Skip to main content
SpringerLink
Log in

The effects of acute transfer to freshwater on ion transporters of the pharyngeal cavity in European seabass (Dicentrarchus labrax)

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Gene expression of key ion transporters (the Na+/K+-ATPase NKA, the Na+, K+-2Cl− cotransporter NKCC1, and CFTR) in the gills, opercular inner epithelium, and pseudobranch of European seabass juveniles (Dicentrarchus labrax) were studied after acute transfer up to 4 days from seawater (SW) to freshwater (FW). The functional remodeling of these organs was also studied. Handling stress (SW to SW transfer) rapidly induced a transcript level decrease for the three ion transporters in the gills and operculum. NKA and CFTR relative expression level were stable, but in the pseudobranch, NKCC1 transcript levels increased (up to 2.4-fold). Transfer to FW induced even more organ-specific responses. In the gills, a 1.8-fold increase for NKA transcript levels occurs within 4 days post transfer with also a general decrease for CFTR and NKCC1. In the operculum, transcript levels are only slightly modified. In the pseudobranch, there is a transient NKCC1 increase followed by 0.6-fold decrease and 0.8-fold CFTR decrease. FW transfer also induced a density decrease for the opercular ionocytes and goblet cells. Therefore, gills and operculum display similar trends in SW-fish but have different responses in FW-transferred fish. Also, the pseudobranch presents contrasting response both in SW and in FW, most probably due to the high density of a cell type that is morphologically and functionally different compared to the typical gill-type ionocyte. This pseudobranch-type ionocyte could be involved in blood acid-base regulation masking a minor osmotic regulatory capacity of this organ compared to the gills.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Bachmann S, Bostanjoglo M, Schmitt R, Ellison DH (1999) Sodium transport-related proteins in the mammalian distal nephron—distribution, ontogeny and functional aspects. Anat Embryol (Berl) 200(5):447–468

    Article  CAS  Google Scholar 

  • Bertin L (1958) Organes de la respiration aquatique. In: Grassé PP (ed) Traité de zoologie, vol. XIII. Masson & Cie, Paris, pp 1303–1341

    Google Scholar 

  • Blondeau-Bidet E, Bossus M, Maugars G, Farcy E, Lignot JH, Lorin-Nebel C (2016) Molecular characterization and expression of Na+/K+-ATPase α1 isoforms in the European sea bass Dicentrarchus labrax osmoregulatory tissues following salinity transfer. Fish Physiol Biochem 42(6):1647–1664

    Article  PubMed  CAS  Google Scholar 

  • Bodinier C, Lorin-Nebel C, Charmantier G, Boulo V (2009) Influence of salinity on the localisation and expression of the CFTR chloride channel in the ionocytes of Dicentrarchus labrax exposed to seawater and freshwater. Comp Biochem Physiol A Mol Integr Physiol 153:345–351

    Article  PubMed  CAS  Google Scholar 

  • Bossus M, Charmantier G, Blondeau-Bidet E, Valletta B, Boulo V, Lorin-Nebel C (2013) The ClC-3 chloride channel and osmoregulation in the European sea bass, Dicentrarchus labrax. J Comp Physiol B 183(5):641–662

    Article  PubMed  CAS  Google Scholar 

  • Bridges CR, Berenbrink M, Müller R, Waser W (1998) Physiology and biochemistry of the pseudobranch: an unanswered question? Comp Biochem Physiol A 119(1):67–77

    Article  CAS  Google Scholar 

  • Brix KV, Grosell M (2012) Comparative characterization of Na+ transport in Cyprinidon variegatus variegatus and Cyprindon variegatus hubbsi: a model species complex for studying teleost invasion of freshwater. J Exp Biol 215:1199–1209

    Article  PubMed  CAS  Google Scholar 

  • Burns J, Copeland DE (1950) Chloride excretion in the head region of fundulus heteroclitus. Biol Bull 99(3):381–385

    Article  PubMed  CAS  Google Scholar 

  • Bystriansky JS, Schulte PM (2011) Changes in gill H+-ATPase and Na+/K+-ATPase expression and activity during freshwater acclimation of Atlantic salmon (Salmo salar). J Exp Biol 214:2435–2442

    Article  PubMed  CAS  Google Scholar 

  • Bystriansky JS, Richards JG, Schulte PM, Ballantyne JS (2006) Reciprocal expression of gill Na+/K+-ATPase α-subunit isoforms α 1a and α 1b during seawater acclimation of three salmonid fishes that vary in their salinity tolerance. J Exp Biol 209:1848–1858

    Article  PubMed  CAS  Google Scholar 

  • Chang CH, Yang WK, Lin CH, Kang CK, Tang CH, Lee TH (2016) FXYD11 mediated modulation of Na+/K+-ATPase activity in gills of the brackish medaka (Oryzias dancena) when transferred to hypoosmotic or hyperosmotic environments. Comp Biochem Physiol A 194:19–26

    Article  CAS  Google Scholar 

  • Copeland DE (1947) The interrelation of the chloride excreting cell (gill) and the pseudobranch of Fundulus heteroclitus. Biol Bull 93(2):222

    Article  PubMed  CAS  Google Scholar 

  • Cutler CP, Cramb G (2002) Branchial expression of an aquaporin 3 (AQP-3) homologue is downregulated in the European eel (Anguilla anguilla) following seawater acclimation. J Exp Biol 205:2643–2651

    PubMed  CAS  Google Scholar 

  • Dendy LA, Philpott CW, Deter RL (1973) Localization of Na+, K+-ATPase and other enzymes in teleost pseudobranch. II. Morphological characterization of intact pseudobranch, subcellular fractions and plasma membrane structure. J Cell Biol 57:689–703

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Devidas S, Guggino WB (1997) CFTR: domains, structure, and function. J Bioenerg Biomembr 29(5):443–451

    Article  PubMed  CAS  Google Scholar 

  • Edwards SL, Donald JA, Toop T, Donowitz M, Tse CM (2002) Immunolocalisation of sodium/proton exchanger-like proteins in the gills of elasmobranchs. Comp Biochem Physiol A 131:257–265

    Article  CAS  Google Scholar 

  • Esbaugh A, Tufts BL (2006) The structure and function of carbonic anhydrase isozymes in the respiratory system of vertebrates. Respir Physiol Neurobiol 154:185–198

    Article  PubMed  CAS  Google Scholar 

  • Evans CJ, Hartenstein V, Banerjee U (2003) Thicker than blood: conserved mechanisms in Drosophila and vertebrate hematopoiesis. Dev Cell 5(5):673–690

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Giffard-Mena I, Lorin-Nebel C, Charmantier G, Castille R, Boulo V (2008) Adaptation of the sea-bass (Dicentrarchus labrax) to fresh water: role of Aquaporins and Na+/K+-ATPases. Comp Biochem Physiol A Mol Integr Physiol 150:332–338

    Article  PubMed  CAS  Google Scholar 

  • Gilmour KM, Perry SF, Esbaugh AJ, Genz J, Taylor JR, Grosell M (2012) Compensatory regulation of acid–base balance during salinity transfer in rainbow trout (Oncorhynchus mykiss). J Comp Physiol B 182:259–274

    Article  PubMed  CAS  Google Scholar 

  • Hamidian G, Alboghobeish N (2007) Histological study of pseudobranch in Ctenopharyngodon idella. AATEX 14:693–696

    Google Scholar 

  • Harb JM, Devidas DE (1969) Fine structure of the pseudobranch of the flounder Paralichthys lethostigma. A description of a chloride-type cell and pseudobranch-type cell. Z Zellforsch Mikrosk Anat 101(2):167–174

    Article  PubMed  CAS  Google Scholar 

  • Hiroi J, McCormick SD (2007) Variation in salinity tolerance, gill Na+/K+-ATPase, Na+/K+/2Cl– cotransporter and mitochondrion-rich cell distribution among three salmonids Salvelinus namaycush, Salvelinus fontinalis, Salmo salar. J Exp Biol 210:1015–1024

    Article  PubMed  CAS  Google Scholar 

  • Hiroi J, McCormick SD (2012) New insights into gill ionocyte and ion transporter function in euryhaline and diadromous fish. Respir Physiol Neurobiol 184(3):257–268

    Article  PubMed  CAS  Google Scholar 

  • Hwang PP (2009) Ion uptake and acid secretion in zebrafish (Danio rerio). J Exp Biol 212(11):1745–1752

    Article  PubMed  CAS  Google Scholar 

  • Hwang PP, Lee TH (2007) New insights into fish ion regulation and mitochondrion-rich cells. Comp Biochem Physiol 148A(3):479–497

    Article  CAS  Google Scholar 

  • Hwang PP, Lee TH, Lin LY (2011) Ion regulation in fish gills: recent progress in the cellular and molecular mechanisms. Am J Phys 301:R28–R47

    CAS  Google Scholar 

  • Ip YK, Loong AM, Kuah JS, Sim EWL, Chen XL, Wong WP, Lam SH, Delgado ILS, Wilson JM, Chew SF (2012) Roles of three branchial Na+-K+-ATPase α-subunit isoforms in freshwater adaptation, seawater acclimation, and active ammonia excretion in Anabas testudineus. Am J Phys 303:R112–R125

    CAS  Google Scholar 

  • Jensen MK, Madsen SS, Kristiansen K (1998) Osmoregulation and salinity effects on the expression and activity of Na+,K(+)-ATPase in the gills of European sea bass, Dicentrarchus labrax (L.). J Exp Zool 282(3):290–300

    Article  PubMed  CAS  Google Scholar 

  • Kang CK, Yang SY, Lin ST, Lee TH (2015) The inner opercular membrane of the euryhaline teleost: a useful surrogate model for comparisons of different characteristics of ionocytes between seawater- and freshwater-acclimated medaka. Histochem Cell Biol 143(1):69–81

    Article  PubMed  CAS  Google Scholar 

  • Karnaky KJ Jr, Degnan KJ, Zadunaisky JA (1977) Chloride transport across isolated opercular epithelium of killifish: a membrane rich in chloride cells. Science 195(4274):203–205

    Article  PubMed  CAS  Google Scholar 

  • Katoh F, Kaneko T (2003) Short-term transformation and long-term replacement of branchial chloride cells in killifish transferred from seawater to freshwater, revealed by morphofunctional observations and a newly established 'time-differential double fluorescent staining’ technique. J Exp Biol 206(22):4113–4123

    Article  PubMed  Google Scholar 

  • King JAC (1993) Ultrastructure of the pseudobranch in the euryhaline cyprinodontid fish, Rivulus marmoratus. J Morphol 218(2):127–142

    Article  PubMed  Google Scholar 

  • Lasserre P (1971) Increase of Na+K+−dependent ATPase activity in gills and kidneys of two euryhaline marine teleost, Crenimugil labrosus (Risso, 1826) and Dicentrarchus labrax (Linnaeus, 1758), during adaptation to fresh water. Life Sci 10:113–119

    Article  CAS  Google Scholar 

  • Laurent P (1967) La pseudobranchie des Téléostéens, preuves électrophysiologiques de ses fonctions chémoréceptrices et baroréceptrices. C R Acad Sci (Paris) 264:1879–1882

    CAS  Google Scholar 

  • Laurent P, Dunel-Erb S (1984) The pseudobranch: morphology and function. In: Hoar WS, Randall DJ (eds) Fish physiology. Vol. X. Academic Press, New York, pp 285–325

    Google Scholar 

  • Laurent P, Hebibi N (1989) Gill morphometry and fish osmoregulation. Can J Zool 67:3055–3063

    Article  Google Scholar 

  • Laurent P, Dunel S, Barets A (1969) Localisation histochimique de l’anhydrase carbonique au niveau de chémorécepteurs artériels de mammifères, des batraciens et des poisons. Histochimie 17(2):99–107

    Article  PubMed  CAS  Google Scholar 

  • Leiner M (1938) Die Augenkiemendrüse (Pseudobranchie) der Knochenfische. Experimentelle Untersuchungen über ihre physiologische Bedeutung. Z Vergl Physiol 26:416–466

    Google Scholar 

  • Leiner M (1940) Das Atmungsferment Kohlensäureanhydrase im Tierkörper. Naturwissenschaften 28:165–171

    Article  CAS  Google Scholar 

  • Lorin-Nebel C, Boulo V, Bodinier C, Charmantier G (2006) The Na+/K+/2Cl− cotransporter in the sea bass Dicentrarchus labrax during ontogeny: involvement in osmoregulation. J Exp Biol 209:4908–4922

    Article  PubMed  CAS  Google Scholar 

  • Lytle C, Xu JC, Biemesderfer D, Forbush B 3rd (1995) Distribution and diversity of Na-K-cl cotransport proteins: a study with monoclonal antibodies. Am J Phys 269(6):1496–1505

    Article  Google Scholar 

  • Madsen SS, Kiilerich P, Tipsmark CK (2009) Multiplicity of expression of Na+, K+-ATPase α-subunit isoforms in the gill of Atlantic salmon (Salmo salar): cellular localisation and absolute quantification in response to salinity change. J Exp Biol 212:78–88

    Article  PubMed  CAS  Google Scholar 

  • Maetz J (1956) Le rôle biologique de l’anhydrase carbonique chez quelques téléostéens. Bull Biol Fr Belg Suppl XL:1–129

    Google Scholar 

  • Marshall WS, Bryson SE (1998) Transport mechanisms of seawater teleost chloride cells: an inclusive model of a multifunctional cell. Comp Biochem Physiol A 119:97–106

    Article  CAS  Google Scholar 

  • Martoja R, Martoja-Pierson M (1967) Initiation aux techniques de l’histologie animale. Masson & Cie, Paris 1232 p

    Google Scholar 

  • Mattey DL, Moate R, Morgan M (1978) Comparison of ‘pseudobranch’ type and ‘chloride’ type cells in the pseudobranch of marine, freshwater and euryhaline teleosts. J Fish Biol 13(5):535–542

    Article  Google Scholar 

  • Mazon Ade F, Nolan DT, Lock RA, Wendelaar Bonga SE, Fernandes MN (2007) Opercular epithelial cells: a simple approach for in vitro studies of cellular responses in fish. Toxicology 230(1):53–63

    Article  PubMed  CAS  Google Scholar 

  • McCormick SD, Sundell K, Bjornsson BT, Brown CL, Hiroi J (2003) Influence of salinity on the localization of Na+/K+-ATPase, Na+/K+/2Cl− cotransporter (NKCC) and CFTR anion channel in chloride cells of the Hawaiian goby (Stenogobius hawaiiensis). J Exp Biol 206:4575–4583

    Article  PubMed  CAS  Google Scholar 

  • McCormick SD, Regish AM, Christensen AK, Björnsson BT (2013) Differential regulation of sodium-potassium pump isoforms during smolt development and seawater exposure of Atlantic salmon. J Exp Biol 216:1142–1151

    Article  PubMed  CAS  Google Scholar 

  • Munshi JSD, Hughes GM (1981) Gross and fine structure of the pseudo branch of the climbing perch, Anabas testudineus (Bloch). J Fish Biol 19(4):427–438

    Article  Google Scholar 

  • Nebel C, Romestand B, Nègre-Sadargues G, Grousset E, Aujoulat F, Bacal J, Bonhomme F, Charmantier G (2005) Differential freshwater adaptation in juvenile sea-bass Dicentrarchus labrax: involvement of gills and urinary system. J Exp Biol 208:3859–3871

    Article  PubMed  CAS  Google Scholar 

  • Nilsson S (1986) Control of gill blood flow. In: Nilsson S, Holmgren S (eds) Fish physiology: recent advances. Croom Helm, London, pp 86–101

    Chapter  Google Scholar 

  • Parry G, Holliday FGT (1960) An experimental analysis of the function of the pseudobranch in teleosts. J Exp Biol 37:344–353

    Google Scholar 

  • Pelis RM, Zydlewski J, McCormick SD (2001) Gill Na(+)-K(+)-2Cl(−) cotransporter abundance and location in Atlantic salmon: effects of seawater and smolting. Am J Physiol Regul Integr Comp Physiol 280(6):1844–1852

    Article  Google Scholar 

  • Quinn MCJ, Veillette PA, Young G (2003) Pseudobranch and gill Na+, K+-ATPase activity in juvenile Chinook salmon, Oncorhynchus tshawytscha: developmental changes and effects of growth hormone, cortisol and seawater transfer. Comp Biochem Physiol A 135:249–262

    Article  CAS  Google Scholar 

  • Rahim SM, Mazlan AG, Simon KD, Delaunoy JP, Laurent P (2014) Immunocytochemical localization of carbonic anhydrase in the pseudobranch tissue of the rainbow trout Oncorhynchus mykiss. J Zhejiang Univ-Sci B (Biomed & Biotechnol) 15(2):194–200

    Article  CAS  Google Scholar 

  • Randall DJ, Baumgarten D, Malyusz M (1972) The relationship between gas and ion transfer across the gills of fishes. Comp Biochem Physiol A 41:629–637

    Article  CAS  Google Scholar 

  • Reilly BD, Cramp RL, Wilson JM, Campbell HA, Franklin CE (2011) Branchial osmoregulation in the euryhaline bull shark, Carcharhinus leucas: a molecular analysis of ion transporters. J Exp Biol 214:2883–2895

    Article  PubMed  CAS  Google Scholar 

  • Richards JG, Semple JW, Bystriansky JS, Schulte PM (2003) Na+/ K+-ATPase α-isoform switching in gills of rainbow trout (Oncorhynchus mykiss) during salinity transfer. J Exp Biol 206:4475–4486

    Article  PubMed  CAS  Google Scholar 

  • Robertson LM, Val AL, Almeida-Val VF, Wood CM (2015) Ionoregulatory aspects of the osmorespiratory compromise during acute environmental hypoxia in 12 tropical and temperate teleosts. Physiol Biochem Zool 88:357–370

    Article  PubMed  Google Scholar 

  • Rombough P (2002) Gills are needed for ionoregulation before they are needed for O2 uptake in developing zebrafish, Danio rerio. J Exp Biol 205:1787–1794

    PubMed  Google Scholar 

  • 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: 55–58

  • Saroglia M, Terova G, De Stradis A, Caputo A (2002) Morphometric adaptations of sea bass gills to different dissolved oxygen partial pressures. J Fish Biol 60:1423–1430

    Article  Google Scholar 

  • Saroglia M, Caricato G, Frittella F, Brambilla F, Terova G (2010) Dissolved oxygen regimen (PO2) may affect osmorespiratory compromise in European sea bass (Dicentrarchus labrax, L.). Ital J Anim Sci 9(e15):73–78

    Google Scholar 

  • Scott GR, Richards JG, Forbush B, Isenring P, Schulte PM (2004) Changes in gene expression in gills of the euryhaline killifish Fundulus heteroclitus after abrupt salinity transfer. Am J Phys 287:300–309

    Article  Google Scholar 

  • Scott GR, Claiborne JB, Edwards SL, Schulte PM, Wood CM (2005) Gene expression after freshwater transfer in gills and opercular epithelia of killifish: insight into divergent mechanisms of ion transport. J Exp Biol 208(14):2719–2729

    Article  PubMed  CAS  Google Scholar 

  • Shen WP, Horng JL, Lin LY (2011) Functional plasticity of mitochondrion-rich cells in the skin of euryhaline medaka larvae (Oryzias latipes) subjected to salinity changes. Am J Phys 300:R858–R868

    CAS  Google Scholar 

  • Shieh YE, Tsai RS, Hwang PP (2003) Morphological modification of mitochondria-rich cells of the opercular epithelium of freshwater tilapia, Oreochromis mossambicus, acclimated to low chloride levels. Zool Stud 42:522–528

    Google Scholar 

  • Singh ON, Ghosh TK, Munshi JSD (1986) Structure of pseudobranch of two clupeoid fishes, Hilsa ilisha and Gadusia chapra. Proc Indian natn Sci Acad 52(2):274–279

    Google Scholar 

  • Sobotka H, Kann S (1941) Carbonic anhydrase in fish and invertebrates. J Cell Comp Physiol 17:341–334

    Article  CAS  Google Scholar 

  • Tang CH, Lee TH (2011) Morphological and ion-transporting plasticity of branchial mitochondrion-rich cells in the euryhaline spotted green pufferfish, Tetraodon nigroviridis. Zool Stud 50:31–42

    Google Scholar 

  • Tipsmark CK, Madsen SS, Ceidelin M, Christensen AS, Cutler CP, Cramb G (2002) Dynamics of Na+, K+, 2Cl− cotransporter and Na+, K+-ATPase expression in the branchial epithelium of brown trout (Salmo trutta) and Atlantic salmon (Salmo salar). J Exp Zool 293:106–118

    Article  PubMed  CAS  Google Scholar 

  • Tipsmark CK, Breves JP, Seale AP, Lerner DT, Hirano T, Grau EG (2011) Switching of Na+, K+-ATPase isoforms by salinity and prolactin in the gill of a cichlid fish. J Endocrinol 209(2):237–244

    Article  PubMed  CAS  Google Scholar 

  • Tse WK, Au DW, Wong CK (2006) Characterization of ion channel and transporter mRNA expressions in isolated gill chloride and pavement cells of seawater acclimating eels. Biochem Biophys Res 346:1181–1190

    Article  CAS  Google Scholar 

  • Urbina MA, Schulte PM, Bystriansky JS, Glover CN (2013) Differential expression of Na+, K+-ATPase α-1 isoforms during seawater acclimation in the amphidromous galaxiid fish Galaxias maculatus. J Comp Physiol B 183:345–357

    Article  PubMed  CAS  Google Scholar 

  • Varsamos S, Diaz J-P, Charmantier G, Flik G, Blasco C, Connes R (2002) Branchial chloride cells in sea bass (Dicentrarchus labrax) adapted to fresh water, seawater, and doubly concentrated seawater. J Exp Zool 293:12–26

    Article  PubMed  CAS  Google Scholar 

  • Varsamos S, Nebel C, Charmantier G (2005) Ontogeny of osmoregulation in postembryonic fish: a review. Comp Biochem Physiol A 141:401–429

    Article  CAS  Google Scholar 

  • Wang PJ, Lin CH, Hwang LY, Huang CL, Lee TH, Hwang PP (2009) Differential responses in gills of euryhaline tilapia, Oreochromis mossambicus, to various hyperosmotic shocks. Comp Biochem Physiol A 152:544–551

    Article  CAS  Google Scholar 

  • Wittenberg JB, Haedrich R (1974) The choroid rete mirabile of the fish eye. II. Distribution and relation to the pseudobranch and to the swimbladder rete mirabile. Biol Bull 146(1):137–156

    Article  PubMed  CAS  Google Scholar 

  • Yang WK, Kang CK, Chang CH, Hsu AD, Lee TH, Hwang PP (2013) Expression profiles of branchial FXYD proteins in the brackish medaka Oryzias dancena: a potential saltwater fish model for studies of osmoregulation. PLoS One 8:e55470

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang SH, Kang CK, Kung HN, Lee TH (2014) The lamellae-free-type pseudobranch of the euryhaline milkfish (Chanos chanos) is a Na(+), K(+)-ATPase-abundant organ involved in hypoosmoregulation. Comp Biochem Physiol 170:15–25

    Article  CAS  Google Scholar 

  • Yang SH, Kang CK, Hu YC, Yen LC, Tsai SC, Hsieh YL, Lee TH (2015) Comparisons of two types of teleostean pseudobranchs, silver moony (Monodactylus argenteus) and tilapia (Oreochromis mossambicus), with salinity-dependent morphology and ion transporter expression. J Comp Physiol B 185(6):677–693

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

JH Lignot is grateful to Pierre Laurent, for the numerous and valuable scientific conversations held between 2001 and 2010 at the DEPE-IPHC (formerly CEPE) of Strasbourg, France. We also thank the technical staff of the IFREMER experimental research station of Palavas-les-Flots for providing us with the animals used in this study, the MRI imaging center, and the electron microscopy facility of the University of Montpellier (SCME), and Munro Language Services for proofreading the manuscript.

Author information

Authors and Affiliations

  1. University of Montpellier, UMR MARBEC, MARBEC (IRD – Ifremer – Univ. Montpellier - CNRS), Place Eugène Bataillon, 34095, Montpellier Cedex 5, France

    Gersende Maugars, Marie-Chanteuse Manirafasha, Evelyse Grousset & Jehan-Hervé Lignot

  2. Ifremer, UR Lagons, Ecosystèmes et Aquaculture Durable, Nouvelle-Calédonie, France

    Viviane Boulo

Authors
  1. Gersende Maugars
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marie-Chanteuse Manirafasha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Evelyse Grousset
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Viviane Boulo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jehan-Hervé Lignot
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jehan-Hervé Lignot.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maugars, G., Manirafasha, MC., Grousset, E. et al. The effects of acute transfer to freshwater on ion transporters of the pharyngeal cavity in European seabass (Dicentrarchus labrax). Fish Physiol Biochem 44, 1393–1408 (2018). https://doi.org/10.1007/s10695-018-0529-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-018-0529-6

Keywords

Search

Navigation