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Stress-induced effects on feeding behavior and growth performance of the sea bass (Dicentrarchus labrax): a self-feeding approach

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Abstract

Repetitive aquaculture-related protocols may act as cyclic stressors that induce chronic stress in cultured fish. The sea bass is particularly sensitive to stressful conditions and the mere presence of humans will disturb feeding behavior. In this paper, we study whether chronic stress induced by repetition of acute stress protocols affects long-term feeding behavior and growth performance in sea bass and whether exogenous cortisol may induce stress-like changes in these parameters. We demonstrate that both chronic stress and dietary cortisol decrease food intake and have a negative effect on feed conversion efficiency, severely impairing sea bass performance. Both experimental approaches induced changes in the daily feeding activity by lengthening the active feeding periods. Fish subjected to a cyclic stressor modify their daily feeding pattern in an attempt to avoid interference with the time of the stressor. The delay in feeding when fish are acutely and repeatedly stressed could be of substantial adaptive importance.

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References

  • Aluru N, Vijayan MM (2009) Stress transcriptomics in fish: a role for genomic cortisol signaling. Gen Comp Endocrinol 164:142–150

    Article  PubMed  CAS  Google Scholar 

  • Ashley PJ (2007) Fish welfare: current issues in aquaculture. Appl Anim Behav Sci 104:199–235

    Article  Google Scholar 

  • Azzaydi M, Rubio VC, Martínez López FJ, Sánchez-Vázquez FJ, Zamora S, Madrid JA (2007) Effect of time-restricted feeding on annual rhythms of demand-feeding and food anticipatory activity in European sea bass. Chronobiol Internat 24:859–874

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Barton BA, Schreck CB, Barton LD (1987) Effects of chronic cortisol administration and daily acute stress on growth, physiological conditions, and stress responses in juvenile rainbow-trout. Dis Aquat Org 2:173–185

    Article  CAS  Google Scholar 

  • Bernier NJ (2006) The corticotrophin-releasing factor system as mediator of the appetite-suppressing effects of stress in fish. Gen Comp Endocrinol 146:45–55

    Article  PubMed  CAS  Google Scholar 

  • Bernier NJ, Peter RE (2001) The hypothalamic-pituitary-interrenal axis and the control of food intake in teleost fish. Comp Biochem Physiol 129:639–644

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Boujard T, Jourdan M, Kentouri M, Divanach P (1996) Diel feeding activity and the effect of time-restricted self-feeding on growth and feed conversion in European sea bass. Aquaculture 139:117–127

    Article  Google Scholar 

  • Cavagnini F, Croci M, Putignano P, Petroni ML, Invitti C (2000) Glucocorticoids and neuroendocrine function. Int J Obes Relat Metab Disord 2:S77–S79

    Google Scholar 

  • De Boeck G, Alsop D, Wood C (2001) Cortisol effects on aerobic and anaerobic metabolism, nitrogen excretion, and whole-body composition in juvenile rainbow trout. Physiol Biochem Zool 74:858–868

    Article  PubMed  Google Scholar 

  • Dean EE, Woo NYS (2009) Modulation of fish growth hormone levels by salinity temperature, pollutants and aquaculture related stress: a review. Rev Fish Biol Fisheries 19:97–120

    Article  Google Scholar 

  • Di Marco P, Priori A, Finoia MG, Massari A, Mandich A, Marino G (2008) Physiological responses of European sea bass Dicentrarchus labrax to different stocking densities and acute stress challenge. Aquaculture 275:319–328

    Article  Google Scholar 

  • d’Orbcastel ER, Lemarie G, Breuil G, Petochi T, Marino G, Triplet S, Dutto G, Fivelstad S, Coeurdacier JL (2010) Effects of rearing density on sea bass (Dicentrarchus labrax) biological performance blood parameters and disease resistance in a flow through system. Aquat Liv Res 23:109–117

    Article  Google Scholar 

  • Doyon C, Leclair J, Trudeau VL, Moon TW (2006) Corticotropin-releasing factor and neuropeptide Y mRNA levels are modified by glucocorticoids in rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 146:126–135

    Article  PubMed  CAS  Google Scholar 

  • Gregory TR, Wood CM (1999) The effects of chronic plasma cortisol elevation on the feeding behaviour, growth, competitive ability, and swimming performance of juvenile rainbow trout. Physiol Biochem Zool 72:286–295

    Article  PubMed  CAS  Google Scholar 

  • Kajimura S, Hirano T, Visitacion N, Moriyama S, Aida K, Grau EG (2003) Dual mode of cortisol action on GH/IGF-I/IGF binding proteins in the tilapia, Oreochromis mossambicus. J Endocrinol 178:91–99

    Article  PubMed  CAS  Google Scholar 

  • Kasumyan AO, Doving KB (2003) Taste preferences in fishes. Fish and Fishseries 4:289–347

    Article  Google Scholar 

  • Leal E, Sánchez E, Muriach B, Cerdá-Reverter JM (2009) Sex steroid-induced inhibition of food intake in sea bass (Dicentrarchus labrax). J Comp Physiol B 179:77–86

    Article  PubMed  CAS  Google Scholar 

  • Lupatsch I, Santos GA, Schrama JW, Verreth JAJ (2010) Effect of stocking density and feeding level on energy expenditure and stress responsiveness in European sea bass Dicentrarchus labrax. Aquaculture 298:245–250

    Article  Google Scholar 

  • Millot S, Pean S, Leguay D, Vergnet A, Chatain B, Begout ML (2010) Evaluation of behavioral changes induced by a first step of domestication or selection for growth in the European sea bass (Dicentrarchus labrax): a self-feeding approach under repeated acute stress. Aquaculture 306:211–217

    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 

  • Paspatis M, Boujard T, Maragoudaki D, Blanchard G, Kentouri M (2003) Do stocking density and feed reward level affect growth and feeding of self-fed juvenile European sea bass? Aquaculture 216:103–113

    Article  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 L., Teleostei) after handling and confinement stress. Gen Comp Endocrinol 121:333–342

    Article  PubMed  CAS  Google Scholar 

  • Rotllant J, Ruane NM, Caballero MJ, Montero D, Tort L (2003) Response to confinement in sea bass (Dicentrarchus labrax) is characterised by an increased biosynthetic capacity of interrenal tissue with no effect on ACTH sensitivity. Comp Biochem Physiol A 136:613–620

    Article  CAS  Google Scholar 

  • Rubio VC, Sánchez E, Cerdá-Reverter JM (2010) Compensatory feeding in the sea bass after fasting and physical stress. Aquaculture 298:332–337

    Article  Google Scholar 

  • 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 A 154:197–203

    Article  Google Scholar 

  • Sammouth S, d’Orbcastel ER, Gasset E, Lemarie G, Breuil G, Marino G, Coeurdacier JL, Fivelstad S, Blancheton JP (2009) The effect of density on sea bass (Dicentrarchus labrax) performance in a tank-based recirculating system. Aquac Eng 40:72–78

    Article  Google Scholar 

  • Sánchez-Vázquez FJ, Zamora S, Madrid JA (1995a) Light-dark and food restriction cycles in sea bass––effect of conflicting zeitgebers on demand-feeding rhythms. Physiol Behav 58:705–714

    Article  PubMed  Google Scholar 

  • Sánchez-Vázquez FJ, Madrid JA, Zamora S (1995b) Circadian rhythms of feeding activity in sea bass, Dicentrarchus labrax L: dual phasing capacity of diel demand-feeding pattern. J Biol Rhythm 10:256–266

    Article  Google Scholar 

  • Sánchez-Vázquez FJ, Azzaydi M, Martínez FJ, Zamora S, Madrid JA (1998) Annual rhythms of demand-feeding activity in sea bass: evidence of a seasonal phase inversion of the diel feeding pattern. Chronobiol Internat 15:607–622

    Article  Google Scholar 

  • Santos GA, Schrama JW, Mamauag REP, Rombout JHW M, Verreth JAJ (2010) Chronic stress impairs performance, energy metabolism and welfare indicators in European sea bass (Dicentrarchus labrax): the combined effects of fish crowding and water quality deterioration. Aquaculture 299:73–80

    Article  Google Scholar 

  • Simontacchi C, Poltronieri C, Carraro C, Bertotto D, Xiccato G, Trocino A, Radaelli G (2008) Alternative stress indicators in sea bass Dicentrarchus labrax, L. J Fish Biol 72:747–752

    Article  Google Scholar 

  • Teitsma CA, Anglade I, Toutirais G, Muñoz-Cueto JA, Saligaut D, Ducouret B, Kah O (1998) Immunohistochemical localization of glucocorticoid receptors in the forebrain of the rainbow trout (Oncorhynchus mykiss). J Comp Neurol 401:395–410

    Article  PubMed  CAS  Google Scholar 

  • Terova G, Gornati R, Rimoldi S, Bernardini G, Saroglia M (2005) Quantification of a glucocorticoid receptor in sea bass (Dicentrarchus labrax L.) reared at high stocking density. Gene 357:144–151

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

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

    Google Scholar 

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Acknowledgments

This work was supported by grants AGL2007-65744-C03-02, AGL2010-22247-C03-01 and CSD 2007-00002 from Spanish Science and Education Ministry (MEC) to JMC-R. Additional funding was obtained from the “Generalitat Valenciana” (research grant PROMETEO 2010/006). EL was recipient of a Geronimo Forteza fellowship from the Generalitat Valenciana (GV). The authors wish to acknowledge TINAMENOR for supplying the experimental animals. We also thank Matias Sánchez for his technical assistance in fish maintenance and cleaning protocols.

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Authors and Affiliations

  1. Department of Fish Physiology and Biotechnology, Instituto de Acuicultura de Torre de la Sal (IATS), Consejo Superior de Investigaciones Científicas (CSIC), Castellón, Spain

    Esther Leal, Begoña Fernández-Durán, Raul Guillot, Diana Ríos & José Miguel Cerdá-Reverter

  2. Department of Fish Physiology and Biotechnology, Instituto de Acuicultura de Torre de la Sal, 12595 Torre de la Sal, Ribera de Cabanes, Castellón, Spain

    José Miguel Cerdá-Reverter

Authors
  1. Esther Leal
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  2. Begoña Fernández-Durán
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  3. Raul Guillot
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  4. Diana Ríos
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  5. José Miguel Cerdá-Reverter
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Corresponding author

Correspondence to José Miguel Cerdá-Reverter.

Additional information

Communicated by G. Heldmaier.

E. Leal and B. Fernández-Durán contributed equally to this work.

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Leal, E., Fernández-Durán, B., Guillot, R. et al. Stress-induced effects on feeding behavior and growth performance of the sea bass (Dicentrarchus labrax): a self-feeding approach. J Comp Physiol B 181, 1035–1044 (2011). https://doi.org/10.1007/s00360-011-0585-z

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  • DOI: https://doi.org/10.1007/s00360-011-0585-z

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