Abstract
In teleosts, the regulation of hydromineral balance has a direct impact on several physiological functions, biochemical processes, and can influence behaviour, distribution and survival. As European sea bass Dicentrarchus labrax undertake seasonal migrations from seawater (SW) to brackish, estuarine and fresh water (FW) in their habitat, this study investigates their capacity to tolerate fresh water and explores intraspecific variations in physiological responses. Juvenile D. labrax were transferred from SW to FW at various ages. Freshwater-tolerant and non-tolerant phenotypes were discriminated according to behavioural and morphological characteristics. About 30% of the fish exposed to FW were identified as freshwater intolerant following FW challenges performed at different ages. Interestingly, intolerant fish exhibited the same phenotypic traits: erratic swimming, lower speed, isolation from the shoal and darker colour. Freshwater-intolerant fish were also characterised by a significant lower blood osmolality compared to tolerant fish, and significantly lower Na+/K+-ATPase α1a expression in the posterior kidney. An imbalance in ion regulatory mechanisms was further confirmed by a blood Na+/Cl− ratio imbalance observed in some freshwater-intolerant fish. The analysis of glucocorticoid and mineralocorticoid receptor expression levels in gills and kidney revealed significant differences between freshwater-intolerant and -tolerant fish in both organs, suggesting differential stress-related responses. This study clearly shows an intraspecific difference in the responses following FW transfer with a decreased renal ion uptake capacity as a major cause for freshwater intolerance.
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Ágústsson T, Sundell K, Sakamoto T, Ando M, Björnsson BT (2003) Pituitary gene expression of somatolactin, prolactin, and growth hormone during Atlantic salmon parr-smolt transformation. Aquaculture 222:229–238. https://doi.org/10.1016/S0044-8486(03)00124-8
Allegrucci G, Fortunato C, Cataudella S, Sbordoni V (1994) Acclimation to fresh water of the sea bass: evidence of selective mortality of allozyme genotypes. In: Beaumont AR (ed) Genetics and evolution of aquatic organisms. Chapman & Hall, London, pp 487–502
Anastasiadi D, Díaz N, Piferrer F (2017) Small ocean temperature increases elicit stage-dependent changes in DNA methylation and gene expression in a fish, the European sea bass. Sci Rep 7:1–12. https://doi.org/10.1038/s41598-017-10861-6
Angers B, Castonguay E, Massicotte R (2010) Environmentally induced phenotypes and DNA methylation: how to deal with unpredictable conditions until the next generation and after. Mol Ecol 19:1283–1295. https://doi.org/10.1111/j.1365-294X.2010.04580.x
Backström T, Brännäs E, Nilsson J, Magnhagen C (2014) Behaviour, physiology and carotenoid pigmentation in Arctic charr Salvelinus alpinus. J Fish Biol 84:1–9. https://doi.org/10.1111/jfb.12240
Barnabé G (1989) L’élevage du loup et de la daurade. In: Barnabé G (ed) Technique et Documentation- Lavoisier. Aquacultur, Paris, pp 675–720
Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517–525. https://doi.org/10.1093/icb/42.3.517
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 42:1647–1664. https://doi.org/10.1007/s10695-016-0247-x
Blondeau-Bidet E, Hiroi J, Lorin-Nebel C (2019) Ion uptake pathways in European sea bass Dicentrarchus labrax. Gene 692:126–137. https://doi.org/10.1016/j.gene.2019.01.006
Bossus MC, Madsen SS, Tipsmark CK (2015) Functional dynamics of claudin expression in Japanese medaka (Oryzias latipes): response to environmental salinity. Comp Biochem Physiol Part A Mol Integr Physiol 187:74–85. https://doi.org/10.1016/j.cbpa.2015.04.017
Bossus MC, Bollinger RJ, Reed PJ, Tipsmark CK (2017) Prolactin and cortisol regulate branchial claudin expression in Japanese medaka. Gen Comp Endocrinol 240:77–83. https://doi.org/10.1016/j.ygcen.2016.09.010
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 Part D Genom Proteom 2:74–83. https://doi.org/10.1016/j.cbd.2006.12.002
Brauner CJ, Baker DW (2009) Cardio-respiratory control in vertebrates: comparative and evolutionary aspects. Cardiol Respir Control Vert Comp Evol Asp. https://doi.org/10.1007/978-3-540-93985-6
Bui P, Kelly SP (2014) Claudin-6, -10d and -10e contribute to seawater acclimation in the euryhaline puffer fish Tetraodon nigroviridis. J Exp Biol 217:1758–1767. https://doi.org/10.1242/jeb.099200
Bury NR, Sturm A, Le Rouzic P, Lethimonier C, Ducouret B, Guiguen Y, Robinson-Rechavi M, Laudet V, Rafestin-Oblin ME, Prunet P (2003) Evidence for two distinct functional glucocorticoid receptors in teleost fish. J Mol Endocrinol 31:141–156. https://doi.org/10.1677/jme.0.0310141
Carbonara P, Dioguardi M, Cammarata M, Zupa W, Vazzana M, Spedicato MT, Lembo G (2019) Basic knowledge of social hierarchies and physiological profile of reared sea bass Dicentrarchus labrax (L.). PLoS One 14:e0208688. https://doi.org/10.1371/journal.pone.0208688
Cardona L (2006) Habitat selection by grey mullets (Osteichthyes: Mugilidae) in Mediterranean estuaries: the role of salinity. Sci Mar 70:443–455. https://doi.org/10.3989/scimar.2006.70n3443
Caruso G, Genovese L, Maricchiolo G, Modica A (2005) Haematological, biochemical and immunological parameters as stress indicators in Dicentrarchus labrax and Sparus aurata farmed in off-shore cages. Aquac Int 13:67–73. https://doi.org/10.1007/s10499-004-9031-5
Caruso G, Denaro MG, Caruso R, Mancari F, Genovese L, Maricchiolo G (2011) Response to short term starvation of growth, haematological, biochemical and non-specific immune parameters in European sea bass (Dicentrarchus labrax) and blackspot sea bream (Pagellus bogaraveo). Mar Environ Res 72:46–52. https://doi.org/10.1016/j.marenvres.2011.04.005
Castanheira MF, Martínez-Páramo S, Figueiredo F, Cerqueira M, Millot S, Oliveira CCV, Martins CIM, Conceição LEC (2016) Are coping styles consistent in the teleost fish Sparus aurata through sexual maturation and sex reversal? Fish Physiol Biochem 42:1441–1452. https://doi.org/10.1007/s10695-016-0231-5
Cataudella S, Allegrucci G, Bronzi P, Cataldi E, Cioni C, Corti M, Crosetti D, De Merich D, Fortunato C, Garibaldi L, Loy A, Marino G, Sola L, Sbordoni V (1991) Multidisciplinary approach to the optimisation of sea bass (Dicentrarchus labrax) rearing in freshwater—basic morpho-physiology and osmoregulation. EAS Spec Publ 14:56–57
Chasiotis H, Kolosov D, Kelly SP (2012) Permeability properties of the teleost gill epithelium under ion-poor conditions. Am J Physiol Integr Comp Physiol 302:R727–R739. https://doi.org/10.1152/ajpregu.00577.2011
Claiborne J, Walton J, Compton-Mccullough D (1994) Acid-base regulation, branchial transfers and renal output in a marine teleost fish (the long-horned sculpin Myoxocephalus octodecimspinosus) during exposure to low salinities. J Exp Biol 193:79–95
Conde-Sieira M, Valente LMP, Hernández-Pérez J, Soengas JL, Míguez JM, Gesto M (2018) Short-term exposure to repeated chasing stress does not induce habituation in Senegalese sole, Solea senegalensis. Aquaculture 487:32–40. https://doi.org/10.1016/j.aquaculture.2018.01.003
Corey E, Linnansaari T, Cunjak RA, Currie S (2017) Physiological effects of environmentally relevant, multi-day thermal stress on wild juvenile Atlantic salmon (Salmo salar). Conserv Physiol 5:1–13. https://doi.org/10.1093/conphys/cox014
Costa DC, Mattioli CC, Silva WS, Takata R, Leme FOP, Oliveira AL, Luz RK (2017) The effect of environmental colour on the growth, metabolism, physiology and skin pigmentation of the carnivorous freshwater catfish Lophiosilurus alexandri. J Fish Biol 90:922–935. https://doi.org/10.1111/jfb.13208
Crozier LG, Hutchings JA (2014) Plastic and evolutionary responses to climate change in fish. Evol Appl 7:68–87. https://doi.org/10.1111/eva.12135
Cruz SA, Lin CH, Chao PL, Hwang PP (2013) Glucocorticoid receptor, but not mineralocorticoid receptor, mediates cortisol regulation of epidermal ionocyte development and ion transport in zebrafish (Danio rerio). PLoS One. https://doi.org/10.1371/journal.pone.0077997
De Chaumont F, Dallongeville S, Chenouard N, Hervé N, Pop S, Provoost T, Meas-Yedid V, Pankajakshan P, Lecomte T, Le Montagner Y, Lagache T, Dufour A, Olivo-Marin J-C (2012) Icy: an open bioimage informatics platform for extended reproducible research. Nat Methods 9:690
Debat V, David P (2001) Mapping phenotype: canalization, plasticity and developmental stability. Trends Ecol Evol 16:555–561. https://doi.org/10.1016/S0169-5347(01)02266-2
Dendrinos P, Thorpe JP (1985) Effects of reduced salinity on growth and body composition in the European bass Dicentrarchus labrax (L.). Aquaculture 49:333–358. https://doi.org/10.1016/0044-8486(85)90090-0
Dufour V, Cantou M, Lecomte F (2009) Identification of sea bass (Dicentrarchus labrax) nursery areas in the north-western Mediterranean Sea. J Mar Biol Assoc UK 89:1367–1374. https://doi.org/10.1017/S0025315409000368
Dufresne F, Stift M, Vergilino R, Mable BK (2014) Recent progress and challenges in population genetics of polyploid organisms: an overview of current state-of-the-art molecular and statistical tools. Mol Ecol 23:40–69. https://doi.org/10.1111/mec.12581
Evans DH, Clairborne JB (2009) Osmotic and ionic regulation in fishes. Osmotic and ionic regulation: cells and animals, Evans DH. CRC Press, Boca Raton, pp 295–366
Fanouraki E, Mylonas CC, Papandroulakis N, Pavlidis M (2011) Species specificity in the magnitude and duration of the acute stress response in Mediterranean marine fish in culture. Gen Comp Endocrinol 173:313–322. https://doi.org/10.1016/j.ygcen.2011.06.004
Forsman A (2015) Rethinking phenotypic plasticity and its consequences for individuals, populations and species. Heredity (Edinb) 115:276–284. https://doi.org/10.1038/hdy.2014.92
Franklin CE, Forster ME, Davison W (1992) Plasma cortisol and osmoregulatory changes in sockeye salmon transferred to sea water: comparison between successful and unsuccessful adaptation. J Fish Biol 41:113–122. https://doi.org/10.1111/j.1095-8649.1992.tb03174.x
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. https://doi.org/10.1016/j.cbpa.2008.04.004
Goss GG, Perry SF, Wood CM, Laurent P (1992) Mechanisms of ion and acid-base regulation at the gills of freshwater fish. J Exp Zool 263:143–159. https://doi.org/10.1002/jez.1402630205
Greenwood AK, Butler PC, White RB, Demarco U, Pearce D, Fernald RD (2003) Multiple corticosteroid receptors in a teleost fish: distinct sequences, expression patterns, and transcriptional activities. Endocrinology 144:4226–4236. https://doi.org/10.1210/en.2003-0566
Guinand B, Quéré N, Cerqueira F, Desmarais E, Bonhomme F (2014) Fitness difference between cryptic salinity-related phenotypes of sea bass (Dicentrarchus labrax). Sci Mar 78:493–503. https://doi.org/10.3989/scimar.03992.02c
Guinand B, Quéré N, Desmarais E, Lagnel J, Tsigenopoulos CS, Bonhomme F (2015) From the laboratory to the wild: salinity-based genetic differentiation of the European sea bass (Dicentrarchus labrax) using gene-associated and gene-independent microsatellite markers. Mar Biol 162:515–538. https://doi.org/10.1007/s00227-014-2602-8
Hawes NA, Tremblay LA, Pochon X, Dunphy B, Fidler AE, Smith KF (2018) Effects of temperature and salinity stress on DNA methylation in a highly invasive marine invertebrate, the colonial ascidian Didemnum vexillum. PeerJ 6:e5003. https://doi.org/10.7717/peerj.5003
Houslay TM, Earley RL, Young AJ, Wilson AJ (2018) Habituation and individual variation in the endocrine stress response in the Trinidadian guppy (Poecilia reticulata). Gen Comp Endocrinol 270:113–122. https://doi.org/10.1016/j.ygcen.2018.10.013
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 282:290–300
Jeremias G, Barbosa J, Marques S, De Schamphelaere KA, Van Nieuwerburgh F, Deforce D, Gonçalves F, Pereira J, Asselman J (2018) Transgenerational inheritance of DNA hypomethylation in Daphnia magna in response to salinity stress. Environ Sci Technol. https://doi.org/10.1021/acs.est.8b03225
Jiang J, Young G, Kobayashi T, Nagahama Y (1998) Eel (Anguilla japonica) testis 11β-hydroxylase gene is expressed in interrenal tissue and its product lacks aldosterone synthesizing activity. Mol Cell Endocrinol 146:207–211. https://doi.org/10.1016/s0303-7207(98)00147-6
Kelley DF (1988) The importance of estuaries for sea-bass, Dicentrarchus labrax (L.). J Fish Biol 33:25–33. https://doi.org/10.1111/j.1095-8649.1988.tb05555.x
Kelly SP, Chasiotis H (2011) Glucocorticoid and mineralocorticoid receptors regulate paracellular permeability in a primary cultured gill epithelium. J Exp Biol 214:2308–2318. https://doi.org/10.1242/jeb.055962
Kesbiç OS, Yiğit M, Acar Ü (2016) Effects of Tank Color on Growth Performance and Nitrogen Excretion of European Sea bass (Dicentrarchus labrax) Juveniles. Proc Natl Acad Sci India Sect B Biol Sci 86:205–210. https://doi.org/10.1007/s40011-014-0441-5
Khan UW, Øverli Ø, Hinkle PM, Pasha FA, Johansen IB, Berget I, Silva PIM, Kittilsen S, Höglund E, Omholt SW, Vage DI (2016) A novel role for pigment genes in the stress response in rainbow trout (Oncorhynchus mykiss). Sci Rep 6:1–11. https://doi.org/10.1038/srep28969
Kiilerich P, Kristiansen K, Madsen SS (2007a) Cortisol regulation of ion transporter mRNA in Atlantic salmon gill and the effect of salinity on the signaling pathway. J Endocrinol 194:417–427. https://doi.org/10.1677/JOE-07-0185
Kiilerich P, Kristiansen K, Madsen SS (2007b) Hormone receptors in gills of smolting Atlantic salmon, Salmo salar: expression of growth hormone, prolactin, mineralocorticoid and glucocorticoid receptors and 11β-hydroxysteroid dehydrogenase type 2. Gen Comp Endocrinol 152:295–303. https://doi.org/10.1016/j.ygcen.2006.12.018
Kiilerich P, Milla S, Sturm A, Valotaire C, Chevolleau S, Giton F, Terrien X, Fiet J, Fostier A, Debrauwer L, Prunet P (2011) Implication of the mineralocorticoid axis in rainbow trout osmoregulation during salinity acclimation. J Endocrinol 209:221–235. https://doi.org/10.1530/JOE-10-0371
Kittilsen S, Schjolden J, Beitnes-Johansen I, Shaw JC, Pottinger TG, Sørensen C, Braastad BO, Bakken M, Øverli Ø (2009) Melanin-based skin spots reflect stress responsiveness in salmonid fish. Horm Behav 56:292–298. https://doi.org/10.1016/j.yhbeh.2009.06.006
Kokou F, Con P, Barki A, Nitzan T, Slosman T, Mizrahi I, Cnaani A (2019) Short- and long-term low-salinity acclimation effects on the branchial and intestinal gene expression in the European seabass (Dicentrarchus labrax). Comp Biochem Physiol Part A Mol Integr Physiol 231:11–18. https://doi.org/10.1016/j.cbpa.2019.01.018
Korte SM, Olivier B, Koolhaas JM (2007) A new animal welfare concept based on allostasis. Physiol Behav 92:422–428. https://doi.org/10.1016/j.physbeh.2006.10.018
Lai F, Fagernes CE, Jutfelt F, Nilsson GE (2016) Expression of genes involved in brain GABAergic neurotransmission in three-spined stickleback exposed to near-future CO2. Conserv Physiol 4:1–15. https://doi.org/10.1093/conphys/cow068
Lasserre P, Gallis JL (1975) Osmoregulation and differential penetration of two grey mullets, Chelon labrosus (Risso) and Liza ramada (Risso) in estuarine fish ponds. Aquaculture 5:323–344. https://doi.org/10.1016/0044-8486(75)90053-8
Lemaire C, Allegrucci G, Naciri M, Bahri-Sfar L, Kara H, Bonhomme F (2000) Do discrepancies between microsatellite and allozyme variation reveal differential selection between sea and lagoon in the sea bass (Dicentrarchus labrax)? Mol Ecol 9:457–467. https://doi.org/10.1046/j.1365-294X.2000.00884.x
Liew HJ, Fazio A, Faggio C, Blust R, De Boeck G (2015) Cortisol affects metabolic and ionoregulatory responses to a different extent depending on feeding ration in common carp, Cyprinus carpio. Comp Biochem Physiol Part A Mol Integr Physiol 189:45–57. https://doi.org/10.1016/j.cbpa.2015.07.011
Lin CH, Tsai RS, Lee TH (2004) Expression and distribution of Na, K-ATPase in gill and kidney of the spotted green pufferfish, Tetraodon nigroviridis, in response to salinity challenge. Comp Biochem Physiol A Mol Integr Physiol 138(3):287–295. https://doi.org/10.1016/j.cbpb.2004.04.005
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. https://doi.org/10.1242/jeb.02591
Marshall WS, Grosell M (2006) Ion Transport, Osmoregulation, and Acid-Base Balance. In: Evans DH, Claiborne JB (eds) The physiology of fishes. CRC Press, Boca Raton, FL, pp 177–214
Martins CIM, Galhardo L, Noble C, Damsgård B, Spedicato MT, Zupa W, Beauchaud M, Kulczykowska E, Massabuau JC, Carter T, Planellas SR, Kristiansen T (2012) Behavioural indicators of welfare in farmed fish. Fish Physiol Biochem 38:17–41. https://doi.org/10.1007/s10695-011-9518-8
Masroor W, Farcy E, Gros R, Lorin-Nebel C (2018) Effect of combined stress (salinity and temperature) in European sea bass Dicentrarchus labrax osmoregulatory processes. Comp Biochem Physiol Part A Mol Integr Physiol 215:45–54. https://doi.org/10.1016/j.cbpa.2017.10.019
Massicotte R, Whitelaw E, Angers B (2011) DNA methylation: a source of random variation in natural populations. Epigenetics 6:422–428. https://doi.org/10.4161/epi.6.4.14532
McCairns RJS, Bernatchez L (2010) Adaptive divergence between freshwater and marine sticklebacks: insights into the role of phenotypic plasticity from an integrated analysis of candidate gene expression. Evolution 64:1029–1047. https://doi.org/10.1111/j.1558-5646.2009.00886.x
McCormick SD (2001) Endocrine control of osmoregulation in teleost fish. Am Zool 41:781–794
McCormick SD (2013) Smolt physiology and endocrinology. In: McCormick SD, Farrell AP, Brauner CJ (eds) Euryhaline fishes. Academic Press, Oxford, pp 199–251
McCormick SD, Regish A, O’Dea MF, Shrimpton JM (2008) Are we missing a mineralocorticoid in teleost fish? Effects of cortisol, deoxycorticosterone and aldosterone on osmoregulation, gill Na+ , K+ -ATPase activity and isoform mRNA levels in Atlantic salmon. Gen Comp Endocrinol 157:35–40. https://doi.org/10.1016/j.ygcen.2008.03.024
McKenzie DJ, Vergnet A, Chatain B, Vandeputte M, Desmarais E, Steffensen JF, Guinand B (2014) Physiological mechanisms underlying individual variation in tolerance of food deprivation in juvenile European sea bass, Dicentrarchus labrax. J Exp Biol 217:3283–3292
Mercier L, Mouillot D, Bruguier O, Vigliola L, Darnaude AM (2012) Multi-element otolith fingerprints unravel sea-lagoon lifetime migrations of gilthead sea bream Sparus aurata. Mar Ecol Prog Ser 444:175–194. https://doi.org/10.3354/meps09444
Metzger DCH, Schulte PM (2017) Persistent and plastic effects of temperature on DNA methylation across the genome of threespine stickleback (Gasterosteus aculeatus). Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2017.1667
Mitter K, Kotoulas G, Magoulas A, Mulero V, Sepulcre P, Figueras A, Novoa B, Sarropoulou E (2009) Evaluation of candidate reference genes for QPCR during ontogenesis and of immune-relevant tissues of European seabass (Dicentrarchus labrax). Comp Biochem Physiol B Biochem Mol Biol 153:340–347. https://doi.org/10.1016/j.cbpb.2009.04.009
Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268. https://doi.org/10.1023/A:1008924418720
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
Nilsson GE (2007) Gill remodeling in fish - a new fashion or an ancient secret? J Exp Biol 210(14):2403–2409
Nilsson GE, Dixson DL, Domenici P, McCormick MI, Sørensen C, Watson SA, Munday PL (2012) Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nat Clim Chang 2:201–204. https://doi.org/10.1038/nclimate1352
Øverli Ø, Sørensen C, Pulman KGT, Pottinger TG, Korzan W, Summers CH, Nilsson GE (2007) Evolutionary background for stress-coping styles: relationships between physiological, behavioral, and cognitive traits in non-mammalian vertebrates. Neurosci Biobehav Rev 31:396–412. https://doi.org/10.1016/j.neubiorev.2006.10.006
Parsons KJ, Sheets HD, Skúlason S, Ferguson MM (2011) Phenotypic plasticity, heterochrony and ontogenetic repatterning during juvenile development of divergent arctic charr (Salvelinus alpinus). J Evol Biol 24:1640–1652. https://doi.org/10.1111/j.1420-9101.2011.02301.x
Pavlidis M, Karantzali E, Fanouraki E, Barsakis C, Kollias S, Papandroulakis N (2011) Onset of the primary stress in European sea bass Dicentrarchus labrax, as indicated by whole body cortisol in relation to glucocorticoid receptor during early development. Aquaculture 315:125–130. https://doi.org/10.1016/j.aquaculture.2010.09.013
Pérez-Ruzafa A, Marcos C, Pérez-Ruzafa IM, Pérez-Marcos M (2011) Coastal lagoons: “transitional ecosystems” between transitional and coastal waters. J Coast Conserv 15:369–392. https://doi.org/10.1007/s11852-010-0095-2
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucl Acids Res 29:e45
Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP (2010) Phenotypic plasticity’s impacts on diversification and speciation. Trends Ecol Evol 25:459–467. https://doi.org/10.1016/j.tree.2010.05.006
Pierce DW, Gleckler PJ, Barnett TP, Santer BD, Durack PJ (2012) The fingerprint of human-induced changes in the ocean’s salinity and temperature fields. Geophys Res Lett 39:2–7. https://doi.org/10.1029/2012GL053389
Pottinger TG, Carrick TR (2001) ACTH does not mediate divergent stress responsiveness in rainbow trout. Comp Biochem Physiol A Mol Integr Physiol 129:399–404
Rigal F, Chevalier T, Lorin-Nebel C, Charmantier G, Tomasini J-A, Aujoulat F, Berrebi P (2008) Osmoregulation as a potential factor for the differential distribution of two cryptic gobiid species, Pomatoschistus microps and P. marmoratus in French Mediterranean lagoons. Sci Mar 72:469–476. https://doi.org/10.3989/scimar.2008.72n3469
Sadoul B, Alfonso S, Bessa E, Bouchareb A, Blondeau-Bidet E, Clair P, Chatain B, Bégout ML, Geffroy B (2018) Enhanced brain expression of genes related to cell proliferation and neural differentiation is associated with cortisol receptor expression in fishes. Gen Comp Endocrinol 267:76–81. https://doi.org/10.1016/j.ygcen.2018.06.001
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
Samaras A, Pavlidis M (2018) Regulation of divergent cortisol responsiveness in European sea bass, Dicentrarchus labrax L. PLoS One. https://doi.org/10.1371/journal.pone.0202195
Samaras A, Dimitroglou A, Sarropoulou E, Papaharisis L, Kottaras L, Pavlidis M (2016) Repeatability of cortisol stress response in the European sea bass (Dicentrarchus labrax) and transcription differences between individuals with divergent responses. Sci Rep 6:1–11. https://doi.org/10.1038/srep34858
Scott GR, Richards JG, Forbush B, Isenring P, Schulte PM (2004a) Changes in gene expression in gills of the euryhaline killifish Fundulus heteroclitus after abrupt salinity transfer. Am J Physiol Cell Physiol 287:C300–C309. https://doi.org/10.1152/ajpcell.00054.2004
Scott GR, Rogers JT, Richards JG, Wood CM, Schulte PM (2004b) Intraspecific divergence of ionoregulatory physiology in the euryhaline teleost Fundulus heteroclitus: possible mechanisms of freshwater adaptation. J Exp Biol 207:3399–3410. https://doi.org/10.1242/jeb.01130
Scott GR, Keir KR, Schulte PM (2005a) Effects of spironolactone and RU486 on gene expression and cell proliferation after freshwater transfer in the euryhaline killifish. J Comp Physiol B Biochem Syst Environ Physiol 175:499–510. https://doi.org/10.1007/s00360-005-0014-2
Scott GR, Claiborne JB, Edwards SL, Schulte PM, Wood CM (2005b) Gene expression after freshwater transfer in gills and opercular epithelia of killifish: insight into divergent mechanisms of ion transport. J Exp Biol 208:2719–2729. https://doi.org/10.1242/jeb.01688
Sloman KA, Desforges PR, Gilmour KM (2001) Evidence for a mineralocorticoid-like receptor linked to branchial chloride cell proliferation in freshwater rainbow trout. J Exp Biol 204:3953–3961
Sturm A, Bury N, Dengreville L, Fagart J, Flouriot G, Rafestin-Oblin ME, Prunet P (2005) 11-Deoxycorticosterone is a potent agonist of the rainbow trout (Oncorhynchus mykiss) mineralocorticoid receptor. Endocrinology 146:47–55. https://doi.org/10.1210/en.2004-0128
Takahashi H, Sakamoto T (2013) The role of “mineralocorticoids” in teleost fish: relative importance of glucocorticoid signaling in the osmoregulation and “central” actions of mineralocorticoid receptor. Gen Comp Endocrinol 181:223–228. https://doi.org/10.1016/j.ygcen.2012.11.016
Tine M, Kuhl H, Gagnaire PA, Louro B, Desmarais E, Martins RST, Hecht J, Knaust F, Belkhir K, Klages S, Dieterich R, Stueber K, Piferrer F, Guinand B, Bierne N, Volckaert FAM, Bargelloni L, Power DM, Bonhomme F, Canario AVM, Reinhardt R (2014) European sea bass genome and its variation provide insights into adaptation to euryhalinity and speciation. Nat Commun 5:5770. https://doi.org/10.1038/ncomms6770
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 209:237–244. https://doi.org/10.1530/JOE-10-0495
Tomy S, Chang YM, Chen YH, Cao JC, Wang TP, Chang CF (2009) Salinity effects on the expression of osmoregulatory genes in the euryhaline black porgy Acanthopagrus schlegelii. Gen Comp Endocrinol 161:123–132. https://doi.org/10.1016/j.ygcen.2008.12.003
Trautner JH, Reiser S, Blancke T, Unger K, Wysujack K (2017) Metamorphosis and transition between developmental stages in European eel (Anguilla anguilla, L.) involve epigenetic changes in DNA methylation patterns. Comp Biochem Physiol Part D Genom Proteom 22:139–145. https://doi.org/10.1016/j.cbd.2017.04.002
Trayer V, Hwang PP, Prunet P, Thermes V (2013) Assessment of the role of cortisol and corticosteroid receptors in epidermal ionocyte development in the medaka (Oryzias latipes) embryos. Gen Comp Endocrinol 194:189–197. https://doi.org/10.1016/j.ygcen.2013.09.011
Tsalafouta A, Papandroulakis N, Gorissen M, Katharios P, Flik G, Pavlidis M (2014) Ontogenesis of the HPI axis and molecular regulation of the cortisol stress response during early development in Dicentrarchus labrax. Sci Rep 4:5525. https://doi.org/10.1038/srep05525
Turner BM (2009) Epigenetic responses to environmental change and their evolutionary implications. Philos Trans R Soc B Biol Sci 364:3403–3418. https://doi.org/10.1098/rstb.2009.0125
Varsamos S, Diaz JP, Charmantier GUY, 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. https://doi.org/10.1002/jez.10099
Vasconcelos RP, Reis-Santos P, Maia A, Fonseca V, França S, Wouters N, Costa MJ, Cabral HN (2010) Nursery use patterns of commercially important marine fish species in estuarine systems along the Portuguese coast. Estuar Coast Shelf Sci 86:613–624. https://doi.org/10.1016/j.ecss.2009.11.029
Venturini G, Cataldi E, Marino G, Pucci P, Garibaldi L, Bronzi P, Cataudella S (1992) Serum ions concentration and atpase activity in gills, kidney and oesophagus of european sea bass (Dicentrarchus labrax, Pisces, Perciformes) during acclimation trials to fresh water. Comp Biochem Physiol Part A Physiol 103:451–454. https://doi.org/10.1016/0300-9629(92)90271-Q
Vijayan MM, Moon TW (1994) The stress response and the plasma disappearance of corticosteroid and glucose in a marine teleost, the sea raven. Can J Zool 72:379–386. https://doi.org/10.1139/z94-054
Waldman J (1995) Sea bass: biology, exploitation, and conservation. Trans Am Fish Soc 124:643–644. https://doi.org/10.1577/1548-8659-124.4.643
Wang X, Kültz D (2017) Osmolality/salinity-responsive enhancers (OSREs) control induction of osmoprotective genes in euryhaline fish. Proc Natl Acad Sci 114:E2729–E2738. https://doi.org/10.1073/pnas.1614712114
Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625. https://doi.org/10.1152/physrev.1997.77.3.591
Williams TD (2008) Individual variation in endocrine systems: moving beyond the “tyranny of the Golden Mean”. Philos Trans R Soc B Biol Sci 363:1687–1698. https://doi.org/10.1098/rstb.2007.0003
Wong APS, Bindoff NL, Church JA (1999) Large-scale freshening of intermediate waters in the Pacific and Indian oceans. Nature 400:440–443. https://doi.org/10.1038/22733
Wood CM, Laurent P (2003) Na+ versus Cl− transport in the intact killifish after rapid salinity transfer. Biochim Biophys Acta Biomembr 1618:106–119. https://doi.org/10.1016/j.bbamem.2003.08.014
Yada T, Hyodo S, Schreck CB (2008) Effects of seawater acclimation on mRNA levels of corticosteroid receptor genes in osmoregulatory and immune systems in trout. Gen Comp Endocrinol 156:622–627. https://doi.org/10.1016/j.ygcen.2008.02.009
Zhao BS, Roundtree IA, He C (2016) Post-transcriptional gene regulation by mRNA modifications. Nat Rev Mol Cell Biol 18:31–42. https://doi.org/10.1038/nrm.2016.132
Acknowledgements
We would like to thank Bruno Guinand, François Bonhomme, David McKenzie and Laurence Besseau for their critical comments on this topic, Stephane Lallement, Marie-Odile Blanc and Alain Vergnet of Ifremer Palavas-les-flots for helping us in the design of the experiment and maintenance of the fish. The project used instruments that were financially supported by the 2015–2020 CPER CELIMER (funded by the French Ministry of Higher Education, Research and Innovation, the Occitanie Region, Montpellier Méditerranée Metropolis, Sète Agglopole Méditerranée, Ifremer, IRD).
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Thibaut, L., Emilie, F., Béatrice, C. et al. Are European sea bass as euryhaline as expected? Intraspecific variation in freshwater tolerance. Mar Biol 166, 102 (2019). https://doi.org/10.1007/s00227-019-3551-z
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DOI: https://doi.org/10.1007/s00227-019-3551-z