Abstract
The black sea bream (Acanthopagrus schlegelii) is an important marine economic fish found on the southeast coast of China. Because of the frequent climate change, the salinity of the waters inhabited by A. schlegelii often decreases, which interferes with the fish’s physiological homeostasis. The isotonic salinity of teleosts are usually lower than that of seawater, so maximum economic benefits cannot be obtained from conventional mariculture. This study was performed to preliminarily clarify the osmotic regulation and antioxidant mechanism of juvenile A. schlegelii and find an appropriate culture salinity value. We selected 5 psu, 10 psu, 15 psu, and 25 psu (control) to conduct physiological experiments for 96 h and growth experiments for 60 days. We found that the juvenile A. schlegelii could adjust their osmotic pressure within 12 h. The growth hormone and cortisol were found to be seawater-acclimating hormones, whereas prolactin was freshwater-acclimating hormone. The activity and mRNA expression of Na+/K+-ATPase showed a U-shaped trend with the decrease of in salinity at 12–96 h. Serum ion concentration and osmotic pressure remained at a relatively stable level after being actively adjusted from 6 to 12 h. At 96 h, the osmotic pressure of the serum isotonic point of juvenile A. schlegelii was approximately equal to that of water with 14.94 salinity. The number and volume of Cl−-secreting cells in the gills decreased. The glomeruli were more developed and structurally sound, with the renal tubules increasing in diameter and the medial brush border being more developed; this may indicate a decrease in salt secretion and an enhanced reabsorption function in the low salinity groups. The activities of superoxide dismutase and catalase and concentration of malondialdehyde were the lowest in the 15 psu group. In addition, the culture conditions of the 15 psu group improved the feed conversion rate without significant differences in weight gain when compared with the control group. Our results show that 15 psu salinity may be the best parameter for obtaining the maximum economic benefits.
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Abbreviations
- PSU:
-
Practical salinity units
- FW:
-
Freshwater
- SW:
-
Seawater
- COR:
-
Cortisol
- NKA:
-
Na+/K+-ATPase
- MRCs:
-
Mitochondrial-rich cells
- GH:
-
Growth hormone
- PRL:
-
Prolactin
- ROS:
-
Reactive oxygen species
- MDA:
-
Malonyldialdehyde
- SOD:
-
Superoxide dismutase
- CAT:
-
Catalase
- WGR:
-
Weight gain rate
- FR:
-
Feed rate
- FCE:
-
Feed conversion rate
- MRC:
-
Mitochondria rich cell
- PVC:
-
Pavement cell
- PiC:
-
Pillar cell
- BC:
-
Blood cell
- MC:
-
Mucous cells
- G:
-
Glomerulus
- P:
-
Proximal segment
- DSM:
-
Distal segment
- CS:
-
Collecting segment
- CV:
-
Central veins
- LC:
-
Liver cell
- LCC:
-
Liver cell cord
- IV:
-
Interlobular vein
- V:
-
Vacuole
References
Abou Anni IS, Bianchini A, Barcarolli IF, Varela Junior AS, Robaldo RB, Tesser MB, Sampaio LA (2016) Salinity influence on growth, osmoregulation and energy turnover in juvenile pompano Trachinotus marginatus Cuvier 1832. Aquaculture 455:63–72. https://doi.org/10.1016/j.aquaculture.2016.01.010
Arunachalam S, Reddy SR (1979) Food intake, growth, food conversion, and body composition of catfish exposed to different salinities. Aquaculture 16:163–171. https://doi.org/10.1016/0044-8486(79)90147-9
Bœuf G, Payan P (2001) How should salinity influence fish growth? Comp Biochem Physiol c: Toxicol Pharmacol 130:411–423. https://doi.org/10.1016/S1532-0456(01)00268-X
Boutet I, Lorin-Nebel C, De Lorgeril J, Guinand B (2007) Molecular characterisation of prolactin and analysis of extrapituitary expression in the European sea bass Dicentrarchus labrax under various salinity conditions. Comp Biochem Physiol d: Genomics Proteomics 2:74–83. https://doi.org/10.1016/j.cbd.2006.12.002
Breves J, P., Watanabe, Soichi, Kaneko, Toyoji, Hirano, Tetsuya & Grau, (2010) Prolactin restores branchial mitochondrion-rich cells expressing Na+/Cl-cotransporter in hypophysectomized Mozambique tilapia. Am J Physiol Regul Integr Comp Physiol 68:R702–R710
Breves JP, Hasegawa S, Yoshioka M, Fox BK, Davis LK, Lerner DT, Takei Y, Hirano T, Grau EG (2010) Acute salinity challenges in Mozambique and Nile tilapia: differential responses of plasma prolactin, growth hormone and branchial expression of ion transporters. Gen Comp Endocrinol 167:135–142. https://doi.org/10.1016/j.ygcen.2010.01.022
Chang C-H, Mayer M, Rivera-Ingraham G, Blondeau-Bidet E, Wu W-Y, Lorin-Nebel C, Lee T-H (2021) Effects of temperature and salinity on antioxidant responses in livers of temperate (Dicentrarchus labrax) and tropical (Chanos Chanos) marine euryhaline fish. J Therm Biol 99:103016. https://doi.org/10.1016/j.jtherbio.2021.103016
Chasiotis H, Kelly SP (2011) Effect of cortisol on permeability and tight junction protein transcript abundance in primary cultured gill epithelia from stenohaline goldfish and euryhaline trout. Gen Comp Endocrinol 172:494–504. https://doi.org/10.1016/j.ygcen.2011.04.023
Deane EE, Woo NYS (2005) Cloning and characterization of sea bream Na+-K+-ATPase α and β subunit genes: in vitro effects of hormones on transcriptional and translational expression. BBRC 331:1229–1238. https://doi.org/10.1016/j.bbrc.2005.04.038
Deane EE, Kelly SP, Luk J, Woo N (2002) Chronic salinity adaptation modulates hepatic heat shock protein and insulin-like growth factor I expression in black sea bream. Mar Biotechnol 4:193–205
Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85(97):177
Farshadian R, Salati AP, Keyvanshokooh S, Pasha-Zanoosi H (2018) Physiological responses of Yellowfin seabream (Acanthopagrus latus) to acute salinity challenge. Mar Freshwat Behav Physiol 51:313–325
Fielder DS, Allan GL, Pepperall D, Pankhurst PM (2007) The effects of changes in salinity on osmoregulation and chloride cell morphology of juvenile Australian snapper, Pagrus auratus. Aquaculture 272:656–666. https://doi.org/10.1016/j.aquaculture.2007.08.043
Horton BP, Rahmstorf S, Engelhart SE, Kemp AC (2014) Expert assessment of sea-level rise by AD 2100 and AD 2300. Qsrv 84:1–6. https://doi.org/10.1016/j.quascirev.2013.11.002
Hossain F, Islam SMM, Islam MS, Shahjahan M (2022) Behavioral and histo-pathological indices of striped catfish (Pangasionodon hypophthalmus) exposed to different salinities. Aquacu Reports 23:101038. https://doi.org/10.1016/j.aqrep.2022.101038
Imsland AK, Björnsson BT, Gunnarsson S, Foss A, Stefansson SO (2007) Temperature and salinity effects on plasma insulin-like growth factor-I concentrations and growth in juvenile turbot (Scophthalmus maximus). Aquaculture 271:546–552. https://doi.org/10.1016/j.aquaculture.2007.07.007
Jarvis PL, Ballantyne JS (2003) Metabolic responses to salinity acclimation in juvenile shortnose sturgeon Acipenser brevirostrum. Aquaculture 219:891–909. https://doi.org/10.1016/S0044-8486(03)00063-2
Jin M, Pan T, Cheng X, Zhu TT, Sun P, Zhou F, Ding X, Zhou Q (2019) Effects of supplemental dietary l-carnitine and bile acids on growth performance, antioxidant and immune ability, histopathological changes and inflammatory response in juvenile black seabream (Acanthopagrus schlegelii) fed high-fat diet. Aquaculture 504:199–209. https://doi.org/10.1016/j.aquaculture.2019.01.063
Kato A, Doi H, Nakada T, Sakai H, Hirose S (2005) Takifugu obscurus is a euryhaline fugu species very close to Takifugu rubripes and suitable for studying osmoregulation. BMC Physiol 5:18
Kelly SP, Wood CM (2002) Cultured gill epithelia from freshwater tilapia (Oreochromis niloticus): effect of cortisol and homologous serum supplements from stressed and unstressed fish. J Membr Biol 190:29–42
Kueltz D (2015) Physiological mechanisms used by fish to cope with salinity stress. J Exp Biol 218:1907–1914. https://doi.org/10.1242/jeb.118695
Laiz-Carrión R, Sangiao-Alvarellos S, Guzmán JM, Martín Del Río MP, Soengas JL, Mancera JM (2005) Growth performance of gilthead sea bream Sparus aurata in different osmotic conditions: Implications for osmoregulation and energy metabolism. Aquaculture 250:849–861. https://doi.org/10.1016/j.aquaculture.2005.05.021
Lee TH, Hwang PP, Shieh YE, Lin CH (2000) The relationship between `deep-hole’ mitochondria-rich cells and salinity adaptation in the euryhaline teleost, Oreochromis mossambicus. Fish Physiol Biochem 23:133–140
Li X, Shen Y, Bao Y, Wu Z, Yang B, Jiao L, Zhang C, Tocher DR, Zhou Q, Jin M (2022) Physiological responses and adaptive strategies to acute low-salinity environmental stress of the euryhaline marine fish black seabream (Acanthopagrus schlegelii). Aquaculture 554:738117. https://doi.org/10.1016/j.aquaculture.2022.738117
Lin Z, Lei J, Liu B, Hong W, Zhu J (2013) Effects of salinities on growth and flesh quality of juvenile turbot( Scophthalmus maximus). J Fish China 37:1535
Madsen SS (1990) The role of cortisol and growth hormone in seawater adaptation and development of hypoosmoregulatory mechanisms in sea trout parr (Salmo trutta trutta). Gen Comp Endocrinol 79:1–11. https://doi.org/10.1016/0016-6480(90)90082-W
Mancera JM, Mccormick SD (1998) Evidence for growth hormone/insulin-like growth factor I axis regulation of seawater acclimation in the Euryhaline TeleostFundulus heteroclitus. Gen Comp Endocrinol 111:103–112. https://doi.org/10.1006/gcen.1998.7086
Martinez-Palacios CA, Ross LG, Rosado-Vallado M (1990) The effects of salinity on the survival and growth of juvenile Cichlasoma urophthalmus. Aquaculture 91:65–75. https://doi.org/10.1016/0044-8486(90)90177-O
Mccormick & S., D. (2001) Endocrine Control of Osmoregulation in Teleost Fish. Am Zool 41:781–794
Mcenroe M, Cech JJ (1985) Osmoregulation in juvenile and adult white sturgeon, Acipenser transmontanus. Environ Biol Fishes 14:23–30
Nordlie FG (2009) Environmental influences on regulation of blood plasma/serum components in teleost fishes: a review. Rev Fish Biol Fish 19:481–564
Partridge GJ, Jenkins GI (2002) The effect of salinity on growth and survival of juvenile black bream (Acanthopagrus butcheri). Aquaculture 210:219–230. https://doi.org/10.1016/S0044-8486(01)00817-1
Piermarini PM, Evans DH (2000) Effects of environmental salinity on Na(+)/K(+)-ATPase in the gills and rectal gland of a euryhaline elasmobranch (Dasyatis sabina). J Exp Biol 203:2957–2966
Rhee J-S, Kim R-O, Seo JS, Lee J, Lee Y-M, Lee J-S (2010) Effects of salinity and endocrine-disrupting chemicals on expression of prolactin and prolactin receptor genes in the euryhaline hermaphroditic fish, Kryptolebias marmoratus. Comp Biochem Physiol c: Toxicol Pharmacol 152:413–423. https://doi.org/10.1016/j.cbpc.2010.07.001
Sakamoto T, Mccormick SD (2006) Prolactin and growth hormone in fish osmoregulation. Gen Comp Endocrinol 147:24–30. https://doi.org/10.1016/j.ygcen.2005.10.008
Sakuragui MM, Sanches JR, Fernandes MN (2003) Gill chloride cell proliferation and respiratory responses to hypoxia of the neotropical erythrinid fishHoplias malabaricus. J Comp Physiol [b] 173:309–317
Sangiao-Alvarellos S, Arjona FJ, Míguez JM, Martín Del Río MP, Soengas JL, Mancera JM (2006) Growth hormone and prolactin actions on osmoregulation and energy metabolism of gilthead sea bream (Sparus auratus). Comp Biochem Physiol a: Mol Integr Physiol 144:491–500. https://doi.org/10.1016/j.cbpa.2006.04.015
Seale AP, Stagg JJ, Yamaguchi Y, Breves JP, Soma S, Watanabe S, Kaneko T, Cnaani A, Harpaz S, Lerner DT, Grau EG (2014) Effects of salinity and prolactin on gene transcript levels of ion transporters, ion pumps and prolactin receptors in Mozambique tilapia intestine. Gen Comp Endocrinol 206:146–154. https://doi.org/10.1016/j.ygcen.2014.07.020
Seidelin M, Madsen SS (1997) Prolactin antagonizes the seawater-adaptive effect of cortisol and growth hormone in anadromous brown trout (Salmo trutta). Zool Sci 14:249–256
Shao Q, Ma J, Xu Z, Hu W, Xu J, Xie S (2008) Dietary phosphorus requirement of juvenile black seabream, Sparus macrocephalus. Aquaculture 277:92–100. https://doi.org/10.1016/j.aquaculture.2008.01.029
Sherwani FA, Parwez I (2008) Plasma thyroxine and cortisol profiles and gill and kidney Na+/K+-ATPase and SDH activities during acclimation of the catfish Heteropneustes fossilis (bloch) to higher salinity, with special reference to the effects of exogenous cortisol on hypo-osmoregulatory ability of the catfish. Zool Sci 25:164
Sudo R, Suetake H, Suzuki Y, Aoyama J, Tsukamoto K (2013) Profiles of mRNA expression for prolactin, growth hormone, and somatolactin in Japanese eels, Anguilla japonica: the effect of salinity, silvering and seasonal change. Comp Biochem Physiol a: Mol Integr Physiol 164:10–16. https://doi.org/10.1016/j.cbpa.2012.09.019
Tahir D, Shariff M, Syukri F, Yusoff FM (2018) Serum cortisol level and survival rate of juvenileEpinephelus fuscoguttatusfollowing exposure to different salinities. Veterinary World 11:327–331
Tipsmark CK, Madsen SS (2009) Distinct hormonal regulation of Na+, K+-atpase genes in the gill of Atlantic salmon (Salmo salar L.). J Endocrinol 203:301–310
Tipsmark CK, Madsen SS, Borski RJ (2004) Effect of salinity on expression of branchial ion transporters in striped bass (Morone saxatilis). J Exp Zool Part Ecol Integr Physiol 301A:979–991
Viviana L, Fernanda BI, André SL, Adalto B (2015) Effect of salinity on survival, growth and biochemical parameters in juvenile Lebranch mullet Mugil liza (Perciformes: Mugilidae). Neotrop Ichthyol 13:447–452
Wijk E, Rintoul SR (2014) Freshening drives contraction of Antarctic Bottom Water in the Australian Antarctic Basin. GeoRL 41:1657–1664
Winston GW, Giulio R (1991) Prooxidant and Antioxidant Mechanisms in Aquatic Organisms 19:137–161
Wu L, Liang H, Hamunjo CMK, Ge X, Ji K, Yu H, Huang D, Xu H, Ren M (2021) Culture salinity alters dietary protein requirement, whole body composition and nutrients metabolism related genes expression in juvenile Genetically Improved Farmed Tilapia (GIFT) (Oreochromis niloticus). Aquaculture 531:735961. https://doi.org/10.1016/j.aquaculture.2020.735961
Yada T, Mccormick SD, Hyodo S (2012) Effects of environmental salinity, biopsy, and GH and IGF-I administration on the expression of immune and osmoregulatory genes in the gills of Atlantic salmon (Salmo salar). Aquaculture 362–363:177–183. https://doi.org/10.1016/j.aquaculture.2010.12.029
Yan M, Li Z, Xiong B, Zhu J (2010) Effects of salinity on food intake, growth, and survival of pufferfish (Fugu obscurus). J Appl Ichthyol 20:146–149
Zhu H, Liu Z, Gao F, Lu M, Liu Y, Su H, Ma D, Ke X, Wang M, Cao J, Yi M (2018) Characterization and expression of Na+/K+-ATPase in gills and kidneys of the Teleost fish Oreochromis mossambicus, Oreochromis urolepis hornorum and their hybrids in response to salinity challenge. Comp Biochem Physiol a: Mol Integr Physiol 224:1–10. https://doi.org/10.1016/j.cbpa.2018.05.017
Chang, C.Y., Tang, C.H., Hsin, Y.H., Lai, H.T. & Lee, T.H. (2014) FXYD2c plays a potential role in modulating Na+/K+-ATPase activity in HK-2 cells upon hypertonic challenge. J Membr Biol, 247.
Dawood, M.a.O., Noreldin, A.E. & Sewilam, H. (2021) Long term salinity disrupts the hepatic function, intestinal health, and gills antioxidative status in Nile tilapia stressed with hypoxia. Ecotoxicol Environ Saf, 220. https://doi.org/10.1016/j.ecoenv.2021.112412
El-Leithy, A., Hemeda, S.A., Naby, W., Nahas, A. & Helmy, Z.A. (2019) Optimum salinity for Nile tilapia (Oreochromis niloticus) growth and mRNA transcripts of ion-regulation, inflammatory, stress- and immune-related genes. Fish Physiol Biochem.
Liu, Z., Ma, A., Yuan, C., Zhao, T., Chang, H. & Zhang, J. (2021) Transcriptome analysis of liver lipid metabolism disorders of the turbot Scophthalmus maximus in response to low salinity stress. Aquaculture, 534. https://doi.org/10.1016/j.aquaculture.2020.736273
Mccormick, M. (1998) Osmoregulatory actions of the GH/IGF axis in non-salmonid teleosts. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology.
Mccormick, S.D. (2011) Hormonal control of metabolism and ionic regulation | The Hormonal Control of Osmoregulation in Teleost Fish. Encyclopedia of Fish Physiology: 1466–1473.
Moorman, B.P. (2014) The effects of rearing Mozambique tilapia in a tidally-changing salinity on osmoregulation and growth. Dissertations & Theses - Gradworks.
Perevedentsev, Y.P. (2019) Current climate change and its effects. Proceedings of Voronezh State University Series: Geography Geoecology: 98–102.
Sakuragui, M.M., Valentim, M.L. & Fernandes, M.N. (2007) 16.P14. Chloride cell density in the gills of the erythrinid fish, Hoplias malabaricus, after exposure to deionized water and hypoxia. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology, 148: 0–0.
Shepherd, Brian, S., Drennon, Katherine, Johnson, Jaime, Nichols, Joel & W. (2005) Salinity acclimation affects the somatotropic axis in rainbow trout. Am J Physiol Regul Integr Comp Physiol, 57: R1385-R1395.
Shui, C., Shi, Y., Hua, X., Zhang, Z., Zhang, H., Lu, G. & Xie, Y. (2018) Serum osmolality and ions,and gill Na^(+)/K^(+)-ATPase of spottedtail goby Synechogobius ommaturus(R.)in response to acute salinity changes. Aquaculture and Fisheries, 3: 5.
Stephen, D. & Mccormick (2001) Endocrine control of osmoregulation in teleost fish. Amer Zool.
Sumpter, J.P. (1997) The endocrinology of stress. Fish Stress & Health in Aquaculture.
Tatsuya, Sakamoto, And, Tomohiro, Kozaka, And, Akiyoshi, Takahashi, And & Hiroshi (2001) Medaka (Oryzias latipes) as a model for hypoosmoregulation of euryhaline fishes. Aquaculture.
Tian, L., Tan, P., Yang, L., Zhu, W. & Xu, D. (2020) Effects of salinity on the growth, plasma ion concentrations, osmoregulation, non-specific immunity, and intestinal microbiota of the yellow drum (Nibea albiflora). Aquaculture, 528. https://doi.org/10.1016/j.aquaculture.2020.735470
Tian, Y., Wen, H., Qi, X., Zhang, X., Liu, S., Li, B., Sun, Y., Li, J., He, F., Yang, W. & Li, Y. (2019) Characterization of full-length transcriptome sequences and splice variants of Lateolabrax maculatus by single-molecule long-read sequencing and their involvement in salinity regulation. FRONTIERS IN GENETICS, 10. https://doi.org/10.3389/fgene.2019.01126
Zoology, R.I. (2013) Fish Physiology: Euryhaline Fishes. Fish Physiol.
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This work was supported by the National Natural Science Foundation of China (31872586), the Major Project of Science, Technology and Innovation 2025 In Ningbo City (2021Z003), and by K. C. Wong Magna Fund in Ningbo University.
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Yibo Zhang and Shun Zhang performed the experiments and analyzed the data. Yibo Zhang wrote the manuscript. All authors have read and approved the final manuscript.
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Zhang, Y., Zhang, S., Xu, S. et al. Effects of acute low-salinity stress on osmoregulation, antioxidant capacity, and growth of the black sea bream (Acanthopagrus schlegelii). Fish Physiol Biochem 48, 1599–1617 (2022). https://doi.org/10.1007/s10695-022-01144-7
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DOI: https://doi.org/10.1007/s10695-022-01144-7