Advertisement

Fish response to hypoxia stress: growth, physiological, and immunological biomarkers

  • Mohsen Abdel-TawwabEmail author
  • Mohamed N. Monier
  • Seyed Hossein Hoseinifar
  • Caterina Faggio
Article

Abstract

Water quality encompasses the water physical, biological, and chemical parameters. It generally affects the fish growth and welfare. Thus, the success of a commercial aquaculture project depends on supplying the optimum water quality for prompt fish growth at the minimum cost of resources. Although the aquaculture environment is a complicated system, depending on various water quality variables, only less of them have a critical role. One of these vital parameters is dissolved oxygen (DO) level, which requires continuous oversight in aquaculture systems. In addition, the processes of natural stream refinement require suitable DO levels in order to extend for aerobic life forms. The depletion of DO concentration (called hypoxia) in pond water causes great stress on fish where DO levels that remain below 1–2 mg/L for a few hours can adversely affect fish growth resulting in fish death. Furthermore, hypoxia has substantial effects on fish physiological and immune responses, making them more susceptible to diseases. Therefore, to avoid disease outbreak in modern aquaculture production systems where fish are intensified and more crowded, increasing attention should be taken into account on DO levels.

Keywords

Fish Hypoxia Performance Innate immunity Oxidative stress Biomarkers 

Notes

References

  1. Abdel-Tawwab M (2016) Effect of feed availability on susceptibility of Nile tilapia, Oreochromis niloticus (L.) to environmental zinc toxicity: growth performance, biochemical response, and zinc bioaccumulation. Aquaculture 464:309–315CrossRefGoogle Scholar
  2. Abdel-Tawwab M, Wafeek M (2017) Fluctuations in water temperature affected waterborne cadmium toxicity: hematology, anaerobic glucose pathway, and oxidative stress status of Nile tilapia, Oreochromis niloticus (L.). Aquaculture 477:106–111CrossRefGoogle Scholar
  3. Abdel-Tawwab M, Hagras AE, Elbaghdady HM, Monier MN (2014) Dissolved oxygen level and stocking density effects on growth, feed utilization, physiology, and innate immunity of Nile tilapia, Oreochromis niloticus. J Appl Aquac 26:340–355CrossRefGoogle Scholar
  4. Abdel-Tawwab M, Hagras AE, Elbaghdady HM, Monier MN (2015) Effects of dissolved oxygen and fish size on Nile tilapia, Oreochromis niloticus (L.): growth performance, whole-body composition, and innate immunity. Aquac Int 23:1261–1274CrossRefGoogle Scholar
  5. Aboagye DL, Allen PJ (2018) Effects of acute and chronic hypoxia on acid-base regulation, hematology, ion, and osmoregulation of juvenile American paddlefish. J Comp Physiol B 188(1):77–88CrossRefPubMedGoogle Scholar
  6. Acerete L, Balasch JC, Espinosa E, Josa A, Tort L (2004) Physiological responses in Eurasian perch (Perca fluviatilis, L.) subjected to stress by transport and handling. Aquaculture 237:167–178CrossRefGoogle Scholar
  7. Affonso EG, Polez VL, Correa CF, Mazon AF, Araujo MR, Moraes G, Rantin FT (2002) Blood parameters and metabolites in the teleost fish Colossoma macropomum exposed to sulfide or hypoxia. Comp Biochem Physiol (C) 133:375–382Google Scholar
  8. Aliko V, Qirjo M, Sula E, Morina V, Faggio C (2018) Antioxidant defense system, immune response and erythron profile modulation in gold fish, Carassius auratus, after acute manganese treatment. Fish Shellfish Immunol 76:101–109CrossRefPubMedGoogle Scholar
  9. Al-Salahy MB (2006) Studies on the effect of hypoxic water on lipid peroxidation, DNA fragmentation and haematological responses in the catfish, Clarias gariepinus. J Egypt Ger Soc Zool 49:203–218Google Scholar
  10. Araújo-Luna R, Ribeiro L, Bergheim A, Pousão-Ferreira P (2018) The impact of different rearing condition on gilthead seabream welfare: dissolved oxygen levels and stocking densities. Aquac Res 49:3845–3855CrossRefGoogle Scholar
  11. Arend KK, Beletsky D, DePinto JV, Ludsin SA, Roberts JJ, Rucinski DK, Scavia D, Schwab DJ, Höök TO (2011) Seasonal and interannual effects of hypoxia on fish habitat quality in Central Lake Erie. Freshw Biol 56(2):366–383CrossRefGoogle Scholar
  12. Barcellos LJG, Kreutz LC, de Souza C, Rodrigues LB, Fioreze I, Quevedo RM, Cericato L, Soso AB, Fagundes M, Conrad J, Lacerda LA, Terra S (2004) Hematological changes in jundià (Rhamida quelen Quoy and Gaimard Pimelodidae) after acute and chronic stress caused by usual aquacultural management, with emphasis on immunosuppressive effects. Aquaculture 237:229–236CrossRefGoogle Scholar
  13. Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42(3):517–525CrossRefPubMedGoogle Scholar
  14. Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Ann Rev Fish Dis 10:3–26CrossRefGoogle Scholar
  15. Bartoskova M, Dobsikova R, Stancova V, Zivna D, Blahova J, Marsalek P, Zelnickova L, Bartos M, Di Tocco FC, Faggio C (2013) Evaluation of ibuprofen toxicity for zebrafish (Danio rerio) targeting on selected biomarkers of oxidative stress. Neuro Endocrinol Lett 34:102–108PubMedGoogle Scholar
  16. Bartrons R, Caro J (2007) Hypoxia, glucose metabolism and the Warburg’s effect. J Bioenerg Biomembr 39:223–229CrossRefPubMedGoogle Scholar
  17. Bera A, Sawant PB, Dasgupta S, Chadha NK, Sawant BT, Pal AK (2017) Diel cyclic hypoxia alters plasma lipid dynamics and impairs reproduction in goldfish (Carassius auratus). Fish Physiol Biochem 43:1677–1688CrossRefPubMedGoogle Scholar
  18. Bernier NJ, Craig PM (2005) CRF-related peptides contribute to stress response and regulation of appetite in hypoxic rainbow trout. Am J Physiol Regul Integr Comp Physiol 289:982–990CrossRefGoogle Scholar
  19. Bernier NJ, Gorissen M, Flik G (2012) Differential effects of chronic hypoxia and feed restriction on the expression of leptin and its receptor, food intake regulation and the endocrine stress response in common carp. J Exp Biol 215:2273–2282CrossRefPubMedGoogle Scholar
  20. Boeuf G, Payan P (2001) How should salinity influence fish growth? Comp Biochem Phys (C) 130:411–423Google Scholar
  21. Boleza KA, Burnett LE, Burnett KG (2001) Hypercapnic hypoxia compromises bactericidal activity of fish anterior kidney cells against opportunistic environmental pathogens. Fish Shellfish Immunol 11:593–610CrossRefPubMedGoogle Scholar
  22. Booth JH (1978) The distribution of blood flow in the gills of fish: application of a new technique to rainbow trout (Salmo gairdneri). J Exp Biol 73:119–129Google Scholar
  23. Bowyer JN, Booth MA, Qin JG, D’Antignana T, Thomson MJS, Stone DAJ (2014) Temperature and dissolved oxygen influence growth and digestive enzyme activities of yellowtail kingfish Seriola lalandi (Valenciennes, 1833). Aquac Res 45:2010–2020CrossRefGoogle Scholar
  24. Brauner CJ (1999) The effect of diet and short duration hyperoxia exposure on seawater transfer in coho salmon smolts (Oncorhynchus kishutch). Aquaculture 177:257–265CrossRefGoogle Scholar
  25. Brauner CJ, Seidelin M, Madsen SS, Jensen FB (2000) Effect of freshwater hyperoxia and hypercapnia and their influences on subsequent seawater transfer in Atlantic salmon (Salmo salar) smolts. Can J Fish Aquat Sci 57:2054–2064CrossRefGoogle Scholar
  26. Breitburg DL (2002) Effects of hypoxia, and the balance between hypoxia and enrichment, on coastal fishes and fisheries. Estuaries 25:767–781CrossRefGoogle Scholar
  27. Brett JR (1979) Environmental factors and growth. In: Fish physiology, vol. VIII. In: Hoar WS, Randall DJ, Brett JR (eds) Academic Press, New York, p 599–675Google Scholar
  28. Brett JR, Blackburn JM (1981) Oxygen requirements for growth of young coho (Oncorhynchus kisutch) and sockeye (O. nerka) salmon at 15 °C. Can J Fish Aquat Sci 38:399–404CrossRefGoogle Scholar
  29. Buentello JA, Gatlin DM III, Neill WH (2000) Effects of water temperature and dissolved oxygen on daily feed consumption, feed utilization and growth of channel catfish (Ictalurus punctatus). Aquaculture 182:339–352CrossRefGoogle Scholar
  30. Bunch EC, Bejerano I (1997) The effect of environmental factors on the susceptibility of hybrid tilapia Oreochromis niloticus x O. aures to streptococcosis. Isr J Aquacult 49:67–76Google Scholar
  31. Burgos-Aceves MA, Cohen A, Smith Y, Faggio C (2018) MicroRNAs and their role on fish oxidative stress during xenobiotic environmental exposures. Ecotoxicol Environ Saf 148:995–1000CrossRefGoogle Scholar
  32. Bushnell PG, Brill RW (1992) Oxygen transport and cardiovascular responses in skipjack tuna (Katsuwonus pelamis) and yellowfin tuna (Thunnus albacares) exposed to acute hypoxia. J Comp Physiol B 162:131–143CrossRefPubMedGoogle Scholar
  33. Cadiz L, Zambonino-Infante JL, Quazuguel P, Madec L, Le Delliou H, Mazurais D (2017) Metabolic response to hypoxia in European sea bass (Dicentrarchus labrax) displays developmental plasticity. Comp Biochem Physiol (B) 215:1–9CrossRefGoogle Scholar
  34. Caldwell CA, Hinshaw J (1994) Physiological and haematological responses in rainbow trout subjected to supplemental dissolved oxygen in fish culture. Aquaculture 126:183–193CrossRefGoogle Scholar
  35. Campbell NA (1990) Biology. Circulation and gas exchange. Chapter 38. Benjamin/Cummings Publishing Company, Redwood City, pp 683–705Google Scholar
  36. Cecchini S, Caputo AR (2003) Acid-base balance in sea bass (Dicentrarchus labrax, L.) in relation to water oxygen concentration. Aquac Res 34:1069–1073CrossRefGoogle Scholar
  37. Cecchini S, Saroglia M (2002) Antibody response in sea bass Dicentrarchus labrax (L.) in relation to water temperature and oxygenation. Aquac Res 33:607–613CrossRefGoogle Scholar
  38. Chabot D, Claireaux G (2008) Environmental hypoxia as a metabolic constraint on fish: the case of Atlantic cod, Gadus morhua. Mar Poll Bull 57:287–294CrossRefGoogle Scholar
  39. Chen JM, Cutler C, Jacques C, Boeuf G, Denamur E, Lecointre G, Mercier B, Cramb G, Ferec C (2001) A combined analysis of the cystic fibrosis transmembrane conductance regulator: implications for structure and diseases model. Mol Biol Evol 18:1771–1778CrossRefPubMedGoogle Scholar
  40. Cnaani A, Tinman S, Avidar Y, Ron M, Hulata G (2004) Comparative study of biochemical parameters in response to stress in Oreochromis aureus, O. mossambicus and two strains of O. niloticus. Aquac Res 35:1434–1440CrossRefGoogle Scholar
  41. Cook DG, Herbert NA (2012) The physiological and behavioural response of juvenile kingfish (Seriola lalandi) differs between escapable and inescapable progressive hypoxia. J Exp Mar Biol Ecol 413:138–144CrossRefGoogle Scholar
  42. Cooper RU, Clough LM, Farwell MA, West TL (2002) Hypoxia-induced metabolic and antioxidant enzymatic activities in the estuarine fish Leiostomus xanthurus. J Exp Mar Biol Ecol 279:1–20CrossRefGoogle Scholar
  43. Cossins AR, Crawford DL (2005) Fish as models for environmental genomics. Nat Rev Genet 6:324–333CrossRefPubMedGoogle Scholar
  44. Cuesta A, Esteban MA, Meseguer J (2003) Effects of different stressor agents on gilthead seabream natural cytotoxic activity. Fish Shellfish Immunol 15:433–441CrossRefPubMedGoogle Scholar
  45. Delaney MA, Klesius PH (2004) Hypoxic conditions induce Hsp70 production in blood, brain and head kidney of juvenile Nile tilapia Oreochromis niloticus (L.). Aquaculture 236:633–644CrossRefGoogle Scholar
  46. 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
  47. Domenici P, Steffensen JF, Marras S (2017) The effect of hypoxia on fish schooling. Philos Trans Soc B 372:236–249CrossRefGoogle Scholar
  48. Douxfils J, Deprez M, Mandiki SNM, Milla S, Henrotte E, Mathieu C, Silvestre F, Vandecan M, Rougeot C, Mélard C, Dieu M, Raes M, Kestemont P (2012) Physiologic al and proteomic responses to single and repeated hypoxia in juvenile Eurasian perch under domestication- clues to physiological acclimation and humoral immune modulations. Fish Shellfish Immunol 33:1112–1122CrossRefPubMedGoogle Scholar
  49. Duan Y, Dong X, Zhang X, Miao Z (2011) Effects of dissolved oxygen concentration and stocking density on the growth, energy budget and body composition of juvenile Japanese flounder, Paralichthys olivaceus (Temminck et Schlegel). Aquac Res 42:407–416CrossRefGoogle Scholar
  50. Duthie GG, Hughes GM (1987) The effect of reduced gill area and hyperoxia on oxygen consumption and swimming speed of rainbow trout. J Exp Biol 127:349–354Google Scholar
  51. Evans DH (1993) Osmotic and ionic regulation. In: Evans DH (ed) The physiology of fishes. CRC Press, Boca Raton, pp 315–341Google Scholar
  52. Evans JJ, Shoemaker CA, Klesius PH (2003) Effects of sublethal dissolved oxygen stress on blood glucose and susceptibility to Streptococcus agalactiae in Nile tilapia Oreochromis niloticus. J Aquat An Health 15:202–208CrossRefGoogle Scholar
  53. Faggio C, Pagano M, Alampi R, Vazzana I, Felice MR (2016) Cytotoxicity, haemolymphatic parameters, and oxidative stress following exposure to sub-lethal concentrations of quaternium-15 in Mytilus galloprovincialis. Aquat Toxicol 180:258265CrossRefGoogle Scholar
  54. Faggio C, Tsarpali V, Dailianis S (2018) Mussel digestive gland as a model for assessing xenobiotics: an overview. Sci Total Environ 613:220–229CrossRefGoogle Scholar
  55. Fazio F, Faggio C, Marafioti S, Torre A, Sanfilippo M, Piccione G (2012) Comparative study of haematological profile on Gobius niger in two different habitat sites: Faro Lake and Tyrrhenian Sea. Cah Biol Mar 53:213–219Google Scholar
  56. Fitzgibbon QP, Strawbridge A, Seymour RS (2007) Metabolic scope, swimming performance and the effects of hypoxia in the mulloway, Argyrosomus japonicus (Pisces: Scianeidae). Aquaculture 270:358–368CrossRefGoogle Scholar
  57. Foss A, Evensen TH, Oiestad V (2002) Effects of hypoxia and hyperoxia on growth and food conversion efficiency in the spotted wolfish Anarhichas minor (Olafsen). Aquac Res 33:437–444CrossRefGoogle Scholar
  58. Fukuda Y, Maita M, Satoh K, Okamoto N (1997) Influence of dissolved oxygen concentration on the mortality of yellowtail experimentally infected with Enterococcus seriolicida. Fish Pathol 32:129–130CrossRefGoogle Scholar
  59. Gallage S, Katagiri T, Endo M, Futami K, Endo M, Maita M (2016) Influence of moderate hypoxia on vaccine efficacy against Vibrio anguillarum in Oreochromis niloticus (Nile tilapia). Fish Shellfish Immunol 51:271–281CrossRefPubMedGoogle Scholar
  60. Gallage S, Katagiri T, Endo M, Maita M (2017) Comprehensive evaluation of immunomodulation by moderate hypoxia in S. agalactiae vaccinated Nile tilapia. Fish Shellfish Immunol 66:445–454CrossRefPubMedGoogle Scholar
  61. Gan L, Liu YJ, Tian LX, Yue YR, Yang HJ, Liu FJ, Chen YJ, Liang GY (2013) Effect of dissolved oxygen and dietary lysine levels on growth performance, feed conversion ratio and body composition of grass carp, Ctenopharyngodon idella. Aquacult Nut 19:860–869CrossRefGoogle Scholar
  62. Genz J, Jyde MB, Svendsen JC, Steffensen JF, Ramløv H (2013) Excess post-hypoxic oxygen consumption is independent from lactate accumulation in two cyprinid fishes. Comp Biochem Physiol (A) 165:54–60CrossRefGoogle Scholar
  63. Glass ML, Andersen NA, Kruhoffer M, Williams EM, Heisler N (1990) Combined effects of environmental PO2 and temperature on ventilation and blood gases in the carp Cyprinus carpio L. J Exp Biol 148:1–17Google Scholar
  64. Gobi N, Vaseeharan B, Rekha R, Vijayakumar S, Faggio C (2018) Bioaccumulation, cytotoxicity and oxidative stress of the acute exposure selenium in Oreochromis mossambicus. Ecotoxicol Environ Saf 162:147–159CrossRefPubMedGoogle Scholar
  65. Gracey A, Troll J, Somero G (2001) Hypoxia-induced gene expression profiling in the euryoxic fish Gillichthys mirabilis. Proc Natl Acad Sci U S A 98:1993–1998CrossRefPubMedPubMedCentralGoogle Scholar
  66. Grau EG, Richman NH III, Borski RJ (1994) Osmoreception and a simple endocrine reflex of the prolactin cell of tilapia Oreochromis mossambicus. In: Davey KG, Peter RE, Tobe SS (eds) Perspectives in comparative endocrinology. National Research Council of Canada, Ottawa, pp 251–256Google Scholar
  67. Greaney GS, Place AR, Cashon RE, Smith G, Powers DA (1980) Time course of changes in enzyme activities and blood respiratory properties of killifish during long-term acclimation to hypoxia. Physiol Zool 53:136–144CrossRefGoogle Scholar
  68. Greco AM, Fenwick JC, Perry SF (1996) The effects of soft-water acclimatation on gill structure in rainbow trout Oncorhynchus mykiss. Cell Tiss Res 285:75–82.Google Scholar
  69. Guan W-Z, Guo D-D, Sun Y-W, Chen J, Jiang X-Y, Zou S-M (2017) Characterization of duplicated heme oxygenase-1 genes and their responses to hypoxic stress in blunt snout bream (Megalobrama amblycephala). Fish Physiol Biochem 43:641–651CrossRefPubMedGoogle Scholar
  70. Guo Z, Cui J, Li M, Liu H, Zhang M, Meng F, Shi G, Wang R, He X, Zhao Y (2018) Effect of feeding frequency on growth performance, antioxidant status, immune response and resistance to hypoxia stress challenge on juvenile dolly varden char Salvelinus malma. Aquaculture 486:197–201CrossRefGoogle Scholar
  71. Hansen TJ, Olsen RE, Stien L, Oppedal F, Torgersen T, Breck O, Remen M, Vagseth T, Fjelldal G (2015) Effect of water oxygen level on performance of diploid and triploid Atlantic salmon post-smolts reared at high temperature. Aquaculture 435:354–360CrossRefGoogle Scholar
  72. Henriksson P, Mandic M, Richards JG (2008) The osmoregulatory compromise in sculpin: impaired gas exchange is associated with freshwater tolerance. Physiol Biochem Zool 81:310–319CrossRefPubMedGoogle Scholar
  73. Henrique M, Gomes E, Gouillou-Coustans M, Oliva-Teles A, Davies S (1998) Influence of supplementation of practical diets with vitamin C on growth and response to hypoxic stress of seabream, Sparus aurata. Aquaculture 161:415–426CrossRefGoogle Scholar
  74. Hughes GM (1984) General anatomy of the gills. In: Hoar WS, Randall DJ (eds) Fish Physiology, vol 10. Academic Press, San Diego, pp 1–72Google Scholar
  75. Hughes GM, Morgan M (1973) The structure of gills in relation to their respiratory function. Biol Rev 48:419–475CrossRefGoogle Scholar
  76. Imsland AK, Foss A, Gunnarsson S, Berntssen MHG, FitzGerald R, Bonga SW, Ham EV, Nævdal G, Stefansson SO (2001) The interaction of temperature and salinity on growth and food conversion in juvenile turbot (Scophthalmus maximus). Aquaculture 198:353–367CrossRefGoogle Scholar
  77. Ishibashi Y, Ekawa H, Hirata H, Kumai H (2002) Stress response and energy metabolism in various tissues of Nile tilapia Oreochromis niloticus exposed to hypoxic conditions. Fish Sci 68:1374–1383CrossRefGoogle Scholar
  78. Israeli D, Kimmel E (1996) Monitoring the behaviour of hypoxia-stressed Carassius auratus using computer vision. Aquac Eng 15:423–440CrossRefGoogle Scholar
  79. Jha AR, Miles CM, Lippert NR, Brown CD, White KP, Martin K (2015) Whole-genome re-sequencing of experimental populations reveals polygenic basis of egg-size variation in Drosophila melanogaster. Mol Biol Evol 32(10):2616–2632CrossRefPubMedPubMedCentralGoogle Scholar
  80. Jobling M (1994) Fish bioenergetics. Chapman and Hall, London 309 ppGoogle Scholar
  81. Jobling M (1995) The influence of environmental temperature on growth and conversion efficiency in fish. Causes of observed variations in fish growth. ICES 1-25 C.M./P:4Google Scholar
  82. Johnston IA, Bernard LM (1982) Ultrastructure and metabolism of skeletal muscle fibres in the tench: effects of long-term acclimation to hypoxia. Cell Tissue Res 227:179–199PubMedGoogle Scholar
  83. Kestemont P, Baras E (2001) Environmental factors and feed intake: mechanisms and interactions. In: Houlihan DF, Boujard T, Jobling M (eds) Food intake in fish. Blackwell Science, Oxford, pp 131–156CrossRefGoogle Scholar
  84. Kisia SM, Hughes GM (1992) Estimation of oxygen-diffusing capacity of different sizes of a tilapia, Oreochromis niloticus. J Zool London 227:405–415CrossRefGoogle Scholar
  85. Kisia SM, Hughes GM (1993) Routine oxygen consumption in different size of a tilapia, Oreochromis niloticus (Trewavas) using the closed chamber respiratory method. Acta Biol Hun 44:367–374Google Scholar
  86. Kraemer LD, Schulte PM (2004) Prior PCB exposure suppresses hypoxia-induced up-regulation of glycolytic enzymes in Fundulus heteroclitus. Comp Biochem Physiol C 139:23–39Google Scholar
  87. Kvamme BO, Gadan K, Finne-Fridell F, Niklasson L, Sundh H, Sundell K, Taranger GL, Evensen Ø (2013) Modulation of innate immune responses in Atlantic salmon by chronic hypoxia-induced stress. Fish Shellfish Immunol 34:55–65CrossRefPubMedGoogle Scholar
  88. Law SHW, Wu RSS, Ng PKS, Yu RMK, Kong RYC (2006) Cloning and expression analysis of two distinct HIF-alpha isoforms - gcHIF-1alpha and gcHIF-4alpha - from the hypoxia-tolerant grass carp, Ctenopharyngodon idellus. BMC Mol Biol 7:15CrossRefPubMedPubMedCentralGoogle Scholar
  89. Lays N, Iversen MMT, Frantzen M, Jorgensen EH (2009) Physiological stress responses in spotted wolfish (Anarhichas minor) subjected to acute disturbance and progressive hypoxia. Aquaculture 295:126–133CrossRefGoogle Scholar
  90. Li M, Wang X, Qi C, Li E, Du Z, Qin JG, Chen L (2018) Metabolic response of Nile tilapia (Oreochromis niloticus) to acute and chronic hypoxia stress. Aquaculture 495:187–195CrossRefGoogle Scholar
  91. Lovell T (1998) Nutritional and feeding of fish, 2nd edn. Kluwer Academic Publishers, DordrechtCrossRefGoogle Scholar
  92. Lushchak VI, Bagnyukova TV, Lushchak OV, Storey JM, Storey KB (2005) Hypoxia and recovery perturb free radical processes and antioxidant potential in common carp (Cyprinus carpio) tissues. Int J Biochem Cell Biol 37:1319–1330CrossRefPubMedGoogle Scholar
  93. Mahfouz ME, Hegazi MM, El-Magd MA, Kasem EA (2015) Metabolic and molecular responses in Nile tilapia, Oreochromis niloticus during short and prolonged hypoxia. Mar Freshw Behav Physiol 48(5):319–340CrossRefGoogle Scholar
  94. Majmundar AJ, Wong WJ, Simon MC (2010) Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell 40:294–309CrossRefPubMedPubMedCentralGoogle Scholar
  95. Mallya YJ (2007) The effects of dissolved oxygen on fish growth in aquaculture. The United Nations University fisheries training programmer, Final project, pp 30Google Scholar
  96. Marshall WS, Embherley TR, Singer TD, Bryson SE, McCormick SD (1999) Time course of salinity adaptation in a strongly euryhaline estuarine teleost, Fundulus heteroclitus: a multivariable approach. J Exp Biol 202:1535–1544PubMedGoogle Scholar
  97. Martinez ML, Landry C, Boehm R, Manning S, Cheek AO, Rees BB (2006) Effects of long-term hypoxia on enzymes of carbohydrate metabolism in the Gulf killifish, Fundulus grandis. J Exp Biol 209:3851–3861CrossRefPubMedGoogle Scholar
  98. Martínez ML, Raynard EL, Rees BB, Chapman LJ (2011) Oxygen limitation and tissue metabolic potential of the African fi sh Barbus neumayeri: roles of native habitat and acclimatization. BMC Ecol 11:1–8CrossRefGoogle Scholar
  99. Maxime V, Nonnotte G, Peyraud C, Williot P, Truchot JP (1995) Circulatory and respiratory effects of an hypoxic stress in the Siberian sturgeon. Res Physiol 100:203–212CrossRefGoogle Scholar
  100. Milla S, Mathieu C, Wang N, Lambert S, Nadzialek S, Massart S, Henrotte E, Douxfils J, Mélard C, Mandiki SN, Kestemont P (2010) Spleen immune status is affected after acute handling stress but not regulated by cortisol in Eurasian perch, Perca fluviatilis. Fish Shellfish Immunol 28:931–941CrossRefPubMedGoogle Scholar
  101. Mohindra V, Tripathi RK, Singh RK, Lal KK (2013) Molecular characterization and expression analysis of three hypoxia-inducible factor alpha subunits, HIF-1α, −2α and -3α in hypoxia-tolerant Indian catfish, Clarias batrachus (Linnaeus, 1758). Mol Biol Rep 40:5805–5815CrossRefPubMedGoogle Scholar
  102. Mohindra V, Tripathi RK, Singh A, Patangia R, Singh RK, Lal KK, Jena JK (2016) Hypoxic stress-responsive genes in air breathing catfish, Clarias magur (Hamilton 1822) and their possible physiological adaptive function. Fish Shellfish Immunol 59:46–56CrossRefPubMedGoogle Scholar
  103. Morgan JD, Iwama GK (1999) Energy cost of NaCl transport in isolated gills of cutthroat trout. Am J Phys 277:631–639Google Scholar
  104. Muusze B, Marcon J, van den Thillart G, Almeida-Val V (1998) Hypoxia tolerance of Amazon fish respirometry and energy metabolism of the cichlid Astronotus Ocellatus. Comp Biochem Physiol (A) 120:151–156CrossRefGoogle Scholar
  105. Ni M, Wen H, Li J, Chi M, Bu Y, Ren Y, Zhang M, Song Z, Ding H (2014) The physiological performance and immune responses of juvenile Amur sturgeon (Acipenser schrenckii) to stocking density and hypoxia stress. Fish Shellfish Immunol 36:325–335CrossRefPubMedGoogle Scholar
  106. Nikinmaa M (2002) Oxygen-dependent cellular functions-why fishes and their aquatic environment are a prime choice of study. Comp Biochem Physiol (A) 133:1–16CrossRefGoogle Scholar
  107. Nilsson S (1986) Control of gill blood flow. In: Nilsson S, Holmgren S (eds) Fish physiology: recent advances. Croom Helm, London, pp 86–101CrossRefGoogle Scholar
  108. Nilsson GE (2007) Gill remodeling in fish – a new fashion or an ancient secret? J Exp Biol 210:2403–2409CrossRefPubMedGoogle Scholar
  109. Null SE, Mouzon NR, Elmore LR (2017) Dissolved oxygen, stream temperature, and fish habitat response to environmental water purchases. J Environ Manag 197:559–570CrossRefGoogle Scholar
  110. Olson KR (1991) Vasculature of the fish gill: anatomical correlates of physiological functions. J Elect Technol 19:389–405CrossRefGoogle Scholar
  111. Ortiz-Barahona A, Villar D, Pescador N, Amigo J, del Peso L (2010) Genome-wide identification of hypoxia-inducible factor binding sites and target genes by a probabilistic model integrating transcription-profiling data and in silico binding site prediction. Nucl Acids Res 38:2332–2345CrossRefPubMedGoogle Scholar
  112. Ortuno J, Esteban MA, Meseguer J (2002) Lack of effect of combining different stressors on innate immune responses of seabream. Vet Immunol Immunopathol 84:17–27CrossRefPubMedGoogle Scholar
  113. Papoutsoglou SE, Tziha G (1996) Blue tilapia (Oreochromis aureus) growth rate in relation to dissolved oxygen concentration under recirculated water conditions. Aquac Eng 15:181–192CrossRefGoogle Scholar
  114. Perry SF, McDonald G (1993) Gas Exchange. In: Evans DH (ed) The physiology of fishes. CRC Press, Boca Raton, pp 251–278Google Scholar
  115. Pichavant K, Person-Le-Ruyet J, Le Bayon N, Severe A, Le Roux A, Quemener L, Maxime V, Nonnotte G, Boeuf G (2000) Effects of hypoxia on growth and metabolism of juvenile turbot. Aquaculture 188:103–114CrossRefGoogle Scholar
  116. Pichavant K, Person-Le-Ruyet J, Le Bayon N, Severe A, Le Roux A, Boeuf G (2001) Comparative effects of long-term hypoxia on growth, feeding and oxygen consumption in juvenile turbot and European sea bass. J Fish Biol 59:875–883CrossRefGoogle Scholar
  117. Pichavant K, Maxime V, Thébault MT, Ollivier H, Garnier JP, Bousquet B, Diouris M, Boeuf G, Nonnotte G (2002) Effects of hypoxia and subsequent recovery on turbot Scophtalmus maximus: hormonal changes and anaerobic metabolism. Mar Ecol Prog Ser 225:275–285CrossRefGoogle Scholar
  118. Pollock MS, Clarke LMJ, Dubé MG (2007) The effects of hypoxia on fishes: from ecological relevance to physiological effects. Environ Rev 15:1–14CrossRefGoogle Scholar
  119. Polymeropoulos ET, Elliott NG, Frappell PB (2017) Hypoxic acclimation leads to metabolic compensation after reoxygenation in Atlantic salmon yolk-sac alevins. Comp Biochem Physiol (A) 213:28–35CrossRefPubMedGoogle Scholar
  120. Poon WL, Hung CY, Nakano K, Randall DJ (2007) An in vivo study of common carp (Cyprinus carpio L.) liver during prolonged hypoxia. Comp Biochem Physiol (D) 2:295–302Google Scholar
  121. Portner H-O (2010) Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climaterelated stressor effects in marine ecosystems. J Exp Biol 213:881–893CrossRefPubMedGoogle Scholar
  122. Prasad MS (1986) Oxygen uptake during early life in the fresh water fish, Esomus danricus (Ham) (Pisces, Cypriniformes). Acta Physiol Hung 67:367–376PubMedGoogle Scholar
  123. Prokic MD, Petrović TG, Gavric JP, Despotović SG, Gavrilović BR, Radovanovic TB, Faggio C, Saičić ZS (2018) Comparative assessment of the antioxidative defense system in subadult and adult anurans: a lesson from the Bufotes viridis toad. Zoology 130:30–37CrossRefPubMedGoogle Scholar
  124. Qi D, Chao Y, Zhao Y, Xia M, Wu R (2018) Molecular evolution of myoglobin in the Tibetan Plateau endemic schizothoracine fish (Cyprinidae, Teleostei) and tissue-specific expression changes under hypoxia. Fish Physiol Biochem 44:557–571CrossRefPubMedGoogle Scholar
  125. Rahman MS, Thomas P (2007) Molecular cloning, characterization and expression of two hypoxia-inducible factor alpha subunits, HIF-1α and HIF-2α, in a hypoxia-tolerant marine teleost, Atlantic croaker (Micropogonias undulatus). Gene 396:273–282CrossRefPubMedGoogle Scholar
  126. Randall DJ, Daxboeck C (1984) Oxygen and carbon dioxide transfer across fish gills. In: Hoar WS, Randall DJ (eds) Fish Physiology, vol 10A. Academic Press, Orlando, pp 263–314Google Scholar
  127. Randall DJ, Baumgarten D, Malyusz M (1972) The relationship between gas and ion transfer across the gills of fishes. Comp Biochem Physiol (A) 41:629–637CrossRefGoogle Scholar
  128. Randolph KN, Clemens HP (1976) Some factors influencing the feeding behaviour of channel catfish in culture ponds. Trans Am Fish Soc 105:718–724CrossRefGoogle Scholar
  129. Remen M, Oppedal F, Torgersen T, Imsland AK, Olsen RE (2012) Effects of cyclic environmental hypoxia on physiology and feed intake of post-smolt Atlantic salmon: initial responses and acclimation. Aquaculture 326–329:148–155CrossRefGoogle Scholar
  130. Richards JG (2011) Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia. J Exp Biol 214:191–199CrossRefPubMedGoogle Scholar
  131. Rinaldi L, Basso P, Tettamanti G, Grimaldi A, Terova G, Saroglia M, de Eguileor M (2005) Oxygen availability causes morphological changes and a different VEGF/FIk-1/HIF-2 expression pattern in sea bass gills. It J Zool 72:103–111CrossRefGoogle Scholar
  132. Rodrigues FA, Marcolino-Gomes J, de Fátima Corrêa Carvalho J, do Nascimento LC, Neumaier N, Farias JRB, Carazzolle MF, Marcelino FC, Nepomuceno AL (2012) Subtractive libraries for prospecting differentially expressed genes in the soybean under water deficit. Gene Mol Biol 35:304–314CrossRefGoogle Scholar
  133. Roesner A, Hankeln T, Burmester T (2006) Hypoxia induces a complex response of globin expression in zebrafish (Danio rerio). J Exp Biol 209(21):29–2137Google Scholar
  134. Routley MH, Nilsson GE, Renshaw GMC (2002) Exposure to hypoxia primes the respiratory and metabolic responses of the epaulette shark to progressive hypoxia. Comp Biochem Physiol (A) 131:313–321CrossRefGoogle Scholar
  135. Ruyet PJ, Lacut A, Le Bayon N, Le Roux A, Pichavant K, Quéméner L (2003) Effects of repeated hypoxic shocks on growth and metabolism of turbot juveniles. Aquat Living Resour 16:25–34CrossRefGoogle Scholar
  136. Sardella AB, Brauner CJ (2007) The osmorespiratory compromise in fish: the effects of physiological state and the environmental. In: Fernandes MN, Rantin FT, Glass ML, Kapoor BG (eds) Fish respiration and environment. Science Publishers, Enfield, pp 147–165CrossRefGoogle Scholar
  137. Saroglia M, Cecchini S, Terova G, Caputo A, De Stradis A (2000) Influence of environmental temperature and water oxygen concentration on gas diffusion distance in sea bass (Dicentrarchus labrax, L.). Fish Physiol Biochem 23:55–58CrossRefGoogle Scholar
  138. Saroglia M, Terova G, De Stradis A, Caputa A (2002) Morphometric adaptations of sea bass gills to different dissolved oxygen partial pressures. J Fish Biol 60:1423–1430CrossRefGoogle Scholar
  139. Saroglia M, Terova G, Prati M (2007) Dissolved oxygen and gill morphometry. In: Fernandes MN, Rantin FT, Glass ML, Kapoor BG (eds) Fish respiration and environment. Science Publishers, Enfield, pp 167–190CrossRefGoogle Scholar
  140. Saroglia M, Caricato G, Frittella F, Brambilla F, Terova G (2010) Dissolved oxygen regimen (PO2) may affect osmo-respiratory compromise in European sea bass (Dicentrarchus labrax, L.). It J An Sci 9:1–15CrossRefGoogle Scholar
  141. Schrøder MB, Villena AJ, Jørgensen T (1998) Ontogeny of lymphoid organs and immunoglobulin producing cells in Atlantic cod (Gadus morhua L). Dev Comp Immunol 22:507–517CrossRefPubMedGoogle Scholar
  142. 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 38:85–105CrossRefPubMedGoogle Scholar
  143. Sehonova P, Svobodova Z, Dolezelova P, Vosmerova P, Faggio C (2018) Effects of waterborne antidepressants on non-target animals living in the aquatic environment: a review. Sci Total Environ 631-632:789–794CrossRefPubMedGoogle Scholar
  144. Shoemaker CA, Evans JJ, Klesius PH (2000) Density and dose: factors affecting mortality of Streptococcus iniae infected tilapia Oreochromis niloticus. Aquaculture 188:229–235CrossRefGoogle Scholar
  145. Soivio A, Nikinmaa M, Westman K (1980) The blood oxygen binding properties of hypoxic Salmogairdneri. J Comp Physiol 136(B):83–87CrossRefGoogle Scholar
  146. Speers-Roesch B, Sandblom E, Lau GY, Farrell AP, Richards JG (2010) Effects of environmental hypoxia on cardiac energy metabolism and performance in tilapia. Am J Phys Regul Integr Comp Phys 298:104–119Google Scholar
  147. Sula E, Aliko V (2017) Effects of stressors on hematological and immunological response in the fresh water crucian carp fish, Carassius carassius. Albanian J Agric Sci (Special edition) 583–590. ISSN: 2218-2020Google Scholar
  148. Svobodova Z, Richard L, Jana M, Blanka V (1993) Water quality and fish health. EIFAC technical paper 54Google Scholar
  149. Swanson C (1998) Interactive effects of salinity on metabolic rate, activity, growth and osmoregulation in the euryhaline milkfish (Chanos chanos). J Exp Biol 201:3355–3366PubMedGoogle Scholar
  150. Taylor JS, Braasch I, Frickey T, Meyer A, Van de Peer Y (2003) Genome duplication, a trait shared by 22000 species of ray-finned fish. Genome Res 13:382–390CrossRefPubMedPubMedCentralGoogle Scholar
  151. Terova G, Rimoldi S, Corà S, Bernardini G, Gornati R, Saroglia M (2008) Acute and chronic hypoxia affects HIF-1α mRNA levels in sea bass (Dicentrarchus labrax). Aquaculture 279:150–159CrossRefGoogle Scholar
  152. Terova G, Rimoldi S, Ceccuzzi P, Brambilla F, Antonini M, Saroglia M (2009) Molecular characterization and in vivo expression of hypoxia inducible factor (HIF)-1α in sea bass (Dicentrarchus labrax) exposed to acute and chronic hypoxia. It J Anim Sci 8(sup 2):875–877CrossRefGoogle Scholar
  153. Thetmeyer H, Waller U, Black KD, Inselmann S, Rosenthal H (1999) Growth of European sea bass (Dicentrarchus labrax L.) under hypoxic and oscillating oxygen conditions. Aquaculture 174:355–367CrossRefGoogle Scholar
  154. Thomas LW, Mcnulty ST, Klesius PH (2007) Effect of sublethal hypoxia on the immune response and susceptibility of channel catfish, Ictalurus punctatus to enteric septicemia. J World Aquacult Soc 38:12–23CrossRefGoogle Scholar
  155. Thorarensen H, Gustavsson AO, Mallya Y, Gunnarsson S (2010) The effect of oxygen saturation on the growth and feed conversion of Atlantic halibut (Hippoglossus hippoglossus L.). Aquaculture 309:96–102CrossRefGoogle Scholar
  156. Tran-Duy A, Schrama JW, van Dam AA, Verreth JAJ (2008) Effects of oxygen concentration and body weight on maximum feed intake, growth and hematological parameters of Nile tilapia, Oreochromis niloticus. Aquaculture 275:152–162CrossRefGoogle Scholar
  157. Tripathi RK, Mohindra V, Singh A, Kumar R, Mishra RM, Jena JK (2013) Physiological responses to acute experimental hypoxia in the air-breathing Indian catfish, Clarias batrachus (Linnaeus, 1758). J Biol Sci 38:373–383Google Scholar
  158. Tsadik GG, Kutty MN (1987) Influence of ambient oxygen on feeding and growth of tilapia, Oreochromis niloticus. ARAC/87/WP/10.United Nation Development Programme. Food and agriculture Organization of the United Nations, Nigerian institute for oceanography and marine research project RAF/87/009Google Scholar
  159. Tzaneva V, Perry SF (2014) Heme oxygenase-1 (HO-1) mediated respiratory responses to hypoxia in the goldfish, Carassius auratus. Respir Physiol Neurobiol 199:1–8CrossRefPubMedGoogle Scholar
  160. Uchida T, Rossignol F, Matthay MA, Mounier R, Couette S, Clottes E, Clerici C (2004) Prolonged hypoxia differentially regulates hypoxia-inducible factor (HIF)-1α and HIF-2α expression in lung epithelial cells: implication of natural antisense HIF-1α. J Biol Chem 279:14871–14878CrossRefPubMedGoogle Scholar
  161. Virani NA, Rees BB (2000) Oxygen consumption, blood lactate and inter-individual variation in the gulf killifish, Fundulus grandis, during hypoxia and recovery. Comp Biochem Physiol (A) 126:397–405CrossRefGoogle Scholar
  162. Wang J, Lu D-Q, Jiang B, Luo H-L, Lu G-L, Li A-X (2018) The effect of intermittent hypoxia under different temperature on the immunomodulation in Streptococcus agalactiae vaccinated Nile tilapia (Oreochromis niloticus). Fish Shelfish Immunol 79:181–192CrossRefGoogle Scholar
  163. Wedemeyer GA (1996) Interactions with water quality conditions in physiology of fish in intensive culture systems. Chapman and Hall, New YorkGoogle Scholar
  164. Welker TL, Mcnulty ST, Klesius PH (2007) Effect of sublethal hypoxia on the immune response and susceptibility of channel catfish, Ictalurus punctatus, to enteric septicemia. J World Aquacult Soc 38:12–23CrossRefGoogle Scholar
  165. Wells RMG, Baldwin J (2006) Plasma lactate and glucose flushes following burst swimming in silver trevally (Pseudocaranx dentex: Carangidae) support the “releaser” hypothesis. Comp Biochem Physiol (A) 143:347–352CrossRefGoogle Scholar
  166. Withers PC (1992) Comparative animal physiology. Saunders College Publishing, SydneyGoogle Scholar
  167. Wright PA, Perry SF, Moon TW (1989) Regulation of hepatic gluconeogenesis and glycogenolysis by catecholamines in rainbow trout during environmental hypoxia. J Exp Biol 147:148–169Google Scholar
  168. Wu RSS (2002) Hypoxia: from molecular responses to ecosystem responses. Mar Pollut Bull 45:35–45CrossRefPubMedGoogle Scholar
  169. Wu Y, Zhong H, Zhao HH, Li T (2007) Effects of different dissolved oxygen concentration on metabolic level of juvenile rainbow trout (Oncorhynchus mykiss) in the recirculating systems. J Shanghai Fish Univ 16(5):438–442Google Scholar
  170. Xia M, ChaoY JJ, Li C, Kong Q, Zhao Y, Guo S, Qi D (2016) Changes of hemoglobin expression in response to hypoxia in a Tibetan schizothoracine fish, Schizopygopsis pylzovi. J Comp Physiol B 186:1033–1043CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Fish Biology and EcologyCentral Laboratory for Aquaculture ResearchSharqiaEgypt
  2. 2.Department of Fisheries, Faculty of Fisheries and Environmental SciencesGorgan University of Agricultural Sciences and Natural ResourcesGorganIran
  3. 3.Department of Chemical, Biological, Pharmaceutical and Environmental SciencesUniversity of MessinaMessinaItaly

Personalised recommendations