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Altered physiological response and gill histology in black rockfish, Sebastes schlegelii, during progressive hypoxia and reoxygenation

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Abstract

Hypoxia has gradually become common in aquatic ecosystems and imposes a significant challenge for fish farming. The loss of equilibrium (LOE), 50% lethal time (LT50), plasma cortisol, glucose, red blood cells (RBC), hemoglobin (Hb), gill histological alteration, and related parameters (lamellar length [SLL] and width [SLW], interlamellar distance [ID], basal epithelial thickness [BET], lamellar surface area [LA], and gill surface area [GSA]); respiratory rate; the proportion of the secondary lamellae available for gas exchange (PAGE); and hypoxia-inducible factor (hif-1α, hif-2α) mRNA expression were determined during progressive hypoxia and reoxygenation (R-0, R-12, R-24 h) to illustrate the underlying physiological response mechanisms in black rockfish Sebastes schlegelii. Results showed that the DO concentration significantly decreased during progressive hypoxia, while DO at LOE and LT50 were 2.42 ± 0.10 mg L−1 and 1.67 ± 0.38 mg L−1, respectively. Cortisol and glucose were significantly increased at LOE and LT50, with the highest levels observed at LT50, and then gradually recovered to normal within reoxygenation 24 h. RBC number and Hb results were like those of glucose. Hypoxia stress resulted in lamellar clubbing, hypertrophy, and hyperplasia. Respiratory frequency significantly increased at LOE and decreased at LT50. Lamellar perimeters, SLL, ID, LA, GSA, and PAGE, significantly increased at LOE and LT50, with the highest values observed at LT50. However, SLW and BET significantly decreased at LOE, LT50, and R-0. These parameters recovered to nearly normal levels at R-24 h. hif-1α mRNAs in gill and liver were significantly upregulated at LOE and LT50, and recovery to normal after reoxygenation 24 h. hif-2α mRNAs in gill was similar to that of hif-1α, whereas hepatic hif-2α mRNAs remained unchanged during hypoxia-reoxygenation. These results indicated that progressive hypoxia stress elevated RBC number, Hb, cortisol, and glucose levels, induced the alteration of gill morphology, increased LA and GSA, stimulated respiratory frequency and PAGE, and upregulated the transcription of hif-1α and hif-2α in gill and liver. Reoxygenation treatment for 24 h alleviated the stress mentioned above effects. These findings expand current knowledge on hypoxia tolerance in black rockfish Sebastes schlegelii.

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References

  • 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 26:340–355

  • Abdel-Tawwab M, Monier MN, Hoseinifar SH, Faggio C (2019) Fish response to hypoxia stress: growth, physiological, and immunological biomarkers. Fish Physiol Biochem 45:997–1013

    Article  CAS  PubMed  Google Scholar 

  • 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 133:375–382

    CAS  Google Scholar 

  • Al-Bairuty GA, Shaw BJ, Handy RD, Henry TB (2013) Histopathological effects of waterborne copper nanoparticles and copper sulphate on the organs of rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 126:104–115

    Article  CAS  PubMed  Google Scholar 

  • Al-Ghanbousi R, Ba-Omar T, Victor R (2012) Effect of deltamethrin on the gills of Aphanius dispar: a microscopic study. Tiss Cell 44:7–14

    Article  CAS  Google Scholar 

  • Baker BI, Rance TA (1981) Differences in concentrations of plasma cortisol in the trout and the eel following adaptation to black or white backgrounds. J Endocrionol 89:135–140

    Article  CAS  Google Scholar 

  • Benli ACK, Köksal G, Özkul A (2008) Sublethal ammonia exposure of Nile tilapia (Oreochromis niloticus L.): effects on gill liver and kidney histology. Chemosphere 72:1355–1358

    Article  CAS  PubMed  Google Scholar 

  • Blanco AM (2020) Hypothalamic- and pituitary-derived growth and reproductive hormones and the control of energy balance in fish. Gen Comp Endocrinol 287:113322

    Article  CAS  PubMed  Google Scholar 

  • Boran H, Altinok I, Capkin E (2010) Histopathological changes induced by maneb and carbaryl on some tissues of rainbow trout, Oncorhynchus mykiss. Tiss Cell 42:158–164

    Article  CAS  Google Scholar 

  • Bowden AJ, Gardiner NM, Couturier CS, Stecyk JA, Nilsson GE, Munday PL, Rummer JL (2014) Alterations in gill structure in tropical reef fishes as a result of elevated temperatures. Comp Biochem Physiol A 175:64–71

    Article  CAS  Google Scholar 

  • Brauner CJ, Rombough PJ (2012) Ontogeny and paleo physiology of the gill: new insights from larval and air-breathing fish. Respir Physiol Neurobiol 184:293–300

    Article  PubMed  Google Scholar 

  • Brett JR (1979) Environmental factors and growth. In: Fish physiology, vol. VIII. In: Hoar WS, Randall DJ, Brett JR (eds) Academic Press, New York, pp 599–675

  • Capaldo A, Gay F, Laforgia V (2019) Changes in the gills of the European eel (Anguilla anguilla) after chronic exposure to environmental cocaine concentration. Ecotoxicol Environ Saf 169:112–119

    Article  CAS  PubMed  Google Scholar 

  • Chen N, Chen LP, Zhang J, Chen C, Wei XL, Gul Y, Wang WM, Wang HL (2012) Molecular characterization and expression analysis of three hypoxia inducible factor alpha subunits, HIF-1α/2α/3α of the hypoxia-sensitive freshwater species, Chinese sucker. Gene 498:81–90

    Article  CAS  PubMed  Google Scholar 

  • Choi E, Alsop D, Wilson JY (2018) The effects of chronic acetaminophen exposure on the kidney, gill and liver in rainbow trout (Oncorhynchus mykiss). Aqua Toxicol 198:20–29

    Article  CAS  Google Scholar 

  • Choudhry H, Harris AL (2018) Advances in Hypoxia-inducible factor biology. Cell Metab 27(2):281–298

    Article  CAS  PubMed  Google Scholar 

  • Claireaux G, Chabot D (2016) Responses by fishes to environmental hypoxia: integration through Fry’s concept of aerobic metabolic scope. J Fish Biol 88:232–251

  • 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 413:138–144

    Article  Google Scholar 

  • Crespo S, Sala R, Marlasca MJ (1987) Different cell types in the gill epithelium of juvenile turbot (Scophthalmus maximus). Aquaculture 67:216–217

    Article  Google Scholar 

  • Dacie JV, Lewis SM (1991) Practical haematology, 7th edn. Churchill Livingstone, London

    Google Scholar 

  • Dejours P (1975) Principles of comparative respiratory physiology. North Holland, Amsterdam, pp 1-253

  • Dhillon RS, Yao L, Matey V, Chen BJ, Zhang AJ, Cao ZD, Fu SJ, Brauner CJ, Wang YS, Richards JG (2013) Interspecifc differences in hypoxia- induced gill remodeling in carp. Physiol Biochem Zool 86:727–739

    Article  PubMed  Google Scholar 

  • Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926–929

    Article  CAS  PubMed  Google Scholar 

  • Douxfils J, Deprez M, Mandiki SN, Milla S, Henrotte E, Mathieu C et al (2012) Physiological 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 33:1112–1122

    Article  CAS  PubMed  Google Scholar 

  • Faraway JJ (2005) Linear models with R. Chapman & Hall/CRC, Boca Raton

    Google Scholar 

  • Gandar A, Laffaille P, Canlet C, Tremblay-Franco M, Gautier R, Perrault A et al (2017) Adaptive response under multiple stress exposure in fish: from the molecular to individual level. Chemosphere 188:60–72

    Article  CAS  PubMed  Google Scholar 

  • Gilmore KL, Doubleday ZA, Gillanders BM (2019) Prolonged exposure to low oxygen improves hypoxia tolerance in a freshwater fish. Conser Physiol 1:58

    Google Scholar 

  • Gisbert E, Rodriguez A, Cardona L, Huertas M, Gallardo MA, Sarasquete C, SalaRabanal 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 239:141–154

    Article  CAS  Google Scholar 

  • Hu CJ, Wang LY, Chodosh LA, Keith B, Simon MC (2003) Differential roles of hypoxia-inducible factor 1α (HIF-1α) and HIF-2α in hypoxic gene regulation. Mol Cell Biol 23:9361–9374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu CJ, Iyer S, Sataur A, Covello KL, Chodosh LA, Simon MC (2006) Differential regulation of the transcriptional activities of hypoxia-inducible factor 1 Alpha (HIF-1α) and HIF-2α in stem cells. Mol Cell Biol 26:3514–3526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jee BY, Do YH, Min BH, Park MS, Hwang HG, Myeong JI, Cho JK (2015) Korean J Environ Biol 33(4):412–418

    Article  Google Scholar 

  • Jenny JP, Francus P, Normandeau A, Lapointe F, Perga ME, Ojala A, Schimmelmann A, Zolitschka B (2016) Global spread of hypoxia in freshwater ecosystems during the last three centuries is caused by rising local human pressure. Glob Chang Biol 22:1481–1489

    Article  PubMed  Google Scholar 

  • Johansson D, Laursen F, Fernӧ A, Fosseidengen JE, Klebert P, Stien LH, Vågseth T, Oppedal F (2014) The interaction between water currents and salmon swimming behaviour in sea cages. PLoS One 9:e97635

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jung JH, Kim HN, Chae YS, Shim WJ (2014) Biochemical responses of Juvenile rockfish (Sebastes schlegeli) to low levels of dissolved oxygen in Gamak Bay. Ocean Sci J 49(3):241–247

    Article  CAS  Google Scholar 

  • Ke Q, Costa M (2006) Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol 70:1469–1480

    Article  CAS  PubMed  Google Scholar 

  • Kim KH, Hwang YJ, Kwon SR (2001) Influence of daily water temperature changes on the chemiluminescent response and mortality of cultured rockfish (Sebastes schlegeli). Aquaculture 192:93–99

    Article  Google Scholar 

  • Kramer DL, McClure M (1982) Aquatic surface respiration, a widespread adaptation to hypoxia in tropical freshwater fishes. Environ Biol Fish 7:47–55

    Article  Google Scholar 

  • 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 7:1–15

    Article  CAS  Google Scholar 

  • Lawrence MJ, Eliason EJ, Zolderdo AJ, Lapointe D, Best C, Gilmour KM, Cooke SJ (2019) Cortisol modulates metabolism and energy mobilization in wild-caught pumpkinseed (Lepomis gibbosus). Fish Physiol Biochem 45:1813–1828

    Article  CAS  PubMed  Google Scholar 

  • 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 295:126–133

    Article  Google Scholar 

  • Liebel S, Tomotake MEM, Ribeiro CAO (2013) Fish histopathology as biomarker to evaluate water quality. Ecotoxicol Environ Contam 8(2):9–15

    Google Scholar 

  • Lin HR, Liu XC (2006) The experimental methods of fish physiology[M] pp: 27–29 Guanzhou Guangdong: Guanzhou High Education Press

  • Liu Y, Ma D, Zhao C, Xiao Z, Xu S, Xiao Y, Wang Y, Liu Q, Li J (2017) The expression pattern of hsp70 plays a critical role in thermal tolerance of marine demersal fish: Multilevel responses of Paralichthys olivaceus and its hybrids (P. olivaceus ♀×P. dentatus ♂) to chronic and acute heat stress. Mar Environ Res 129:386–395

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Love MS, Yoklavich M, Thorsteinson LK (2002) The rockfishes of the northeast Pacific: University of California Press

  • Mallatt J (1985) Fish gill structural changes induced by toxicants and other irritants: a statistical review. Can j Fish Aquat Sci 42:630–648

    Article  CAS  Google Scholar 

  • Mitrovic D, Agnieszka D, Nilsson GE, Perry SF (2009) Physiological consequences of gill remodeling in goldfish (Carassius auratus) during exposure to long-term hypoxia. Am J Physiol Regul Integr Comp Physiol 297:224–234

    Article  CAS  Google Scholar 

  • 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 40:5805–5815

    Article  CAS  PubMed  Google Scholar 

  • Moraes G, Avilez IM, Altran AE, Barbosa CC (2002) Biochemical and hematological responses of the banded knife fish Gymnotus carapo (Linnaeus, 1758) exposed to environmental hypoxia. Braz J Biol 62:633–640

    Article  CAS  PubMed  Google Scholar 

  • Mu W, Wen H, Li J, He F (2015) HIFs genes expression and hematology indices responses to different oxygen treatments in an ovoviviparous teleost species Sebastes schlegelii. Mar Env Res 110:142–151

    Article  CAS  Google Scholar 

  • Nero V, Farwell A, Lister A, Van der Kraak G, Lee LE, Van Meer T, MacKinnon MD, Dixon DG (2006) Gill and liver histopathological changes in yellow perch (Perca flavescens) and goldfish (Carassius auratus) exposed to oil sands process-affected water. Ecotoxicol Environ Safe 63(3):365–377

    Article  CAS  Google Scholar 

  • Nilsson GE (2007) Gill remodeling in fish-a new fashion or an ancient secret? J Exp Biol 210:2403–2409

    Article  PubMed  Google Scholar 

  • Nilsson GE, Dymowska A, Stecyk JA (2012) New insights into the plasticity of gill structure. Respir Physiol Neurobiol 184:214–222

    Article  PubMed  Google Scholar 

  • Oppedal F, Vågseth T, Dempster T, Juell JE, Johansson D (2011) Fluctuating sea cage environments modify the effects of stocking densities on production and welfare parameters of Atlantic salmon (Salmo salar L.). Aquaculture 315:361–368

    Article  Google Scholar 

  • Pan YK, Perry SF (2020) Neuroendocrine control of breathing in fish. Mol Cell Endocrinol 509:110800

    Article  CAS  PubMed  Google Scholar 

  • Perry SF, Fletcher C, Bailey S, Ting J, Bradshaw J, Tzaneva V, Gilmour KM (2012) The interactive effects of exercise and gill remodeling in goldfish (Carassius auratus). J Comp Physiol B 182:935–945

    Article  CAS  PubMed  Google Scholar 

  • 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 225:275–285

    Article  CAS  Google Scholar 

  • Powell WH, Hahn ME (2002) Identification and functional characterization of hypoxia-inducible factor 2a from the estuarine teleost, Fundulus heteroclitus: interaction of HIF-2α with two ARNT2 splice variants. J Exp Zool A Ecol Genet Physiol 294:17–29

    CAS  Google Scholar 

  • 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 396:273–282

    Article  CAS  PubMed  Google Scholar 

  • Reiser S, Wuertz S, Schroeder JP, Kloas W, Hanel R (2011) Risks of seawater ozonation in recirculation aquaculture – effects of oxidative stress on animal welfare of juvenile turbot (Psetta maxima, L.). Aquat Toxicol 105:508–517

    Article  CAS  PubMed  Google Scholar 

  • Rimoldi S, Terova G, Ceccuzzi P, Marelli S, Antonini M, Saroglia M (2012) HIF-1a mRNA levels in Eurasian perch (Perca fluviatilis) exposed to acute and chronic hypoxia. Mol Biol Rep 39:4009–4015

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues S, Antunes SC, Nunes B, Correia AT (2017) Histological alterations in gills and liver of rainbow trout (Oncorhynchus mykiss) after exposure to the antibiotic oxytetracycline. Environ Toxicol Pharmacol 53:164–176

    Article  CAS  PubMed  Google Scholar 

  • Rombough P (2007) The functional ontogeny of the teleost gill: which comes first, gas or ion exchange? Comp Biochem Physiol A 148:732–742

    Article  CAS  Google Scholar 

  • Rotllant J, Guerreiro PM, Anjos L, Redruello B, Canario AVM, Power DM (2005) Stimulation of cortisol release by the N terminus of teleost parathyroid hormone-related protein in interrenal cells in vitro. Endocrinology 146:71–76

    Article  CAS  PubMed  Google Scholar 

  • Semenza GL (1998) Hypoxia-inducible factor 1: master regulator of O2 homeostasis. Curr Opin Genet Dev 8:588–594

    Article  CAS  PubMed  Google Scholar 

  • Semenza GL (2000) HIF-1: mediator of physiological and pathophysiologic al responses to hypoxia. J Appl Physiol 88:1474–1480

    Article  CAS  PubMed  Google Scholar 

  • Semenza GL (2001) HIF-1, O2, and the 3 PHDs: how animal cells signal hypoxia to the nucleus. Cell 107:1–3

    Article  CAS  PubMed  Google Scholar 

  • Sollid J, Nilsson GE (2006) Plasticity of respiratory structures-adaptive remodelling of fish gills induced by ambient oxygen and temperature. Respir Physiol Neurobiol 154:241–251

    Article  CAS  PubMed  Google Scholar 

  • Sollid J, Angelis PD, Gundersen K, Nilsson GE (2003) Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. Exp Biol 206:3667–3673

    Article  Google Scholar 

  • Sollid J, Kjernsli A, De Angelis PM, Rohr AK, Nilsson GE (2005) Cell proliferation and gill morphology in anoxic crucian carp. Am J Phys Regul Integr Comp Phys 289:1196–1201

    Google Scholar 

  • Solstorm D, Oldham T, Solstorm F, Klebert P, Stien LH, Vågseth T, Oppedal F (2018) Dissolved oxygen variability in a commercial sea-cage exposes farmed Atlantic salmon to growth limiting conditions. Aquaculture 486:122–129

    Article  Google Scholar 

  • Stierhoff KL, Targett TE, Grecay PA (2003) Hypoxia tolerance of the mummichog: the role of access to the water surface. J Fish Biol 63:580–592

    Article  Google Scholar 

  • Sula E, Aliko V (2017) Effects of stressors on hematological and immunological response in fresh water crucian carp fish (Carassius carassius). Albanian J Agric Sci 1:583–950

  • Sun JL, Zhao LL, Wu H, Liu Q, Liao L, Luo J et al (2020) Acute hypoxia changes the mode of glucose and lipid utilization in the liver of the largemouth bass (Micropterus salmoides). Sci Total Env 713:135157

    Article  CAS  Google Scholar 

  • Takeda N, Maemura K, Imai Y, Harada T, Kawanami D, Nojiri T, Manabe I, Nagai R (2004) Endothelial PAS domain protein 1 gene promotes angiogenesis through the transactivation of both vascular endothelial growth factor and its receptor, Flt-1. Circ Res 95:146–153

    Article  CAS  PubMed  Google Scholar 

  • Terova G, Rimoldi S, Cora S, Bernardini G, Gornati R, Saroglia M (2008) Acute and chronic hypoxia affects HIF-1α mRNA levels in sea bass (Dicentrarchus labrax). Aquaculture 279:150–159

    Article  CAS  Google Scholar 

  • 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 38:12–23

    Article  Google Scholar 

  • Tzaneva V, Bailey S, Perry SF (2011) The interactive effects of hypoxemia, hyperoxia, and temperature on the gill morphology of goldfish (Carassius auratus). Am J Physiol Regul Integr Comp Physiol 300:1344–1351

    Article  CAS  Google Scholar 

  • Vaquer-Sunyer R, Duarte CM (2008) Thresholds of hypoxia for marine biodiversity. PNAS 105(40):15452–15457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang QF, Shen WL, Hou CC, Liu C, Wu XF, Zhu JQ (2017) Physiological responses and changes in gene expression in the large yellow croaker Larimichthys crocea following exposure to hypoxia. Chemosphere 169:418–427

    Article  CAS  PubMed  Google Scholar 

  • Weber JM, Choi K, Gonzalez A, Teye O (2016) Metabolic fuel kinetics in fish: swimming, hypoxia and muscle membranes. J Exp Biol 219:250–258

    Article  PubMed  Google Scholar 

  • 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 143:347–352

    Article  CAS  Google Scholar 

  • Wenger RH, Gassmann M (1997) Oxygen(es) and the hypoxia-inducible factor-1. Biol Chem 378:609–616

    CAS  PubMed  Google Scholar 

  • Wood AT, Clark TD, Elliott NG, Frappell PB, Andrewartha SJ (2020) The effects of constant and cyclical hypoxia on the survival, growth and metabolic physiology of incubating Atlantic salmon (Salmo salar). Aquaculture 527:735449

    Article  CAS  Google Scholar 

  • Wu ZH, You F, Wen AY, Ma DY, Zhang PJ (2016) Physiological and morphological effects of severe hypoxia, hypoxia and hyperoxia in juvenile turbot (Scophthalmus maximus L.). Aquac Res 47:219–227

    Article  CAS  Google Scholar 

  • Wu CB, Liu ZY, Li FG, Chen J, Jiang XY, Zou SM (2017) Gill remodeling in response to hypoxia and temperature occurs in the hypoxia sensitive blunt snout bream (Megalobrama amblycephala). Aquaculture 479:479–486

    Article  CAS  Google Scholar 

  • Wu CB, Zheng GD, Zhao XY, Zhou S, Zou SM (2020) Hypoxia tolerance in a selectively bred F4 population of blunt snout bream (Megalobrama amblycephala) under hypoxic stress. Aquaculture 518:734484

    Article  CAS  Google Scholar 

  • Yang H, Cao ZD, Fu SJ (2013) The effects of diel-cycling hypoxia acclimation on the hypoxia tolerance, swimming capacity and growth performance of southern catfish (Silurus meridionalis). Comp Biochem Physiol A 165:131–138

    Article  CAS  Google Scholar 

  • Zhao L, Cui C, Liu Q, Sun J, He K, Adam AA (2020) Combined exposure to hypoxia and ammonia aggravated biological effects on glucose metabolism, oxidative stress, inflammation and apoptosis in largemouth bass (Micropterus salmoides). Aquatic Toxicol 224:105514

    Article  CAS  Google Scholar 

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Funding

This study was supported by National Key R&D Program of China (2019YFD0900904), Central Public-interest Scientific Institution Basal Research Fund, YSFRI, CAFS (20603022020008, 2020TD51), and Key Project of Shandong Provincial Natural Science foundation (ZR202010310016).

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  1. Qingdao Key Laboratory for Marine Fish Breeding and Biotechnology, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, No. 106 Nanjing Road, Qingdao, 266071, People’s Republic of China

    Yudong Jia, Jinming Wan, Yunhong Gao & Changtao Guan

  2. Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China

    Yudong Jia & Changtao Guan

  3. College of Fisheries and Life Science, Shanghai Ocean University, Shanghai, 201306, China

    Yuntao Gao

  4. Qingdao Agricultural University, Qingdao, 266109, China

    Juan Li

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  1. Yudong Jia
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Contributions

Yudong Jia mainly designed experiment, wrote, and revised the manuscript. Yuntao Gao finished hematological and biochemical parameter analysis, and gill histology experiment. Jinming Wan and Yunhong Gao are responsible for qRT-PCR experiment. Juan Li checked the grammar, word usage, and give more helpful comments. Changtao Guan provided partly funding support. All authors joined the analysis and interpretation of data and approved the final version of the manuscript.

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Jia, Y., Gao, Y., Wan, J. et al. Altered physiological response and gill histology in black rockfish, Sebastes schlegelii, during progressive hypoxia and reoxygenation. Fish Physiol Biochem 47, 1133–1147 (2021). https://doi.org/10.1007/s10695-021-00970-5

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