Abstract
The influence of acclimation of the euryhaline gilthead sea bream (Sparus aurata) larvae/post-larvae to brackish water on growth, energetic contents, and mRNA levels of selected hormones and growth-regulating hypothalamic neurohormones was assessed. Specimens from 49 days post-hatching were acclimated during 28 days to two different environmental salinities: 38 and 20 psu (as brackish water). Both groups were then transferred to 38 psu and acclimated for an additional week. Early juveniles were sampled after 28 days of acclimation to both salinities and one week after transfer to 38 psu. Pituitary adenylate cyclase-activating peptide (adcyap1; pacap), somatostatin-I (sst1), growth hormone (gh1), insulin-like growth factor-I (igf1), and prolactin (prl) mRNA expression were all studied by QPCR. Post-larvae acclimated to 20 psu showed better growth performance and body energetic content than post-larvae maintained at 38 psu. prl, adcyap1, and igf1 mRNA expression levels increased in 20-psu-acclimated post-larvae but decreased upon transfer to 38 psu. GH1 expression did not show significant changes under both experimental conditions. Our results suggested an enhanced general performance for post-larvae in brackish water, supported by the actions of adcyap1, igf1, and prl.
Similar content being viewed by others
References
Arias A (1976) Sobre la biología de la dorada, Sparus aurata L., de los esteros de la provincia de Cádiz. Inv Pesq 40:201–222
Barman UK, Jana SN, Garg SK, Bhatnagar A, Arasu ART (2005) Effect of inland water salinity on growth, feed conversion efficiency and intestinal enzyme activity in growing grey mullet Mugil cephalus 303 (Linn.): field and laboratory studies. Aquac Int 13:241–256
Ben-Tuvia A (1979) Studies of the population and fisheries of Sparus aurata in the Bardawil Lagoon, eastern Mediterranean. Inv Pesq 43(1):43–67
Bodinier C, Sucré E, Lecurieux-Belfond L, Blondeau-Bidet E, Charmantier G (2010) Ontogeny of osmoregulation and salinity tolerance in the gilthead sea bream Sparus aurata. Comp Biochem Physiol 157A:220–228
Boeuf G, Payan P (2001) How should salinity influence fish growth? Comp Biochem Physiol 130C:411–423
Cameron C, Moccia RD, Leatherland JF (2005) Growth hormone secretion from the Atlantic char (Salvelinus alpinus) pituitary gland in vitro: effects of somatostatin-14, insulin-like growth factor-I, and nutritional status. Gen Comp Endocrinol 141(1):93–100
Chervinski J (1984) Salinity tolerance of young gilthead sea bream Sparus aurata. Bamidgeh 36:121–124
Cook AF, Peter RE (1984) The effects of somatostatin on serum growth hormone levels in the goldfish, Carassius auratus. Gen Comp Endocrinol 54(1):109–113
Deane EE, Woo NY (2004) Differential gene expression associated with euryhalinity in sea bream (Sparus sarba). Am J Physiol Regul Integr Comp Physiol 287:R1054–R1063
Deane EE, Woo NY (2005) Upregulation of the somatotropic axis is correlated with increased G6PDH expression in black sea bream adapted to isoosmotic salinity. Ann NY Acad Sci 1040:293–296
Deane EE, Woo NY (2006) Molecular cloning of growth hormone from silver sea bream: effects of abiotic and biotic stress on transcriptional and translational expression. Biochem Biophys Res Commun 342:1077–1082
Deane EE, Woo NY (2009) Modulation of fish growth hormone levels by salinity, temperature, pollutants and aquaculture related stress: a review. Rev Fish Biol Fish 19:97–120
Duan C (1998) Nutritional and developmental regulation of insulin-like growth factors in fish. J Nutr 128:306S–314S
Fielder DS, Bardsley W (1999) A preliminary study on the effects of salinity on growth and survival of mulloway Argyrosomus japonicus larvae and juveniles. J World Aquac Soc 30:380–387
Fridman S, Bron JE, Rana KJ (2012a) Ontogenic changes in the osmoregulatory capacity of the Nile tilapia Oreochromis niloticus and implications for aquaculture. Aquaculture 356–357:243–249
Fridman S, Bron JE, Rana KJ (2012b) Influence of salinity on embryogenesis, survival, growth and oxygen consumption in embryos and yolk-sac larvae of the Nile tilapia. Aquaculture 334:182–190
Johnson DW, Katavic I (1986) Survival and growth of sea bass (Dicentrarchus labrax) larvae as influenced by temperature, salinity, and delayed initial feeding. Aquaculture 52:11–19
Kaneko T, Hiroi J (2008) Osmo- and Ionoregulation. In: Finn RN, Kapoor BG (eds) 338 Fish larval physiology. Science Publishers, Enfield, pp 163–183
Katoh F, Shimizu A, Uchida K, Kaneko T (2000) Shift of chloride cell distribution during early life stages in seawater-adapted killifish (Fundulus heteroclitus). Zool Sci 17:11–18
Laiz-Carrión R, Guerreiro PM, Fuentes J, Canario AV, Martín Del Río MP, Mancera JM (2005a) Branchial osmoregulatory response to salinity in the gilthead sea bream, Sparus auratus. J Exp Zool 303A:563–576
Laiz-Carrión R, Sangiao-Alvarellos S, Guzmán JM, Martín del Río MP, Soengas JL, Mancera JM (2005b) Growth performance of gilthead sea bream Sparus aurata in different osmotic conditions: implications for osmoregulation and energy metabolism. Aquaculture 250:849–861
Laiz-Carrión R, Fuentes J, Redruello B, Guzmán JM, Martín del Río MP, Power D, Mancera JM (2009) Expression of pituitary prolactin, growth hormone and somatolactin is modified in response to different stressors (salinity, crowding and food-deprivation) in gilthead sea bream Sparus auratus. Gen Comp Endocrinol 162:293–300
Link K, Berishvili G, Shved N, D’Cotta H, Baroiller JF, Reinecke M, Eppler E (2010) Seawater and freshwater challenges affect the insulin-like growth factors IGF-I and IGF-II in liver and osmoregulatory organs of the tilapia. Mol Cell Endocrinol 327:40–46
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408
Mancera JM, Fernández-Llebrez P, Grondona JM, Pérez-Fígares JM (1993a) Influence of environmental salinity on prolactin and corticotropic cells in the gilthead sea bream (Sparus aurata L.). Gen Comp Endocrinol 90(220):231
Mancera JM, Fernández-Llebrez P, Pérez-Fígares JM (1993b) Osmoregulatory responses during abrupt salinity changes in the euryhaline gilthead sea bream (Sparus aurata L.). Comp Biochem Physiol 106A:245–250
Mancera JM, Fernández-Llébrez P, Pérez-Fígares JM (1995) Effect of decreased environmental salinity on growth hormone cells in the gilthead sea bream (Sparus aurata). J Fish Biol 46:494–500
Mancera JM, Laiz-Carrión R, Martín del Río MP (2002) Osmoregulatory action of PRL, GH, and cortisol in the gilthead seabream (Sparus aurata L). Gen Comp Endocrinol 129:95–103
Matsuda K, Nagano Y, Uchiyama M, Onoue S, Takahashi A, Kawauchi H, Shioda S (2005) Pituitary adenylate cyclase-activating polypeptide (PACAP)-like immunoreactivity in the brain of a teleost, Uranoscopus japonicus: immunohistochemical relationship between PACAP and adenohypophysial hormones. Regul Pept 126(1–2):129–136
Mohammed-Geba K, Mancera JM, Martínez-Rodríguez G (2015) Acclimation to different environmental salinities induces molecular endocrine changes in the GH/IGF-I axis of juvenile gilthead sea bream (Sparus aurata L.). J Comp Physiol B 185(1):87–101
Moutou KA, Panagiotaki P, Mamuris Z (2004) Effects of salinity on digestive protease activity in the euryhaline sparid Sparus aurata L.: a preliminary study. Aquac Int 35:912–914
Parker DB, Power ME, Swanson P, Rivier J, Sherwood NM (1997) Exon skipping in the gene encoding pituitary adenylate cyclase-activating polypeptide in salmon alters the expression of two hormones that stimulate growth hormone release. Endocrinology 138:414–423
Reinecke M (2010) Influences of the environment on the endocrine and paracrine 380 fish growth hormone insulin-like growth factor-I system. J Fish Biol 76:1233–1254
Rousseau K, Le Belle N, Pichavant K, Marchelidon J, Chow BK, Boeuf G, Dufour S (2001) Pituitary growth hormone secretion in the turbot, a phylogenetically recent teleost, is regulated by a species-specific pattern of neuropeptides. Neuroendocrinology 74:375–385
Saera-Vila A, Calduch-Giner JA, Prunet P, Pérez-Sánchez J (2009) Dynamics of liver GH/IGF axis and selected stress markers in juvenile gilthead sea bream (Sparus aurata) exposed to acute confinement: differential stress response of growth hormone receptors. Comp Biochem Physiol 154A:197–203
Sangiao-Alvarellos S, Arjona FJ, Martín del Río MP, Míguez JM, Mancera JM, Soengas JL (2005) Time course of osmoregulatory and metabolic changes during osmotic acclimation in Sparus auratus. J Exp Biol 208:4291–4304
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 144A:491–500
Shepherd BS, Drennon K, Johnson J, Nichols JW, Playle RC, Singer TD, Vijayan MM (2005) Salinity acclimation affects the somatotropic axis in rainbow trout. Am J Physiol 288:R1385–R1395
Sucré E, Bossus M, Bodinier C, Boulo V, Charmantier G, Charmantier-Daures M, Cucchi P (2013) Osmoregulatory response to low salinities in the European sea bass embryos: a multi-site approach. J Comp Physiol 183B(1):83–97
Tandler A, Anav F, Itzhak C (1995) The effect of salinity on growth rate, survival and swimbladder inflation in gilthead seabream, Sparus aurata, larvae. Aquaculture 135:343–353
Tipsmark CK, Luckenbach JA, Madsen SS, Borski RJ (2007) IGF-I and branchial IGF receptor expression and localization during salinity acclimation in striped bass. Am J Physiol 292:R535–R543
Van der Heijden AJH, van der Meij JCA, Flik G, Bonga SE (1999) Ultrastructure and distribution dynamics of chloride cells in tilapia larvae in freshwater and sea water. Cell Tissue Res 297:119–130
Vargas-Chacoff L, Astola A, Arjona FJ, Martín del Río MP, García-Cózar F, Mancera JM, Martínez-Rodríguez G (2009a) Pituitary gene and protein expression under experimental variation on salinity and temperature in gilthead sea bream Sparus aurata. Comp Biochem Physiol 154B:303–308
Vargas-Chacoff L, Astola A, Arjona FJ, Martín del Río MP, García-Cózar F, Mancera JM, Martínez-Rodríguez G (2009b) Gene and protein expression for prolactin, growth hormone and somatolactin in Sparus aurata: seasonal variations. Comp Biochem Physiol 153B:130–135
Varsamos S, Nebel C, Charmantier G (2005) Ontogeny of osmoregulation in postembryonic fish: a review. Comp Biochem Physiol 141A:401–429
Vaudry D, Gonzalez BJ, Basille M, Yon L, Fournier A, Vaudry H (2000) Pituitary adenylate cyclase-activating polypeptide and its receptors: from structure to functions. Pharmacol Rev 52:269–324
Very NM, Sheridan MA (2002) The role of somatostatins in the regulation of growth in fish. Fish Physiol Biochem 27:217–226
Wada T, Aritaki M, Tanaka M (2004) Effects of low-salinity on the growth and development of spotted halibut Verasper variegatus in the larva-juvenile transformation period with reference to pituitary Prolactin and gill chloride cells responses. J Exp Mar Biol Ecol 308:113–126
Wong AO, Li WS, Lee EK, Leung MY, Tse LY, Chow BK, Lin HR, Chang JP (2000) Pituitary adenylate cyclase activating polypeptide as a novel hypophysiotropic factor in fish. Biochem Cell Biol 78(3):329–343
Xiao D, Wong AO, Lin HR (2002) Lack of growth hormone-releasing peptide-6 action on in vivo and in vitro growth hormone secretion in sexually immature grass carp (Ctenopharyngodon idellus). Fish Physiol Biochem 26(4):315–327
Xu M, Volkoff H (2009) Cloning, tissue distribution and effects of food deprivation 420 on pituitary adenylate cyclase activating polypeptide (PACAP)/PACAP-related peptide (PRP) and preprosomatostatin 1 (PPSS 1) in Atlantic cod (Gadus morhua). Peptides 30:766–776
Yada T, Iguchi K, Yamamoto S, Sakano H, Takasawa T, Katsura K, Abe N, Aawata S, Uchida K (2014) Prolactin and upstream migration of the amphidromous teleost, ayu Plecoglossus altivelis. Zool Sci 31:507–514
Yanagie R, Lee KM, Watanabe S, Kaneko T (2009) Ontogenic change in tissue osmolality and developmental sequence of mitochondria-rich cells in Mozambique tilapia developing in freshwater. Comp Biochem Physiol 154A:263–269
Yúfera M, Polo A, Pascual E (1993) Changes in chemical composition and biomass during the transition from endogenous to exogenous feeding of Sparus aurata L. (Pisces, Sparidae) larvae reared in the laboratory. J Exp Mar Biol Ecol 167:149–161
Very NM, Kittilson JD, Klein SE, Sheridan MA (2008) Somatostatin inhibits basal and growth hormonestimulated hepatic insulin-like growth factor-I production. Mol Cell Endocrinol 281(1–2):19–26
Acknowledgments
This study was partly supported by Grants AGL2007-61211/ACU (Ministerio de Educación y Ciencia and FEDER, Spain), Proyecto de Excelencia PO7-RNM-02843 (Junta de Andalucía) to J.M.M., and AQUAGENOMICS (CDS2007-00002) (Spanish Ministry of Economic Affairs and Competitiveness-MINECO and FEDER/ERDF) to M.Y. Authors would like to thank Dr. Asmaa Galal-Khallaf for the precious help during the conduction of the experiment. Also, authors would like to thank Mr. Manuel Arjonilla and Ms. Esmeralda Ramos-García for conducting the biomass analyses and to CUPIMAR for providing experimental animals. K.M.G. was funded by a full doctorate fellowship from the Egyptian Bureau in Madrid and the Egyptian Government.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mohammed-Geba, K., Yúfera, M., Martínez-Rodríguez, G. et al. Molecular endocrine changes of Gh/Igf1 axis in gilthead sea bream (Sparus aurata L.) exposed to different environmental salinities during larvae to post-larvae stages. Fish Physiol Biochem 42, 1177–1186 (2016). https://doi.org/10.1007/s10695-016-0207-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-016-0207-5