Interactive effect of high environmental ammonia and nutritional status on ecophysiological performance of European sea bass (Dicentrarchus labrax) acclimated to reduced seawater salinities

Aquatic Toxicology

Volumn 160, Issue , 2015, Pages 39-56

  Sinha, Amit Kumar ^a   Rasoloniriana, Rindra ^a   Dasan, Antony Franklin ^a   Pipralia, Nitin ^a   Blust, Ronny ^a   Boeck, Gudrun De ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Ammonia excretion rate; Energy metabolism; Fasting; Ionoregulation; Marine teleosts; Osmoregulation; Osmotic stress

Indexed keywords

AMMONIA; LACTIC ACID; SEA WATER; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 1; UREA; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CARRIER PROTEIN; WATER POLLUTANT;

ACCLIMATION; AMMONIA; ECOPHYSIOLOGY; EXCRETION; METABOLISM; NUTRITIONAL STATUS; OSMOREGULATION; PERCIFORM; SALINITY; SEAWATER; TOXICITY;

AMMONIA BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CHLORIDE BLOOD LEVEL; CONTROLLED STUDY; ECOPHYSIOLOGY; EUROPEAN SEA BASS; FOOD AVAILABILITY; LACTATE BLOOD LEVEL; LC50; NONHUMAN; NUTRITIONAL STATUS; POTASSIUM BLOOD LEVEL; PRIORITY JOURNAL; SALINITY; SERUM OSMOLALITY; SODIUM BLOOD LEVEL; UPREGULATION; UREA BLOOD LEVEL; WATER CONTENT; ACCLIMATIZATION; ANIMAL; BASS; CHEMISTRY; DRUG EFFECTS; GENETICS; GILL; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; TOXICITY; WATER POLLUTANT;

DICENTRARCHUS LABRAX; SERRANIDAE; TELEOSTEI;

ACCLIMATIZATION; AMMONIA; ANIMALS; BASS; GILLS; MEMBRANE TRANSPORT PROTEINS; NUTRITIONAL STATUS; SALINITY; SEAWATER; SODIUM-POTASSIUM-EXCHANGING ATPASE; STRESS, PHYSIOLOGICAL; WATER POLLUTANTS, CHEMICAL;

EID: 84928700322     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2015.01.005     Document Type: Article

References (98)

1. Alam M., Frankel T.L. Gill ATPase activities of silver perch, Bidyanus bidyanus (Mitchell), and golden perch, Macquaria ambigua (Richardson): effects of environmental salt and ammonia. Aquaculture 2006, 251:118-133.
2. Arillo A., Margiocco C., Melodia F., Mesi P., Schenone G. Ammonia toxicity mechanism in fish: studies on rainbow trout (Salmo gairdneri Rich.). Ecotoxicol. Environ. Saf. 1981, 5:316-328.
3. Avella M., Bornancin M. A new analysis of ammonia and sodium transport through the gills of the freshwater rainbow trout (Salmo gairdneri). J. Exp. Biol. 1989, 142:155-175.
4. Barnabé G., Boulineau-Coatanea F., Rene F. Chronology of morphogenesis in Dicentrarchus labrax (L.) (Pisces: Serranidae) obtained by artificial reproduction. Aquaculture 1976, 8:351-363.
5. Bianchini A., Wasielesky W., Miranda-Filho K.C. Toxicity of nitrogenous compounds to juveniles of flatfish Paralichthys orbignyanus. Bull. Environ. Contam. Tox. 1996, 56:453-459.
6. Bligh E.G., Dyer W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 1959, 37:911-917.
7. Boutet I., Long Ky C.L., Bonhomme F. A transcriptomic approach of salinity response in the euryhaline teleost, Dicentrarchus labrax. Gene 2006, 379:40-50.
8. Bradford M.M. A rapid and sensitive method for the quantitation of micro-gram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:249-254.
9. Braun M.H., Steele S.L., Perry S.F. The responses of zebrafish (Danio rerio) to high external ammonia and urea transporter inhibition: nitrogen excretion and expression of rhesus glycoproteins and urea transporter proteins. J. Exp. Biol. 2009, 212:3846-3856.
10. Diricx M., Sinha A.K., Liew H.J., Mauro N., Blust R., De Boeck G. Compensatory responses in common carp (Cyprinus carpio) under ammonia exposure: additional effects of feeding and exercise. Aquat. Toxicol. 2013, 142-143:123-137.
11. Doneen B.A. Effects of adaptation to sea water, 170% sea water and to fresh water on activities and subcellular distribution of branchial Na+,K+-ATPase, low- and high- affinity Ca++-ATPase, and ouabain-insensitive ATPase in Gillichthys mirabilis. J. Comp. Physiol. B 1981, 145:51-61.
12. Dosdat A., Ruyet J.P., Coves D., Dutto G., Gasset E., Roux A., Lemarie G. Effect of chronic exposure to ammonia on growth: food utilization and metabolism of the European sea bass (Dicentrarchus labrax). Aquat. Living Resour. 2003, 16:509-520.
13. Dymowska A.K., Hwang P.P., Goss G.G. Structure and function of ionocytes in the freshwater fish gill. Respir. Physiol. Neurobiol. 2012, 184:282-292.
14. Engin K., Carter C.G. Ammonia and urea excretion rates of juvenile Australian short-finned eel (Anguilla australis australis) as influenced by dietary protein level. Aquaculture 2001, 194:123-136.
15. Evans D.H., Piermarini P.M., Choe K.P. The multifunctional fish gill: dominant site of gas exchange osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol. Rev. 2005, 85:97-177.
16. Franklin C.E., Forster M.E., Davison W. Plasma cortisol and osmoregulatory changes in sockeye salmon transferred to sea water: comparison between successful and unsuccessful adaptation. J. Fish Biol. 1992, 41:113-122.
17. Freeland H., Whitney F. Climatic changes: Gulf of Alaska. Global Issues and Processes, III 2000, 179-186. Pergamon, Amsterdam, Netherlands. C. Sheppard (Ed.).
18. Freire C.A., Amado E.M., Souza L.R., Veiga M., Vitule J.R., Souza M.M., Prodocimo V. Muscle water control in crustaceans and fishes as a function of habitat osmoregulatory capacity, and degree of euryhalinity. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2008, 149:435-446.
19. Gallis J.L., Lasserre P., Belloc F. Freshwater adaptation in the euryhaline teleost, Chelon labrosus. I. Effects of adaptation, prolactin, cortisol and actinomycin-D on plasma osmotic balance and (Na+-K+) ATPase in gill and kidney. Gen. Comp. Endocrinol. 1979, 38:1-10.
20. Geay F., Santigosa I., Culi E., Corporeau C., Boudry P., Dreano Y., Corcos L., Bodin N., Vandeputte M., Zambonino-Infante J.L., Mazurais D., Cahu C.L. Regulation of FADS2 expression and activity in European sea bass (Dicentrarchus labrax: L) fed a vegetable diet. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2010, 156:237-243.
21. Giffard-Mena I., Lorin-Nebel C., Charmantier G., Castille R., Boulo V. Adaptation of the sea bass (Dicentrarchus labrax) to fresh water: role of aquaporins and Na+/K+-ATPases. Comp. Biochem. Physiol. A Mol. Integr. Physiol 2008, 150:332-338.
22. Hakim Y., Harpaz S., Uni Z. Expression of brush border enzymes and transporters in the intestine of European sea bass (Dicentrarchus labrax) following food deprivation. Aquaculture 2009, 290:110-115.
23. Hiroi J., Yasumasu S., McCormick S.D., Hwang P.P., Kaneko T. Evidence for an apical Na-Cl cotransporter involved in ion uptake in a teleost fish. J. Exp. Biol. 2008, 211:2584-2599.
24. Hiroi J., McCormick S.D. Variation in salinity tolerance, gill Na+/K+-ATPase, Na+/K+/2Cl- cotransporter and mitochondria-rich cell distribution in three salmonids Salvelinus namaycush, Salvelinus fontinalis and Salmo salar. J. Exp. Biol. 2007, 210:1015-1024.
25. Hiroi J., McCormick S.D. New insights into gill ionocyte and ion transporter function in euryhaline and diadromous fish. Respir. Physiol. Neurobiol. 2012, 184:257-268.
26. Hsu H.H., Lin L.Y., Tseng Y.C., Horng J.L., Hwang P.P. A new model for fish ion regulation: identification of ionocytes in freshwater-and seawater-acclimated medaka (Oryzias latipes). Cell Tissue Res. 2014, 357:225-243.
27. Hung C.Y.C., Tsui K.N.T., Wilson J.M., Nawata C.M., Wood C.M., Wright P.A. Rhesus glycoprotein gene expression in the mangrove killifish Kryptolebias marmoratus exposed to elevated environmental ammonia levels and air. J. Exp. Biol. 2007, 210:2419-2429.
28. Hwang P.P., Lee T.H., Lin L.Y. Ion regulation in fish gills: recent progress in the cellular and molecular mechanisms. J. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 301:28-47.
29. IPCC Summary for policymakers. Climate Change 2013: The Physical Science Basis Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change 2013, 2013. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA. T.F. Stocker, Q.D. Plattner, G.-K. Tignor, M. Allen, S.K. Boschung, J.A. Nauels, Y. Xia, V. Bex, P.M. Midgley (Eds.).
30. Kajimura M., Croke S.J., Glover C.N., Wood C.M. Dogmas and controversies in the handling of nitrogenous wastes: the effect of feeding and fasting on the excretion of ammonia, urea and other nitrogenous waste products in rainbow trout. J. Exp. Biol. 2004, 207:1993-2002.
31. Katoh F., Shimizu A., Uchida K., Kaneko T. Shift of chloride cell distribution during early life stages in seawater adapted killifish Fundulus heteroclitus. Zool. Sci. 2002, 17:11-18.
32. Katoh F., Cozzi R.R.F., Marshall W.S., Goss G.G. Distinct Na+ /K+/2Cl- cotransporter localization in kidneys and gills of two euryhaline species: rainbow trout and killi fish. Cell Tissue Res. 2008, 334:265-281.
33. Kelley D.F. The importance of estuaries for sea bass: Dicentrarchus labrax (L). J. Fish Biol. 1988, 33:25-33.
34. Kelly S.P., Chow I.N.K., Woo N.Y.S. Haloplasticity of black seabream (Mylio macrocephalus): hypersaline to freshwater acclimation. J. Exp. Zool. 1999, 283:226-241.
35. Khoo K.H., Culberson C.H., Bates R.G. Thermodynamics of the dissociation of ammonia ion in seawater from 5 to 40°C. J. Solution Chem. 1977, 6:281-290.
36. Knoph M.B., Olsen Y.A. Subacute toxicity of ammonia to Atlantic salmon (Salmo salar L.) in seawater effects on water and salt balance, plasma cortisol and plasma ammonia levels. Aquat. Toxicol. 1994, 30:295-310.
37. Knoph M.B., Thorud K. Toxicity of ammonia to Atlantic salmon (Salmo salar L.) in seawater - effects on plasma osmolarity ion, ammonia, urea and glucose levels and hematologic parameters. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 1996, 113:375-381.
38. Langdon J.S. Active osmoregulation in the Australian bass, Macquaria novemaculata (Steindachner), and the golden perch: Macquaria ambigua (Richardson) (Percichthyidae). Aust. J. Mar. Freshwater Res. 1987, 38:771-776.
39. Lasserre P. Increase of (Na++K+)-dependent ATPase activity in gills and kidneys of two euryhaline marine teleosts Crenimugil labrosus (Risso,1826) and Dicentrarchus labrax (Linnaeus, 1758). Life Sci. 1971, 10:113-119.
40. Lin H., Randall D.J. H+-ATPase in crude homogenates of fish gill tissue: inhibitor sensitivity and environmental and hormonal regulation. J. Exp. Biol. 1993, 180:163-174.
41. Lin H., Randall D.J. Proton pumps in fish gills. Cellular and Molecular Approaches to Fish Ionic Regulation: Fish Physiology 1995, 229-255. CA: Academic Press, San Diego. C.M. Wood, T.J. Shuttleworth (Eds.).
42. Lin Y.M., Chen C.N., Lee T.H. The expression of gill Na K-ATPase in milkfish, Chanos chanos, acclimated to seawater, brackish water and fresh water. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2003, 135:489-497.
43. Loong A.M., Chew S.F., Wong W.P., Lam S.H., Ip Y.K. Both seawater acclimation and environmental ammonia exposure lead to increases in mRNA expression and protein abundance of Na+:K+:2Cl- cotransporter in the gills of the freshwater climbing perch, Anabas testudineus. J. Comp. Physiol. B 2012, 182:491-506.
44. Lorin-Nebel C., Boulo V., Bodinier C., Charmantier G. The Na+/K+/2Cl- cotransporter in the sea bass Dicentrarchus labrax during ontogeny: involvement in osmoregulation. J. Exp. Biol. 2006, 209:4908-4922.
45. Marshall W.S., Lynch E.M., Cozzi R.R.F. Redistribution of immunofluorescence of CFTR anion channel and NKCC cotransporter in chloride cells during adaptation to the killifish Fundulus heteroclitus to sea water. J. Exp. Biol. 2002, 205:1265-1273.
46. McCormick S.D. Methods for the nonlethal gill biopsy and measurements of Na+: K+-ATPase activity. Can. J. Fish. Aquat. Sci. 1993, 50:656-658.
47. McKenzie D.J., Vergnet A., Chatain B., Vandeputte M., Desmarais E., Steffensen J.F., Guinand B. Physiological mechanisms underlying individual variation in tolerance of food deprivation in juvenile European sea bass, Dicentrarchus labrax. J. Exp. Biol. 2014, 217:3283-3292.
48. Merino G., Piedrahita R., Concklin D.E. Ammonia and urea excretion rates of California halibut (Paralichthys californicus, Ayres) under farm-like conditions. Aquaculture 2007, 271:227-243.
49. Nakada T., Westhoff C.M., Kato A., Hirose S. Ammonia secretion from fish gill depends on a set of Rh glycoproteins. FASEB J. 2007, 21:1067-1074.
50. Nawata C.M., Hung C.C.Y., Tsui T.K.N., Wilson J.M., Wright P.A., Wood C.M. Ammonia excretion in rainbow trout (Oncorhynchus mykiss): evidence for Rh glycoprotein and H+-ATPase involvement. Physiol. Genomics 2007, 31:463-474.
51. Nawata C.M., Wood C.M. mRNA expression analysis of the physiological responses to ammonia infusion in rainbow trout. J. Comp. Physiol. B 2009, 179:799-810.
52. Nebel C., Romestand B., Nègre-Sadargues G., Grousset E., Aujoulat F., Bacal J., Bonhomme F., Charmantier G. Differential freshwater adaptation in juvenile sea bass Dicentrarchus labrax: involvement of gills and urinary system. J. Exp. Biol. 2005, 208:3859-3871.
53. Patrick M.L., Wood C.M. Ion and acid-base regulation in the freshwater mummichog (Fundulus heteroclitus): a departure from the standard model for freshwater teleosts. Biochem. Comp. Physiol. A Mol. Integr. Physiol. 1999, 122:445-456.
54. Person-Le Ruyet J., Chartois H., Quemener L. Comparative acute ammonia toxicity in marine fish and plasma ammonia response. Aquaculture 1995, 136:181-194.
55. Person-Le Ruyet J., Lamers A., Roux A., Severe A., Boeuf G., Mayer-Gostan N. Long term ammonia exposure of turbot: effects of plasma parameters. J. Fish Biol. 2003, 62:879-894.
56. Pierce D.W., Gleckler P.J., Barnett T.P., Santer B.D., Durack P.J. The fingerprint of human-induced changes in the ocean's salinity and temperature fields. Geophys. Res. Lett. 2012, 39:L21704.
57. Polakof S., Arjona F.J., Sangiao-Alvarellos S., del Río M.P.M., Mancera J.M., Soengas J.L. Food deprivation alters osmoregulatory and metabolic responses to salinity acclimation in gilthead sea bream Sparus auratus. J. Comp. Physiol. B 2006, 176:441-452.
58. Rahmatullah M., Boyde T.R. Improvements in the determination of urea using diacetyl monoxime: methods with and without deproteinization. Clin. Chim. Acta 1980, 107:3-9.
59. Randall D.J., Tsui T.K. Ammonia toxicity in fish. Mar. Pollut. Bull. 2002, 45:17-23.
60. Randall D.J., Wilson J.M., Peng K.W., Kok T.W.K., Kuah S.S.L., Chew S.F., Lam T.J., Ip Y.K. The mudskipper Periophthalmodon schlosseri, actively transports NH4+ against a concentration gradient. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1999, 277:1562-1567.
61. Robinson E.H., Li M.H. Effect of dietary protein concentration and feeding rate on weight gain, feed efficiency, and body composition of pond-raised channel catfish Ictalurus punctatus. J. World Aquacult. Soc. 1999, 30:311-318.
62. Rodríguez A., Gisbert E., Castelló-Orvay F. Nutritional condition of Anguilla anguilla starved at various salinities during the elver phase. J. Fish Biol. 2005, 67:521-534.
63. Roe J.H., Dailey R.E. Determination of glycogen with the anthrone reagent. Anal. Biochem. 1966, 15:245-250.
64. Rueda F.M., Martinez F.J., Zamora S., Kentouri M., Divanach P. Effect of fasting and refeeding on growth and body composition of red porgy Pagrus pagrus L. Aquacult. Res. 1998, 29:447-452.
65. Sampaio L.A., Wasielesky W., Miranda-Filho K.C. Effect of salinity on acute toxicity of ammonia and nitrite to juvenile Mugil platanus. Bull. Environ. Contam. Toxicol. 2002, 68:668-674.
66. Schram E., Roques J.A.C., Abbink W., Spnings T., de Vries P., Biernan S., van de Vis H., Flik G. The impact of elevated water ammonia concentration on physiology, growth and feed intake of African catfish (Clarias gariepinus). Aquaculture 2010, 306:108-115.
67. Scarabello M., Wood C.M., Heigenhauser G.J.F. Glycogen depletion in juvenile rainbow trout as an experimental test of the oxygen debt hypothesis. Can. J. Zool. 1991, 69:2562-2568.
68. Sinha A.K., Liew H.J., Diricx M., Blust R., De Boeck G. The interactive effects of ammonia exposure: nutritional status and exercise on metabolic and physiological responses in goldfish (Carassius auratus L.). Aquat. Toxicol. 2012, 109:33-46.
69. Sinha A.K., Liew H.J., Diricx M., Kumar V., Darras V.M., Blust R., De Boeck G. Combined effects of high environmental ammonia, starvation and exercise onhormonal and ion-regulatory response in goldfish (Carassius auratus L.). Aquat. Toxicol. 2012, 114-115:153-164.
70. Sinha A.K., Diricx M., Chan L.P., Liew H.J., Kumar V., Blust R., De Boeck G. Expression pattern of potential biomarker genes related to growth, ion regulation and stress in response to ammonia exposure, food deprivation and exercise in common carp (Cyprinus carpio). Aquat. Toxicol. 2012, 122-123:93-105.
71. Sinha A.K., Liew H.J., Nawata C.M., Blust R., Wood C.M., De Boeck G. Modulation of Rh glycoproteins, ammonia excretion and Na+ fluxes in three freshwater teleosts when exposed chronically to high environmental ammonia. J. Exp. Biol. 2013, 216:2917-2930.
72. Sinha A.K., Matey V., Giblen T., Blust R., De Boeck G. Gill remodeling in three freshwater teleosts in response to high environmental ammonia. Aquat. Toxicol. 2014, 155:166-180.
73. Sinha A.K., Dasan A.F., Rasoloniriana R., Pipralia N., Blust R., De Boeck G. Hypoosmotic stress induced physiological and ion-osmoregulatory responses in European sea bass (Dicentrarchus labrax) are modulated differentially by nutritional status. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2015, 181:87-99.
74. Stuenkel E.L., Hillyard S.D. Effects of temperature and salinity on gill Na+-K+ ATPase activity in the pupfish, Cyprinodon salinus. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 1980, 67:179-182.
75. Sucré E., Bossus M., Bodinier C., Boulo V., Charmantier G., Charmantier-Daures M., Cucchi P. Osmoregulatory response to low salinities in the European sea bass embryos: a multi-site approach. J. Comp. Physiol. B 2013, 183:83-97.
76. Swanson C. Interactive effects of salinity on metabolic rate, activity, growth and osmoregulation in the euryhaline milkfish (chanos chanos). J. Exp. Biol. 1998, 201:3355-3366.
77. Tang C.H., Tzeng C.S., Hwang L.Y., Lee T.H. Constant muscle water contents and renal HSP90 expression reflect the osmotic homeostasis in euryhaline teleosts acclimatized to different environmental salinities. Zool. Stud. 2009, 48:435-441.
78. Thurston R.V., Russo R.C., Emerson K. Aqueous ammonia equilibrium tabulation of percent of unionized ammonia. US EPA 1979, 600(3):79-91.
79. Tsui T.K.N., Hung C.Y.C., Nawata C.M., Wilson J.M., Wright P.A., Wood C.M. Ammonia transport in cultured gill epithelium of freshwater rainbow trout: the importance of Rhesus glycoproteins and the presence of an apical Na+/NH4+ exchange complex. J. Exp. Biol. 2009, 212:878-892.
80. Uliano E., Cataldi M., Carella F., Migliaccio O., Iaccarino D., Agnisola C. Effects of acute changes in salinity and temperature on routine metabolism and nitrogen excretion in gambusia (Gambusia affinis) and zebrafish (Danio rerio). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2010, 157:283-290.
81. Vedel N.E., Korsgaard B., Jensen F.B. Isolated and combined exposure to ammonia and nitrite in rainbow trout (Oncorhynchus mykiss): effects on electrolyte status, blood respiratory properties and brain glutamine/glutamate concentrations. Aquat. Toxicol. 1998, 41:325-342.
82. Verdouw H., Van Echteld C.J.A., Dekkers E.M.J. Ammonia determination based on indophenol formation with sodium salicylate. Water Res. 1978, 12:399-402.
83. Weihrauch D., Wilkie M.P., Walsh P.J. Ammonia and urea transporters ingills of fish and aquatic crustaceans. J. Exp. Biol. 2009, 212:1716-1730.
84. Weirich C.R., Tomasso J.R., Smith T.I.J. Toxicity of ammonia and nitrite to sunshine bass in selected environments. J. Aquat. Anim. Health 1993, 5:64-72.
85. Weirich C.R., Riche M.A. Tolerance of juvenile black sea bass Centropristis striata to acute ammonia and nitrite exposure at various salinities. Fish Sci. 2006, 72:915-921.
86. Wendelaar Bonga S.E. The stress response in fish. Physiol. Rev. 1997, 77:591-625.
87. Wieser W., Krumschnabel G., Ojwang-Okwor J.P. The energetic of starvation and growth after refeeding in juveniles of three cyprinid species. Environ. Biol. Fish 1992, 33:63-71.
88. Wilkie M.P. Mechanisms of ammonia excretion across fish gills. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 1997, 118:39-50.
89. Wilkie M.P. Ammonia excretion and urea handling by fish gills: present understanding and future research challenges. J. Exp. Zool. 2002, 293:284-301.
90. Wilson R.W., Taylor E.W. Transbranchial ammonia gradients and acid-base responses to high external ammonia concentration in rainbow trout (Oncorhynchus mykiss) acclimated to different salinities. J. Exp. Biol. 1992, 166:95-112.
91. Wilson J.M., Randall D.J., Donowitz M., Vogl A.W., Ip Y.K. Immunolocalization of ion-transport proteins to branchial epithelium mitochondria-rich cells in the mudskipper (Periophthalmodon schlosseri). J. Exp. Biol. 2000, 203:2297-2310.
92. Wilson J.M., Antunes J.C., Bouça P.D., Coimbra J. Osmoregulatory plasticity of the glass eel of Anguilla anguilla: freshwater entry and changes in branchial ion-transport protein expression. Can. J. Fish. Aquat. Sci. 2004, 61:432-442.
93. Wise D.J., Tomasso J.R. Acute toxicity of nitrite to red drum Sciaenops ocellatus: effect of salinity. J. World Aquacult. Soc. 1989, 20:193-198.
94. Wong A.P.S., Bindoff N.L., Church J.A. Large-scale freshening of intermediate waters in the Pacific and Indian oceans. Nature 1999, 400:440-443.
95. Woo N.Y.S., Murat J.C. Studies on the biology of the Red Sea Bream Chrysophrys major III: metabolic response to starvation in different salinities. Mar. Biol. 1981, 61:255-260.
96. Wu Y.C., Lin L.Y., Lee T.H. Na+, K+, 2Cl- cotransporter: a novel marker for identifying freshwater- and seawater-type mitochondria- rich cells in gills of the euryhaline tilapia Oreochromis mossambicus. Zool. Stud. 2003, 42:186-192.
97. Yang T.H., Somero G.N. Effects of feeding and food deprivation on oxygen consumption, muscle protein concentration. J. Exp. Biol. 1993, 181:213-232.
98. Zimmer A.M., Nawata C.M., Wood C.M. Physiological and molecular analysis of the interactive effects of feeding and high environmental ammonia on branchial ammonia excretion and Na+ uptake in freshwater rainbow trout. J. Comp. Physiol. B 2010, 180:1191-1204.