Skip to main content
Log in

The effect of starvation and re-feeding on vasotocinergic and isotocinergic pathways in immature gilthead sea bream (Sparus aurata)

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

This study describes the responses of the vasotocinergic and isotocinergic systems to food deprivation and re-feeding processes in immature gilthead sea bream (Sparus aurata). The animals were subjected to the following experimental treatments: (1) normal feeding (control), (2) food deprivation for 21 days; and (3) re-feeding for 7 days, beginning 14 days after starvation. The animals were sampled at 0, 7, 14 and 21 days from the beginning of the trial. The pituitary and plasma arginine vasotocin (AVT) and isotocin (IT) levels and the hypothalamic pro-vasotocin and pro-isotocin mRNA expression levels were measured. In addition, the mRNA levels of three receptors, avtr v1, avtr v2 and itr, were analyzed in target organs associated with (1) the integration and control of different physiological pathways related to stress and food intake (i.e., the hypothalamus), (2) hormonal release into the bloodstream (i.e., the pituitary), and (3) metabolism and its control (i.e., the liver). The metabolic parameters in the liver were also determined. The hepatosomatic index decreased, and hepatic metabolites were mobilized beginning in the early stages of starvation. Moreover, an over-compensation of these parameters occurred when the fish were re-fed after starvation. In terms of the vasotocinergic and isotocinergic systems, feed restriction induced a clear time-dependent regulation among metabolic organization, stress regulation and orexigenic processes in the mature hormone concentration and pro-peptide and receptor mRNA expression. Our results reveal the important role of the AVT/IT endocrine systems in the orchestration of fish physiology during starvation and re-feeding and indicate their involvement in both central and peripheral organs.

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

Access this article

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

  • Ade T, Segner H, Hanke W (1995) Hormonal response of primary hepatocytes of the clawed toad, Xenopus laevis. Exp Clin Endocrinol Diabetes 103:21–27

    Article  CAS  PubMed  Google Scholar 

  • Agirregoitia N, Laiz-Carrion R, Varona A, Martín del Rio MP, Mancera JM, Irazusta J (2005) Distribution of peptidase activity in teleost and rat tissues. J Comp Physiol B Biochem Syst Environ Physiol 175:433–444

    Article  CAS  Google Scholar 

  • Aoyagi T, Kusakawa S, Sanbe A, Hiroyama M, Fujiwara Y, Yamauchi J, Tanoue A (2009) Enhanced effect of neuropeptide Y on food intake caused by blockade of the V(1 A) vasopressin receptor. Eur J Pharmacol 622:32–36

    Article  CAS  PubMed  Google Scholar 

  • Arends RJ, Mancera JM, Muñoz JL, Wendelaar Bonga SE, Flik G (1999) The stress response of the gilthead sea bream (Sparus aurata L.) to air exposure and confinement. J Endocrinol 163:149–157

    Article  CAS  PubMed  Google Scholar 

  • Arletti R, Benelli A, Bertolini A (1990) Oxytocin inhibits food and fluid intake in rats. Physiol Behav 48:825–830

    Article  CAS  PubMed  Google Scholar 

  • Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517–525.

    Article  CAS  PubMed  Google Scholar 

  • Batten TFC, Cambre ML, Moons L, Vandesande F (1990) Comparative distribution of neuropeptide-immunoreactive systems in the brain of the green molly, Poecilia latipinna. J Comp Neurol 302:893–919

    Article  CAS  PubMed  Google Scholar 

  • Bayir A, Sirkecioglu AN, Bayir M, Halilogly I, Kocaman EM, Aras NM (2011) Metabolic responses to prolonged starvation, food restriction, and refeeding in the brown trout, Salmo trutta: oxidative stress and antioxidant defences. Comp Biochem Physiol B Biochem Mol Biol 159:191–196

    Article  PubMed  Google Scholar 

  • Benedito-Palos L, Ballester-Lozano G, Pérez-Sánchez J (2014) Wide-gene expression analysis of lipid-relevant genes in nutritionally challenged gilthead sea bream (Sparus aurata). Gene 547:34–42

    Article  CAS  PubMed  Google Scholar 

  • Bernier NJ, Bedard N, Peter RE (2004) Effects of cortisol on food intake, growth, and forebrain neuropeptide Y and corticotropin-releasing factor gene expression in goldfish. Gen Comp Endocrinol 135:230–240

    Article  CAS  PubMed  Google Scholar 

  • Bernier NJ, Flik G, Klaren PHM (2009) Regulation and contribution of the corticotropic, melanotropic and thyrotropic axes to the stress response in fishes. In: Bernier N, Van der Kraak G, Arel AP, Brauner CJ (eds) Fish neuroendocrinology, vol 28. Academic, New York, pp 235–311

    Chapter  Google Scholar 

  • Black D, Love RM (1986) The sequential mobilisation and restoration of energy reserves in tissues of Atlantic cod during starvation and refeeding. J Comp Physiol B Biochem Syst Environ Physiol 156:469–479

    Article  CAS  Google Scholar 

  • Brett JR (1979) Environmental factors and growth. In: Hoar WS, Randall DJ, Brett JR (eds) Fish physiology, vol 8. Academic, New York, pp 599–675

    Google Scholar 

  • Cádiz L, Román-Padilla J, Gozdowska M, Kulczykowska E, Martínez-Rodríguez G, Mancera JM, Martos-Sitcha JA (2015) Cortisol modulates vasotocinergic and isotocinergic pathways in the gilthead sea bream. J Exp Biol 218:316–325

    Article  PubMed  Google Scholar 

  • Carmean CM, Bobe AM, Yu JC, Volden PA, Brady MJ (2013) Refeeding-induced brown adipose tissue glycogen hyper-accumulation in mice is mediated by insulin and catecholamines. PLoS One 8(7):e67807. doi:10.1371/journal.pone.0067807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang LL, Kau MM, Wun WS, Ho LT, Wang PS (2002) Effects of fasting on cortiscosterone production by zona fasciculata-reticularis cells in ovariectomized rats. J Investig Med 50:86–94

    Article  CAS  PubMed  Google Scholar 

  • Collins AL, Anderson TA (1995) The regulation of endogenous energy stores during starvation and refeeding in the somatic tissues of the golden perch. J Fish Biol 47:1004–1015

    Article  Google Scholar 

  • FAO (2014) The state of world fisheries and aquaculture. http://www.fao.org/3/a-i3720e.pdf.

  • Farbridge KJ, Leatherland JF (1992) Temporal changes in plasma thyroid hormone, growth hormone and free fatty acid concentrations, and hepatic 5 V-monodeiodinase activity, lipid and protein content during chronic fasting and re-feeding in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 10:245–257

    Article  CAS  PubMed  Google Scholar 

  • Flynn FW, Kirchner TR, Clinton ME (2002) Brain vasopressin and sodium appetite. Am J Physiol Regul Integr Comp Physiol 282:R1236–R1244

    Article  CAS  PubMed  Google Scholar 

  • Fryer J, Lederis K, Rivier J (1985) ACTH-releasing activity of urotensin I and ovine CRF: Interaction with arginine vasotocin, isotocin, and arginine vasopressin. Regul Pept 11:11–15

    Article  CAS  PubMed  Google Scholar 

  • Furné M, Morales AE, Trenzado CE, García-Gallego M, Hidalgo MC, Domezain A, Sanz-Rus A (2012) The metabolic effects of prolonged starvation and re-feeding in sturgeon and rainbow trout. J Comp Physiol B Biochem Syst Environ Physiol 182:63–76

    Article  Google Scholar 

  • Gesto M, Soengas JL, Rodríguez-Illamola A, Míguez JM (2014) Arginine vasotocin treatment induces a stress response and exerts a potent anorexigenic effect in rainbow trout, Oncorhynchus mykiss. J Neuroendocrinol 26:89–99

    Article  CAS  PubMed  Google Scholar 

  • Gozdowska M, Kleszczyńska A, Sokołowska E, Kulczykowska E (2006) Arginine vasotocin (AVT) and isotocin (IT) in fish brain: diurnal and seasonal variations. Comp Biochem Physiol B Biochem Mol Biol 143:330–334

    Article  CAS  PubMed  Google Scholar 

  • Guderley H, Lapointe D, Bedard M, Dutil JD (2003) Metabolic priorities during starvation: enzyme sparing in liver and white muscle of Atlantic cod, Gadus morhua L. Comp Biochem Physiol A Mol Integr Physiol 135:347–356

    Article  PubMed  Google Scholar 

  • Guibbolini ME, Pierson PM, Lahlou B (2000) Neurohypophysial hormone receptors and second messengers in trout hepatocytes. J Endocrinol 167:137–144

    Article  CAS  PubMed  Google Scholar 

  • Hausmann H, Meyerhof W, Zwiers, Lederis, K Richter D (1995) Teleost isotocin receptor: structure, functional expression, mRNA distribution and phylogeny. FEBS Lett 370:227–230

    Article  CAS  PubMed  Google Scholar 

  • Janssens PA, Lowrey P (1987) Hormonal regulation of hepatic glycogenolysis in the carp, Cyprinus carpio. Am J Physiol Regul Integr Comp Physiol 252:R653–R660

    CAS  Google Scholar 

  • Janssens PA, Caine AG, Dixon JE (1983) Hormonal control of glycogenolysis and the mechanism of action of adrenaline in amphibian liver in vitro. Gen Comp Endocrinol 49:477–484

    Article  CAS  PubMed  Google Scholar 

  • Jerez-Cepa I, Mancera JM, Flik G, Gorissen M (2016) Vasotinergic and isotonergic co-regulation in stress response of common carp (Cyprinus carpio L.). In: Calduch-Giner JA, Cerdá-Reverter JM, Pérez-Sánchez J. (eds) Advances in comparative endocrinology, vol VIII. Publicacions de la Universitat Jaume I, Castellón de la Plana, pp 185–187

    Google Scholar 

  • Kalamarz-Kubiak H, Meiri-Ashkenazi I, Kleszczyńska A, Rosenfeld H (2014) In vitro effect of cortisol and urotensin I on arginine vasotocin and isotocin secretion from pituitary cells of gilthead sea bream Sparus aurata. J Fish Biol 84:448–458

    Article  CAS  PubMed  Google Scholar 

  • Keppler D, Decker K (1974) Glycogen determination with amyloglucosidase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic, New York, pp 127–131

    Google Scholar 

  • Kleszczyńska A, Vargas-Chacoff L, Gozdowska M, Kalamarz H, Martínez-Rodríguez G, Mancera JM, Kulczykowska E (2006) Arginine vasotocin, isotocin and melatonin responses following acclimation of gilthead sea bream (Sparus aurata) to different environmental salinities. Comp Biochem Physiol A Mol Integr Physiol 145(2):268–273

    Article  PubMed  Google Scholar 

  • Kulczykowska E (2001) Responses of circulating arginine vasotocin, isotocin, and melatonin to osmotic and disturbance stress in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 24:201–206

    Article  CAS  Google Scholar 

  • Kulczykowska E, Sánchez-Vázquez FJ (2010) Neurohormonal regulation of feed intake and response to nutrients in fish: aspects of feeding rhythm and stress. Aquaculture Res 41:654–667

    Article  CAS  Google Scholar 

  • Kulczykowska E, Gozdowska M, Kalamarz H, Kleszczynska A, Nietrzeba M, Martinez-Rodriguez G, Mancera JM (2009) Hypothalamic arginine vasotocin and isotocin are involved in stress response in fish. Comp Biochem Physiol A 154:S26

    Article  Google Scholar 

  • Kulczykowska E, Gozdowska M, Martos-Sitcha JA, Kalamarz-Kubiak H, Nietrzeba M, Mancera JM, Martinez-Rodriguez G (2010) Melatonin, vasotocin and isotocin as biomarkers of the condition of fish. Comp Biochem Physiol A 157:S18

    Article  Google Scholar 

  • Lema SC (2010) Identification of multiple vasotocin receptor cDNAs in teleost fish: sequences, phylogenetic analysis, sites of expression, and regulation in the hypothalamus and gill in response to hyperosmotic challenge. Mol Cell Biochem 321:215–230

    CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lokrantz CM, Uvnäs-Moberg K, Kaplan JM (1997) Effects of central oxytocin administration on intraoral intake of glucose in deprived and nondeprived rats. Physiol Behav 62:347–352

    Article  CAS  PubMed  Google Scholar 

  • Machado CR, Garofalo MAR, Roselino JES, Kettelhut IC, Migliorini RH (1988) Effects of starvation, refeeding and insulin on energy-linked metabolic processes in catfish (Rhamdia hilarii) adapted to a carbohydrate-rich diet. Gen Comp Endocrinol 71:429–437

    Article  CAS  PubMed  Google Scholar 

  • Mancera JM, Vargas-Chacoff L, García-López A, Kleszczynska A, Kalamarz H, Martínez-Rodríguez G, Kulczykowska E (2008) High density and food deprivation affect arginine vasotocin, isotocin and melatonin in gilthead sea bream (Sparus auratus). Comp Biochem Physiol A Mol Integr Physiol 149:92–97

    Article  PubMed  Google Scholar 

  • Mancera JM, Martínez-Rodríguez G, Skrzynska AK, Martos-Sitcha JA (2017) Osmoregulatory role of vasotocinergic and isotocinergic systems in the gilthead sea bream (Sparus aurata L). Gen Comp Endocrinol. doi:10.1016/j.ygcen.2017.01.005 (in press)

    PubMed  Google Scholar 

  • Martins CIM, Galhardo L, Noble C, Damsgard B, Spedicato MT, Zupa W, Beauchaud M, Kulczykowska E, Massabuau J-C, Carter T, Rey Planellas S, Kristiansen T (2012) Behavioural indicators of welfare in farmed fish. Fish Physiol Biochem 38:17–41

    Article  CAS  PubMed  Google Scholar 

  • Martos-Sitcha JA, Gregório SF, Carvalho ESM, Canario AVM, Power DM, Mancera JM, Martínez-Rodríguez G, Fuentes J (2013a) AVT is involved in the regulation of ion transport in the intestine of the sea bream (Sparus aurata). Gen Comp Endocrinol 193:221–228

    Article  CAS  PubMed  Google Scholar 

  • Martos-Sitcha JA, Wunderink YS, Gozdowska M, Kulczykowska E, Mancera JM Martínez-Rodríguez G (2013b) Vasotocinergic and isotocinergic systems in the gilthead sea bream (Sparus aurata): an osmoregulatory story. Comp Biochem Physiol A Mol Integr Physiol 166:571–581

    Article  CAS  PubMed  Google Scholar 

  • Martos-Sitcha JA, Fuentes J, Mancera JM Martínez-Rodríguez G (2014a) Vasotocin and isotocin receptors in gilthead sea bream Sparus aurata: expression variations during different osmotic challenges. Gen Comp Endocrinol 197:5–17

    Article  CAS  PubMed  Google Scholar 

  • Martos-Sitcha JA, Wunderink YS, Straatjes J, Skrzynska AK, Mancera JM, Martínez-Rodríguez G (2014b) Different stressors induce differential responses of the CRH-stress system in the gilthead sea bream (Sparus aurata). Comp Biochem Physiol A Mol Integr Physiol 177:49–61

    Article  CAS  PubMed  Google Scholar 

  • Martos-Sitcha JA, Martínez-Rodríguez G, Mancera JM, Fuentes J (2015a) AVT and IT regulate ion transport across the opercular epithelium of killifish and sea bream. Comp Biochem Physiol A Mol Integr Physiol 182:93–101

    Article  CAS  PubMed  Google Scholar 

  • McCue MD (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol A Mol Integr Physiol 156:1–18

    Article  PubMed  Google Scholar 

  • Mehner T, Wieser W (1994) Energetics and metabolic correlates of starvation in juvenile perch (Perca fluviatilis). J Fish Biol 45:325–333

    Article  Google Scholar 

  • Méndez G, Wieser W (1993) Metabolic responses to food deprivation and refeeding in juveniles of Rutilus rutilus (Teleostei: Cyprinidae). Environ Biol Fish 36(1):73–81

    Article  Google Scholar 

  • Metón I, Fernández F, Baanante V (2003) Short and long-term effects of re-feeding on key enzyme activities in glycolysis-gluconeogenesis in the liver of gilthead sea bream. Aquaculture 225:99–107

    Article  Google Scholar 

  • Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268.

    Article  Google Scholar 

  • Moon TW, Mommsen TP (1990) Vasoactive peptides and phenylephrine actions in isolated teleost hepatocytes. Am J Physiol Endocrinol Metab 259:E644–E649

    CAS  Google Scholar 

  • Morales AE, Pérez-Jiménez A, Hidalgo MC, Abellán E, Cardenete G (2004) Oxidative stress and antioxidant defences alter prolonged starvation in Dentex dentex liver. Comp Biochem Physiol C Toxicol Pharmacol 139:153–161

    Article  PubMed  Google Scholar 

  • Navarro I, Gutiérrez J (1995) Fasting and starvation. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes. Elsevier, New York, pp 393–433

    Google Scholar 

  • Pascual P, Pedrajas JR, Toribio F, López-Barea J, Peinado J (2003) Effect of food deprivation on oxidative stress biomarkers in fish (Sparus aurata). Chem Biol Interact 145:191–199

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Jiménez A, Guedes MJ, Morales AE, Oliva-Teles A (2007) Metabolic responses to short starvation and re-feeding in Dicentrarchus labrax. Effect of dietary composition. Aquaculture 265:325–335

    Article  Google Scholar 

  • Polakof S, Arjona FJ, Sangiao-Alvarellos S, Martín del Rio MP, Mancera JM, Soengas JL (2006) Food deprivation alters osmoregulatory and metabolic responses to salinity acclimation in gilthead sea bream Sparus auratus. J Comp Physiol B Biochem Syst Environ Physiol 176:441–452

    Article  Google Scholar 

  • Pujante I, Martos-Sitcha JA, Moyano FJ, Ruiz-Jarabo I, Martínez-Rodríguez G, Mancera JM (2015) Starving/re-feeding processes induce metabolic modifications in thick-lipped grey mullet (Chelon labrosus, Risso 1827). Comp Biochem Physiol B Biochem Mol Biol 180:57–67

    Article  CAS  PubMed  Google Scholar 

  • Rotllant J, Tort L (1997) Cortisol and glucose responses after acute stress by net handling in the sparid red porgy previously subjected to crowding stress. J Fish Biol 51:21–28

    Article  CAS  PubMed  Google Scholar 

  • Rotllant J, Balm PHM, Ruane NM, Perez-Sanchez J, Wendelaar Bonga S, Tort L (2000) Pituitary proopiomelanocortin-derived peptidesand hypothalamic- pituitary-interrenal axisactivity in gilthead sea bream (Sparus aurata) during prolonged crowding stress: differential regulation of adrenocorticotropin hormone and melanocyte-stimulating hormone release by corticotropinreleasing hormone and thyrotropin-releasing hormone. Gen Comp Endocrinol 119:152–163

    Article  CAS  PubMed  Google Scholar 

  • Rotllant J, Balm PH, Pérez-Sánchez J, Wendelaar Bonga SE, Tort L (2001) Pituitary and interrenal function in gilthead sea bream (Sparus aurata) after handling and confinement stress. Gen Comp Endocrinol 121:333–342

    Article  CAS  PubMed  Google Scholar 

  • Sangiao-Alvarellos S, Guzmán JM, Láiz-Carrión R, Míguez JM, Martín del Río MP, Mancera JM, Soengas JL (2005) Interactive effects of high stocking density and food-deprivation on carbohydrate metabolism in several tissues of gilthead sea bream Sparus auratus. J Exp Zool A Comp Exp Biol 303:761–775

    Article  PubMed  Google Scholar 

  • Sangiao-Alvarellos S, Polakof S, Arjona FJ, Kleszczynska A, Martin del Rio MP, Miguez JM, Soengas JL, Mancera JM (2006) Osmoregulatory and metabolic changes in the gilthead sea bream Sparus auratus after arginine vasotocin AVT treatment. Gen Comp Endocrinol 148(3):348–358

    Article  CAS  PubMed  Google Scholar 

  • Segner H, Braunbeck T (1988) Hepatocellular adaption to extreme nutritional conditions in ide, Leuciscus idus melanotus L (Cyprinidae). A morphofunctional analysis. Fish Physiol Biochem 5:79–97

    Article  CAS  PubMed  Google Scholar 

  • Shimeno S, Kheyyali D, Takeda M (1990) Metabolic adaptation to prolonged starvation in carp. Nippon Suisan Gakkaishi 56:35–41

    Article  CAS  Google Scholar 

  • Smith RF, French NP, Saphier PW, Lowry PJ, Veldhuis JD, Dobson H (2003) Identification of stimulatory and inhibitory inputs to the hypothalamicpituitary-adrenal axis during hypoglycaemia or transport in ewes. J Neuroendocrinol 15:572–585

    Article  CAS  PubMed  Google Scholar 

  • Soengas JL, Strong EF, Fuentes J, Veira JAR, Andrés MD (1996) Food deprivation and refeeding in Atlantic salmon, Salmo salar: effects on brain and liver carbohydrate and ketone bodies metabolism. Fish Physiol Biochem 15:491–511

    Article  CAS  PubMed  Google Scholar 

  • Tachibana T, Saito ES, Saito S, Tomonaga S, Denbow DM, Furuse M (2004) Comparison of brain arginine-vasotocin and corticotrophin-releasing factor for physiological responses in chicks. Neurosci Lett 360:165–169

    Article  CAS  PubMed  Google Scholar 

  • Uchida K, Kajimura S, Riley LG, HiranoT, Aida K, Grau EG (2003) Effects of fasting on growth hormone/insulin-like growth factor I axis in the tilapia, Oreochromis mossambicus. Comp Biochem Physiol A Mol Integr Physiol 134:429–439

    Article  CAS  PubMed  Google Scholar 

  • Vijayan MM, Foster GD, Moon TW (1993) Effects of cortisol on hepatic carbohydrate metabolism and responsiveness to hormones in the sea raven, Hemitripterus americanus. Fish Physiol Biochem 12(4):327–335

    Article  CAS  PubMed  Google Scholar 

  • Volkoff H, Canosa LF, Unniappan S, Cerdá-Reverter JM, Bernier NJ, Kelly SP, Peter RE (2005) Neuropeptides and the control of food intake in fish. Gen Comp Endocrinol 142:3–19

    Article  CAS  PubMed  Google Scholar 

  • Ward PE, Benter IF, Dick L, Wilk S (1990) Metabolism of vasoactive peptides by plasma and purified renal aminopeptidase M. Biochem Pharmacol 40:1725–1732

    Article  CAS  PubMed  Google Scholar 

  • Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625

    CAS  PubMed  Google Scholar 

  • Winberg S, Höglund E, Øverli Ø (2016) Variation in the neuroendocrine stress response. In: Schreck CB, Tort L, Farrell AP, Brauner CJ (eds) Fish Physiology—biology of stress in fish, vol 35. Academic, San Diego, pp 35–74

    Chapter  Google Scholar 

Download references

Acknowledgements

The authors thank the Servicios Centrales de Investigación en Cultivos Marinos (SCI-CM, CASEM, University of Cádiz, Puerto Real, Cádiz, Spain) for providing the experimental fish and Mrs. María Francisca Osta and Mr. Juan José Blanco for their excellent technical assistance. The experiments were conducted at the Campus de Excelencia Internacional del Mar (CEI-MAR) at two separate institutions (University of Cádiz and ICMAN-CSIC). This study was funded by projects AGL2010-14876 (Ministry of Science and Innovation) and AGL2013-48835-C2-1-R (Ministry of Economy and Competitiveness, MINECO) awarded to J. M. M. (Spain) and by Project 498/N-HISZP-JPR/2009/0 (Polish Ministry of Science and Higher Education) to E.K. J.A.M-S is currently funded by a Postdoctoral Research Fellow (Juan de la Cierva-Formación, Reference FJCI-2014-20161) from MINECO.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Juan Antonio Martos-Sitcha.

Additional information

Communicated by G. Heldmaier.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Skrzynska, A.K., Gozdowska, M., Kulczykowska, E. et al. The effect of starvation and re-feeding on vasotocinergic and isotocinergic pathways in immature gilthead sea bream (Sparus aurata). J Comp Physiol B 187, 945–958 (2017). https://doi.org/10.1007/s00360-017-1064-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-017-1064-y

Keywords

Navigation