Fish Physiology and Biochemistry

, Volume 36, Issue 4, pp 1113–1124 | Cite as

Growth and nutrient utilisation of blackspot seabream (Pagellus bogaraveo) under different feeding regimes

  • A. Cláudia Figueiredo-Silva
  • Geneviève Corraze
  • Joan Sanchez-Gurmaches
  • Joaquim Gutiérrez
  • Luísa M. P. Valente


The growth and nutrient utilization of blackspot seabream was studied under self-feeding or hand feeding for 90 days. Groups of 31 fish with an initial body weight of 24 g were fed either by hand two times a day (09:00, and 18:00 h) to apparent satiety or by self-feeders. The 90 days of the feeding trial included two periods: an adaptation period (30 days) required to achieve a constant number of feed demands per day and a subsequent experimental period (60 days). Final body weight and daily growth index were unaffected by the feeding regimes. However, the marked reduction in voluntary feed intake associated with similar nutrient gain on the self-fed group resulted in improved nutrient efficiency and in subsequent increased protein, lipid and energy retentions compared to fish hand-fed at set hours. The self-fed group displayed depressed malic (<62%) and fatty acid synthetase (<35%) activities as well as reduced triacylglycerol plasma levels, which correlated positively with feed intake and, at some extent, with fish lipid content. These results indicate the ability of blackspot seabream to adjust their lipid metabolism according to fish feeding rhythm. No effect of feeding method was however observed on glycolytic hepatic activities or on glucose, cholesterol and insulin plasma levels. Self-feeders led to similar growth (DGI, 1.4–1.5) but better efficiency (FCR, 1.0 vs. 1.5), and hence, can be regarded as a helpful tool to optimize feed distribution according to this species natural rhythm. The maximal number of demands occurring between 20:00 and 21:00 h (dusk/sunset), together with the fact that 61% of the feed demands took place during the night, reveals a preferential crepuscular/nocturnal feeding pattern of this species.


Diel feeding rhythm Feeding method Glycolytic enzymes Lipogenic enzymes Nutrient utilization Pagellus bogaraveo Self-feeding 



This work was supported by “Optidietas project” (Agência de Inovação, Portugal, with the support of the European fund FEDER). A. Cláudia Figueiredo-Silva was supported by FCT, Fundação para a Ciência e Tecnologia of Portugal (PhD Grant SFRH/BD/22401/2005) and by COST Action 925 (STSM). Special thanks to L. Larroquet, C. Vachot, M.J. Borthaire and António Júlio Pinto for technical assistance.


  1. Alanärä A (1992) Demand feeding as a self-regulating feeding system for rainbow trout (Oncorhynchus mykiss) in net-pens. Aquaculture 108:347–356. doi: 10.1016/0044-8486(92)90118-5 CrossRefGoogle Scholar
  2. Alanärä A (1996) The use of self-feeders in rainbow trout (Oncorhynchus mykiss) production. Aquaculture 145:1–20. doi: 10.1016/S0044-8486(96)01346-4 CrossRefGoogle Scholar
  3. Azzaydi M, Madrid JA, Zamora S, Sánchez-Vázquez FJ, Martínez FJ (1998) Effect of three feeding strategies (automatic, ad libitum demand-feeding and time-restricted demand-feeding) on feeding rhythms and growth in European sea bass (Dicentrarchus labrax L.). Aquaculture 163:285–296. doi: 10.1016/S0044-8486(98)00238-5 CrossRefGoogle Scholar
  4. Azzaydi M, Martínez FJ, Zamora S, Sánchez-Vázquez FJ, Madrid JA (2000) The influence of nocturnal vs. diurnal feeding under winter conditions on growth and feed conversion of European sea bass (Dicentrarchus labrax, L.). Aquaculture 182:329–338. doi: 10.1016/S0044-8486(99)00276-8 CrossRefGoogle Scholar
  5. Bautista J, Garrido-Pertierra A, Soler G (1988) Glucose-6-phosphate dehydrogenase from Dicentrarchus labrax liver: kinetic mechanism and kinetics of NADPH inhibition. Biochim Biophys Acta 967:354–363. doi: 10.1016/0304-4165(88)90098-0 PubMedGoogle Scholar
  6. Bolliet V, Azzaydi M, Boujard T (2001a) Effects of feeding time on feed intake and growth. In: Houlihan D, Boujard T, Jobling M (eds) Food intake in fish. Blackwell Science, Oxford, pp 233–249. doi: 10.1002/9780470999516.ch10
  7. Bolliet V, Aranda A, Boujard T (2001b) Demand-feeding rhythm in rainbow trout and European catfish—synchronisation by photoperiod and food availability. Physiol Behav 73:625–633. doi: 10.1016/S0031-9384(01)00505-4 CrossRefPubMedGoogle Scholar
  8. Bolliet V, Jarry M, Boujard T (2004) Rhythmic pattern of growth and nutrient retention in response to feeding time in the rainbow trout. J Fish Biol 64:1616–1624. doi: 10.1111/j.1095-8649.2004.00418.x CrossRefGoogle Scholar
  9. Boujard T (2001) Feeding behaviour and regulation of food intake. In: Guillaume J, Métailler R (eds) Nutrition and feeding of fish and crustaceans. Springer, London, pp 19–25Google Scholar
  10. Boujard T, Leatherland JF (1992a) Circadian rhythms and feeding time in fish. Env Biol Fish 35:109–131. doi: 10.1007/BF00002186 CrossRefGoogle Scholar
  11. Boujard T, Leatherland JF (1992b) Demand-feeding behaviour and diel pattern activity in Oncorhynchus mykiss held under different photoperiod regimes. J Fish Biol 40:535–544. doi: 10.1111/j.1095-8649.1992.tb02603.x CrossRefGoogle Scholar
  12. 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. doi: 10.1016/0044-8486(95)01148-X CrossRefGoogle Scholar
  13. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi: 10.1016/0003-2697(76)90527-3 CrossRefPubMedGoogle Scholar
  14. Burel C, Robin J, Boujard T (1997) Can turbot, Psetta maxima, be fed with self-feeders? Aquat Living Resour 10:381–384. doi: 10.1051/alr:1997042 CrossRefGoogle Scholar
  15. Carter C, Houlihan D, Kiessling A, Médale F, Jobling M (2001) Physiological effects of feeding. In: Houlihan D, Boujard T, Jobling M (eds) Food intake in fish. Blackwell Science, Oxford, pp 297–331. doi: 10.1002/9780470999516.ch13
  16. Chakrabarty K, Leveille GA (1969) Acetyl-Coa carboxylase and fatty acid synthetase activities in liver and adipose tissue of meal-fed rats. Proc Soc Exp Biol Med 131:1051–1054PubMedGoogle Scholar
  17. Chang H-C, Seidman I, Teebor G, Lane MD (1967) Liver acetyl CoA carboxylase and fatty acid synthetase: relative activities in the normal state and in hereditary obesity. Biochem Biophys Res Commun 28:682–686. doi: 10.1016/0006-291X(67)90369-5 CrossRefPubMedGoogle Scholar
  18. FAO (2007) The state of world fisheries and aquaculture 2006. FAO Fisheries and Aquaculture Department, Rome 162 ppGoogle Scholar
  19. Figueiredo-Silva AC, Corraze G, Borges P, Valente LMP (2009) Dietary protein/lipid level and protein source effects on growth, tissue composition and lipid metabolism of blackspot seabream (Pagellus bogaraveo). Aquacult Nutr doi: 10.1111/j.1365-2095.2009.00649.x
  20. Figueiredo-Silva AC, Corraze G, Rema P, Sanchez-Gurmaches J, Gutiérrez J, Valente LMP (2009b) Blackspot seabream (Pagellus bogaraveo) lipogenic and glycolytic pathways appear to be more related to dietary protein level than dietary starch type. Aquaculture 291:101–110. doi: 10.1016/j.aquaculture.2009.03.003 CrossRefGoogle Scholar
  21. Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509PubMedGoogle Scholar
  22. Foster G, Moon TW (1986) Enzyme activities in the Atlantic hagfish, Myxine glutinosa: changes with captivity and food deprivation. Can J Zool 64:1080–1085. doi: 10.1139/z86-162 CrossRefGoogle Scholar
  23. Froy O (2007) The relationship between nutrition and circadian rhythms in mammals. Front Neuroendocrinol 28:61–71. doi: 10.1016/j.yfrne.2007.03.001 CrossRefPubMedGoogle Scholar
  24. Fukuda H, Iritani N (1991) Diurnal variations of lipogenic enzyme mRNA quantities in rat liver. Biochim Biophys Acta 1086:261–264. doi: 10.1016/0005-2760(91)90168-H PubMedGoogle Scholar
  25. Gélineau A, Mambrini M, Leatherland JF, Boujard T (1996) Effect of feeding time on hepatic nucleic acid, plasma T3, T4, and GH concentrations in rainbow trout. Physiol Behav 59:1061–1067. doi: 10.1016/0031-9384(95)02249-X CrossRefPubMedGoogle Scholar
  26. Gélineau A, Corraze G, Boujard T (1998) Effects of restricted ration, time-restricted access and reward level on voluntary food intake, growth and growth heterogeneity of rainbow trout (Oncorhynchus mykiss) fed on demand with self-feeders. Aquaculture 167:247–258. doi: 10.1016/S0044-8486(98)00320-2 CrossRefGoogle Scholar
  27. Gutiérrez J, Carrillo M, Zanuy S, Planas J (1984) Daily rhythms of insulin and glucose levels in the plasma of sea bass Dicentrarchus labrax after experimental feeding. Gen Comp Endocrinol 55:393–397. doi: 10.1016/0016-6480(84)90009-1 CrossRefPubMedGoogle Scholar
  28. Hirota T, Fukada Y (2004) Resetting mechanism of central and peripheral circadian clocks in mammals. Zoolog Sci 21:359–368. doi: 10.2108/zsj.21.359 CrossRefPubMedGoogle Scholar
  29. Hossain MAR, Haylor GS, Beveridge MCM (2001) Effect of feeding time and frequency on the growth and feed utilization of African catfish Clarias gariepinus (Burchell 1822) fingerlings. Aquacult Res 32:999–1004. doi: 10.1046/j.1365-2109.2001.00635.x CrossRefGoogle Scholar
  30. Kaushik SJ, Médale F (1994) Energy requirements, utilization and dietary supply to salmonids. Aquaculture 124:81–97. doi: 10.1016/0044-8486(94)90364-6 CrossRefGoogle Scholar
  31. Kentouri M, Divanach P, Maignot E (1993) Comparaison de l’ efficacité-coût de trois techniques de rationnement de la daurade Sparus aurata, en élevage intensif en bassins. In: Barnabé G, Kestemont P (eds) Production, environment and quality, vol 18. EAS Spec. Publ, Bordeux Aquaculture’92, Ghent, pp 273–283Google Scholar
  32. Kohbara J, Hidaka I, Matsuoka F, Osada T, Furukawa K, Yamashita M, Tabata M (2003) Self-feeding behavior of yellowtail, Seriola quinqueradiata, in net cages: diel and seasonal patterns and influences of environmental factors. Aquaculture 220:581–594. doi: 10.1016/S0044-8486(02)00642-7 CrossRefGoogle Scholar
  33. Kohsaka A, Bass J (2007) A sense of time: how molecular clocks organize metabolism. Trends Endocrinol Metab 18:4–11. doi: 10.1016/j.tem.2006.11.005 CrossRefPubMedGoogle Scholar
  34. Madrid JA (1994) L′alimentation à la demande et les rythmes endogènes. Aqua-revue 52:33Google Scholar
  35. Madrid JA, Azzaydi M, Zamora S, Sánchez-Vázquez FJ (1997) Continuous recording of uneaten food pellets and demand-feeding activity: a new approach to studying feeding rhythms in fish. Physiol Behav 62:689–695. doi: 10.1016/S0031-9384(97)00155-8 CrossRefPubMedGoogle Scholar
  36. Madrid JA, Boujard T, Sánchez-Vázquez FJ (2001) Feeding rhythms. In: Houlihan D, Boujard T, Jobling MS (eds) Food intake in fish. Blackwell Science, Oxford, pp 189–215. doi: 10.1002/9780470999516.ch8
  37. Ochoa S (1955) Malic enzyme. In: Colowick SP, Kaplan NO (eds) Methods in enzymology. Academic Press, New York, pp 739–753CrossRefGoogle Scholar
  38. Panserat S, Médale F, Blin C, Breque J, Vachot C, Plagnes-Juan E, Gomes E, Krishnamoorthy R, Kaushik S (2000) Hepatic glucokinase is induced by dietary carbohydrates in rainbow trout, gilthead seabream, and common carp. Am J Physiol Regul Integr Comp Physiol 278:R1164–R1170PubMedGoogle Scholar
  39. Paspatis M, Maragoudaki D, Kentouri M (2000) Self-feeding activity patterns in gilthead sea bream (Sparus aurata), red porgy (Pagrus pagrus) and their reciprocal hybrids. Aquaculture 190:389–401. doi: 10.1016/S0044-8486(00)00409-9 CrossRefGoogle Scholar
  40. Plisetskaya EM, Buchelli-Narvaez LI, Hardy RW, Dickhoff WW (1991) Effects of injected and dietary arginine on plasma insulin levels and growth of pacific salmon and rainbow trout. Comp Biochem Physio 98A:165–170. doi: 10.1016/0300-9629(91)90595-4 CrossRefGoogle Scholar
  41. Reebs SG (2002) Plasticity of diel and circadian activity rhythms in fishes. Rev Fish Biol Fish 12:349–371. doi: 10.1023/A:1025371804611 CrossRefGoogle Scholar
  42. Rungruangsak-Torrissen K, Carter CG, Sundby A, Berg A, Houlihan DF (1999) Maintenance ration, protein synthesis capacity, plasma insulin and growth of Atlantic salmon (Salmo salar L.) with genetically different trypsin isozymes. Fish Physiol Biochem 21:223–233. doi: 10.1023/A:1007804823932 CrossRefGoogle Scholar
  43. Sánchez-Muros MJ, Corchete V, Suárez MD, Cardenete G, Gómez-Milán E, de la Higuera M (2003) Effect of feeding method and protein source on Sparus aurata feeding patterns. Aquaculture 224:89–103. doi: 10.1016/S0044-8486(03)00211-4 CrossRefGoogle Scholar
  44. Sánchez-Vázquez FJ, Tabata M (1998) Circadian rhythms of demand-feeding and locomotor activity in rainbow trout. J Fish Biol 52:255–267. doi: 10.1111/j.1095-8649.1998.tb00797.x CrossRefGoogle Scholar
  45. Sánchez-Vázquez FJ, Madrid JA, Zamora S (1995) Circadian rhythms of feeding activity in sea bass, Dicentrarchus labrax L.: dual phasing capacity of diel demand-feeding pattern. J Biol Rhyth 10:256–266. doi: 10.1177/074873049501000308 CrossRefGoogle Scholar
  46. Sánchez-Vázquez FJ, Azzaydi M, Martinez 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. Chron Int 15:607–622. doi: 10.3109/07420529808993197 CrossRefGoogle Scholar
  47. Smith IP, Metcalfe NB, Huntingford FA, Kadri S (1993) Daily and seasonal patterns in the feeding behaviour of Atlantic salmon (Salmo salar L.) in a sea cage. Aquaculture 117:165–178. doi: 10.1016/0044-8486(93)90133-J CrossRefGoogle Scholar
  48. Spieler RE (1992) Feeding-entrained circadian rhythms in fishes. In: Ali MA (ed) Rhythms in fishes. Plenum Press, New York, pp 137–148Google Scholar
  49. Thivend P, Mercier C, Guilbot A (1972) Determination of starch with glucoamylase. In: Whistler RL, Bemiller JN (eds) Methods in carbohydrate chemistry. Academic Press, New York, pp 100–105Google Scholar
  50. Tranulis MA, Dregni O, Christophersen B, Krogdahl Å, Borrebaek B (1996) A glucokinase-like enzyme in the liver of Atlantic salmon (Salmo salar). Comp Biochem Physiol 114B:35–39. doi: 10.1016/0305-0491(95)02119-1 Google Scholar
  51. Valente LMP, Fauconneau B, Gomes EFS, Boujard T (2001) Feed intake and growth of fast and slow growing strains of rainbow trout (Oncorhynchus mykiss) fed by automatic feeders or by self-feeders. Aquaculture 195:121–131. doi: 10.1016/S0044-8486(00)00536-6 CrossRefGoogle Scholar
  52. Velázquez M, Zamora S, Martínez FJ (2004) Influence of environmental conditions on demand-feeding behaviour of gilthead seabream (Sparus aurata). J Appl Ichthyol 20:536–541. doi: 10.1111/j.1439-0426.2004.00613.x CrossRefGoogle Scholar
  53. Velázquez M, Zamora S, Martinez FJ (2006) Effect of different feeding strategies on gilthead sea bream (Sparus aurata) demand-feeding behaviour and nutritional utilization of the diet. Aquacult Nutr 12:403–409. doi: 10.1111/j.1365-2095.2006.00441.x CrossRefGoogle Scholar
  54. Zar JH (1996) Biostatistical analysis. Prentice-Hall, LondonGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • A. Cláudia Figueiredo-Silva
    • 1
    • 2
  • Geneviève Corraze
    • 2
  • Joan Sanchez-Gurmaches
    • 3
  • Joaquim Gutiérrez
    • 3
  • Luísa M. P. Valente
    • 1
  1. 1.CIMAR/CIIMAR, Centro Interdisciplinar de Investigação Marinha e Ambiental and ICBAS, Instituto de Ciências Biomédicas de Abel SalazarUniversidade do PortoPortoPortugal
  2. 2.INRA-UMR Nutrition Aquaculture Génomique, Pôle HydrobiologieSaint Pée-sur-NivelleFrance
  3. 3.Departament de Fisiologia, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain

Personalised recommendations