholar
  77. Matsche MA, Rosemary KM, Brundage HM, O’Herron JC (2013) Hematology and plasma chemistry of wild shortnose sturgeon Acipenser brevirostrum from Delaware River, USA. J Appl Ichthyol 29:6–14CrossRefGoogle Scholar
  78. Matsche MA, Arnold J, Jenkins E, Townsend H, Rosemary K (2014) Determination of hematology and plasma chemistry reference intervals for 3 populations of captive Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus). Vet Clin Pathol 43:387–396PubMedCrossRefGoogle Scholar
  79. Maxime V, Nonnotte G, Peyraud C, Williot P, Truchot JP (1995) Circulatory and respiratory effects of an hypoxic stress in the Siberian sturgeon. Respir Physiol 100:203–212PubMedCrossRefGoogle Scholar
  80. McCormick SD (2001) Endocrine control of osmoregulation in teleost fish. Am Zool 41:781–794Google Scholar
  81. McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43:2–15PubMedCrossRefGoogle Scholar
  82. Metcalfe NB, Alonso-Alvarez C (2010) Oxidative stress as a life-history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Funct Ecol 24:984–996CrossRefGoogle Scholar
  83. Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 12:75–92PubMedCrossRefGoogle Scholar
  84. Morera D, MacKenzie SA (2011) Is there a direct role for erythrocytes in the immune response. Vet Res 42:89PubMedPubMedCentralCrossRefGoogle Scholar
  85. Ni M, Wen H, Li J, Chi M, Ren Y, Song Z, Ding H (2014) Two HSPs gene from juvenile Amur sturgeon (Acipenser schrenckii): cloning, characterization and expression pattern to crowding and hypoxia stress. Fish Physiol Biochem 40:1801–1816PubMedCrossRefGoogle Scholar
  86. Nicks B, Vandenheede M (2014) Animal health and welfare: equivalent or complementary? Rev Sci Tech 33:97–101PubMedCrossRefGoogle Scholar
  87. North BP, Turnbull JF, Ellis T, Porter MJ, Migaud H, Bron J, Bromage NR (2006) The impact of stocking density on the welfare of rainbow trout (Oncorhynchus mykiss). Aquaculture 255:466–479CrossRefGoogle Scholar
  88. OIE (2015) Aquatic Animal Health Code. http://www.oie.int/index.php?id=171&L=0&htmfile= preface.htm. Accessed 24 July 2015
  89. Pacini N, Elia AC, Abete MC, Dörr AJM, Brizio P, Gasco L, Righetti M, Prearo M (2013) Antioxidant response versus selenium accumulation in the liver and kidney of the Siberian sturgeon (Acipenser baeri). Chemosphere 93:2405–2412PubMedCrossRefGoogle Scholar
  90. Palikova M, Mareš J, Jirasek J et al (1999) Characteristics of leukocytes and thrombocytes of selected sturgeon species from intensive breeding. Acta Vet Brno 68:259–264CrossRefGoogle Scholar
  91. Pierson PM, Lamers A, Flik G, Mayer-Gostan N (2004) The stress axis, stanniocalcin, and ion balance in rainbow trout. Gen Comp Endocrinol 137:263–271PubMedCrossRefGoogle Scholar
  92. Prunet P, Øverli Ø, Douxfils J, Bernardini G, Kestemont P, Baron D (2012) Fish welfare and genomics. Fish Physiol Biochem 38:43–60PubMedCrossRefGoogle Scholar
  93. Quade MJ, Roth JA (1997) A rapid, direct assay to measure degranulation of bovine neutrophil primary granules. Vet Immunol Immunopathol 58:239–248PubMedCrossRefGoogle Scholar
  94. Roberts RJ, Agius C, Saliba C, Bossier P, Sung YY (2010) Heat shock proteins (chaperones) in fish and shellfish and their potential role in relation to fish health: a review. J Fish Dis 33:789–801PubMedCrossRefGoogle Scholar
  95. Rochard E, Castelnaud G, Lepage M (1990) Sturgeons (Pisces: Acipenseridae); threats and prospects. J Fish Biol 37:123–132CrossRefGoogle Scholar
  96. Rodríguez A, Gallardo MA, Gisbert E, Santilari S, Ibarz A, Sánchez J, Castelló-Orvay F (2002) Osmoregulation in juvenile Siberian sturgeon (Acipenser baerii). Fish Physiol Biochem 26:345–354CrossRefGoogle Scholar
  97. Rose JD, Arlinghaus R, Cooke SJ, Diggles BK, Sawynok W, Stevens ED, Wynne CDL (2014) Can fish really feel pain? Fish Fish 15:97–133CrossRefGoogle Scholar
  98. Sardella BA, Kültz D (2009) Osmo-and ionoregulatory responses of green sturgeon (Acipenser medirostris) to salinity acclimation. J Comp Physiol, Part B 179:383–390CrossRefGoogle Scholar
  99. Saurabh S, Sahoo PK (2008) Lysozyme: an important defence molecule of fish innate immune system. Aquac Res 39:223–239CrossRefGoogle Scholar
  100. Schreck CB (2010) Stress and fish reproduction: the roles of allostasis and hormesis. Gen Comp Endocrinol 165:549–556PubMedCrossRefGoogle Scholar
  101. Scott AP, Ellis T (2007) Measurement of fish steroids in water—a review. Gen Comp Endocrinol 153:392–400PubMedCrossRefGoogle Scholar
  102. Segner H, Sundh H, Buchmann K, Douxfils J, Sundell KS, 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 38:85–105PubMedCrossRefGoogle Scholar
  103. Sepúlveda MS, Sutton TM, Patrick HK, Amberg JJ (2012) Blood chemistry values for shovelnose and Lake sturgeon. J Aquat Anim Health 24:135–140PubMedCrossRefGoogle Scholar
  104. Shahsavani D, Mohri M, Kanani HG (2010) Determination of normal values of some blood serum enzymes in Acipenser stellatus Pallas. Fish Physiol Biochem 36:39–43PubMedCrossRefGoogle Scholar
  105. Shephard KL (1994) Functions for fish mucus. Rev Fish Biol Fish 4:401–429CrossRefGoogle Scholar
  106. Shi X, Li D, Zhuang P, Nie F, Long L (2006) Comparative blood biochemistry of Amur sturgeon, Acipenser schrenckii, and Chinese surgeon, Acipenser sinensis. Fish Physiol Biochem 32:63–66PubMedCrossRefGoogle Scholar
  107. Shi X, Zhuang P, Zhang L, Chen L, Xu B, Feng G, Huang X (2010) Optimal starvation time before blood sampling to get baseline data on several blood biochemical parameters in Amur sturgeon, Acipenser schrenckii. Aquac Nutr 16:544–548CrossRefGoogle Scholar
  108. Silvestre F, Linares-Casenave J, Doroshov SI, Kültz D (2010) A proteomic analysis of green and white sturgeon larvae exposed to heat stress and selenium. Sci Total Environ 408:3176–3188PubMedPubMedCentralCrossRefGoogle Scholar
  109. Simide R, Richard S, Prévot-D’Alvise N, Miard T, Gaillard S (2016) Assessment of the accuracy of physiological blood indicators for the evaluation of stress, health status and welfare in Siberian sturgeon (Acipenser baerii) subject to chronic heat stress and dietary supplementation. Int Aquat Res:1–15Google Scholar
  110. Sorci G, Faivre B (2009) Inflammation and oxidative stress in vertebrate host–parasite systems. Philos Trans R Soc B 364:71–83CrossRefGoogle Scholar
  111. Srivastava P (2002) Roles of heat-shock proteins in innate and adaptive immunity. Nat Rev Immunol 2:185–194PubMedCrossRefGoogle Scholar
  112. Tort L (2011) Stress and immune modulation in fish. Dev Comp Immunol 35:1366–1375PubMedCrossRefGoogle Scholar
  113. Turnbull J, Bell A, Adams C, Bron J, Huntingford F (2005) Stocking density and welfare of cage farmed Atlantic salmon: application of a multivariate analysis. Aquaculture 243:121–132CrossRefGoogle Scholar
  114. Veissier I, Boissy A (2007) Stress and welfare: two complementary concepts that are intrinsically related to the animal’s point of view. Physiol Behav 92:429–433PubMedCrossRefGoogle Scholar
  115. Volpato GL, Gonçalves-de-Freitas E, Fernandes-de-Castilho M (2007) Insights into the concept of fish welfare. Dis Aquat Org:165–171PubMedCrossRefGoogle Scholar
  116. Wang W, Deng D-F, Riu ND, Moniello G, Hung SS (2013) Heat shock protein 70 (HSP70) responses in tissues of white sturgeon and green sturgeon exposed to different stressors. N Am J Aquac 75:164–169CrossRefGoogle Scholar
  117. Warren DE, Matsumoto S, Roessig JM, Cech JJ (2004) Cortisol response of green sturgeon to acid-infusion stress. Comp Biochem Physiol, Part A: Mol Integr Physiol 137:611–618CrossRefGoogle Scholar
  118. Webb MAH, Allert JA, Kappenman KM, Marcos J, Feist GW, Schreck CB, Shackleton CH (2007) Identification of plasma glucocorticoids in pallid sturgeon in response to stress. Gen Comp Endocrinol 154:98–104PubMedCrossRefGoogle Scholar
  119. Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625PubMedCrossRefGoogle Scholar
  120. Whyte SK (2007) The innate immune response of finfish—a review of current knowledge. Fish Shellfish Immunol 23:1127–1151PubMedCrossRefGoogle Scholar
  121. Williot P (1997) Reproduction de l’esturgeon sibérien (Acipenser baerii Brandt) en élevage: gestion des génitrices, compétence à la maturation in vitro de follicules ovariens et caractéristiques plasmatiques durant l’induction de la ponte. Thèse no 1822, Université Bordeaux 1Google Scholar
  122. Williot P, Comte S, Le Menn F (2011) Stress indicators throughout the reproduction of farmed Siberian sturgeon Acipenser baerii (Brandt) females. Int Aquat Res 3:31–43Google Scholar
  123. Wood AW, Duan C, Bern HA (2005) Insulin-like growth factor signaling in fish. Int Rev Cytol 243:215–285PubMedCrossRefGoogle Scholar
  124. Xie Z, Niu C, Zhang Z, Bao L (2006) Dietary ascorbic acid may be necessary for enhancing the immune response in Siberian sturgeon (Acipenser baerii), a species capable of ascorbic acid biosynthesis. Comp Biochem Physiol, Part A: Mol Integr Physiol 145:152–157CrossRefGoogle Scholar
  125. Zahl IH, Samuelsen O, Kiessling A (2012) Anaesthesia of farmed fish: implications for welfare. Fish Physiol Biochem 38:201–218PubMedCrossRefGoogle Scholar
  126. Zheng K, Wang W, Hung SS, Deng D-F (2015) Feeding rates affect expression of heat-shock protein 70 in green sturgeon fry. N Am J Aquac 77:206–210CrossRefGoogle Scholar
  127. Zhu L, Nie L, Zhu G, Xiang L, Shao J (2013) Advances in research of fish immune-relevant genes: a comparative overview of innate and adaptive immunity in teleosts. Dev Comp Immunol 39:39–62PubMedCrossRefGoogle Scholar
  128. Zubair SN, Peake SJ, Hare JF, Anderson WG (2012) The effect of temperature and substrate on the development of the cortisol stress response in the lake sturgeon, Acipenser fulvescens, Rafinesque (1817). Environ Biol Fish 93:577–587CrossRefGoogle Scholar
  129. Zuccarelli MD, Kusakabe M, Nakamura I, Prentice EF, Young G, Ingermann RL (2008) Acute stress response of Kootenai River white sturgeon Acipenser transmontanus Richardson reflected in peritoneal fluid and blood plasma. J Fish Biol 72:1831–1840CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Rémy Simide
    • 1
  • Sandrine Gaillard
    • 2
  • Simone Richard
    • 3
  1. 1.Institut océanographique Paul RicardSix Fours Les PlagesFrance
  2. 2.Laboratoire Protee, Plateforme BioTechServicesUniversité de Toulon, Campus de la GardeToulon Cedex 9France
  3. 3.Laboratoire Protee, Equipe de Biologie Moléculaire MarineUniversité de Toulon, Campus de la GardeToulon Cedex 9France

Personalised recommendations