Advertisement

Journal of Applied Phycology

, Volume 28, Issue 3, pp 2061–2071 | Cite as

Diets supplemented with seaweed affect metabolic rate, innate immune, and antioxidant responses, but not individual growth rate in European seabass (Dicentrarchus labrax)

  • Maria J. Peixoto
  • Jon C. Svendsen
  • Hans Malte
  • Luis F. Pereira
  • Pedro Carvalho
  • Rui Pereira
  • José F. M. Gonçalves
  • Rodrigo O. A. Ozório
Article

Abstract

This study investigated the effects of seaweed dietary supplementation on measures of fish performance including aerobic metabolism, digestive enzymes activity, innate immune status, oxidative damage, and growth rate using European seabass (Dicentrarchus labrax). Fish were fed for 49 days with three different diets: a control diet (CTRL), a Gracilaria-supplemented diet (GR7.5), and a mixed diet (Mix) composed of Gracilaria, Fucus, and Ulva genera representatives. All diets were isoenergetic (22 kJ g−1 adjusted for dry matter (DM)), isoproteic (47 %DM), and isolipidic (18 %DM) and tested in triplicate groups of 20 fish (initial body weight 25.5 ± 4.1 g). Final results showed similar growth rates and digestive activities between diets. Maximum and standard metabolic rates and aerobic metabolic scope revealed comparable results for the three diets. In contrast, fish fed with GR7.5 exhibited elevated routine metabolic rate (190.7 mg O2 kg−1 h−1). Fish fed with the GR7.5 and Mix diets had lower alternative complement pathway (ACH50) (62.5 and 63 units mL−1 respectively) than CTRL (84 units mL−1) GR7.5 increased lipid peroxidation and cholinesterase levels, as well as glutathione s-transferase activity. Mix diet increased glutathione reductase activity when compared to CTRL. Collectively, our findings suggest that dietary seaweed supplementation may alter seabass metabolic rate, innate immune, and antioxidant responses without compromising growth parameters.

Keywords

Digestive enzymes Growth rate Innate immune response Metabolic rate Oxidative stress Seaweeds 

Notes

Acknowledgments

This study was carried out under the project SEABIOPLAS (grant agreement n° 606032), funded by the European Union Seventh Framework Programme (FP7/2007-2013), as well as partially supported by the Strategic Funding UID/Multi/04423/2013 through national funds provided by Foundation for Science and Technology (FCT) and European Regional Development Fund (ERDF), in the framework of the program PT2020. The research was also supported by a grant (SFRH/BPD/89473/2012) from the Foundation for Science and Technology (FCT) in Portugal to Jon C. Svendsen. We thank the anonymous reviewers for their constructive and helpful comments on the earlier versions of the manuscript.

References

  1. Abreu MH, Pereira R, Yarish C, Buschmann AH, Sousa-Pinto I (2011) IMTA with Gracilaria vermiculophylla: productivity and nutrient removal performance of the seaweed in a land-based pilot scale system. Aquaculture 312:77–87CrossRefGoogle Scholar
  2. Almeida JR, Gravato C, Guilhermino L (2012) Challenges in assessing the toxic effects of polycyclic aromatic hydrocarbons to marine organisms: a case study on the acute toxicity of pyrene to the European seabass (Dicentrarchus labrax L.). Chemosphere 86:926–937CrossRefPubMedGoogle Scholar
  3. Andrade PB, Barbosa M, Matos RP, Lopes G, Vinholes J, Mouga T, Valentao P (2013) Valuable compounds in macroalgae extracts. Food Chem 138:1819–1828CrossRefPubMedGoogle Scholar
  4. Araújo M, Rema P, Sousa-Pinto I, Cunha L, Peixoto M, Pires M, Seixas F, Brotas V, Beltrán C, Valente LP (2015) Dietary inclusion of IMTA-cultivated Gracilaria vermiculophylla in rainbow trout (Oncorhynchus mykiss) diets: effects on growth, intestinal morphology, tissue pigmentation, and immunological response. J Appl Phycol. doi: 10.1007/s10811-015-0591-8 Google Scholar
  5. Atherton PJ, Smith K (2012) Muscle protein synthesis in response to nutrition and exercise. J Physiol 590:1049–1057CrossRefPubMedPubMedCentralGoogle Scholar
  6. Axelsson M (2002) Post-prandial blood flow to the gastrointestinal tract is not compromised during hypoxia in the seabass Dicentrarchus labrax. J Exp Biol 205:2891–2896PubMedGoogle Scholar
  7. Baker MA, Cerniglia GJ, Zaman A (1990) Microtiter plate assay for the measurement of glutathione and glutathione disulfide in large numbers of biological samples. Anal Biochem 190:360–365CrossRefPubMedGoogle Scholar
  8. Bashir-Tanoli S, Tinsley MC (2014) Immune response costs are associated with changes in resource acquisition and not resource reallocation. Funct Ecol 28:1011–1019CrossRefGoogle Scholar
  9. Bele SD, Patil SS, Sharmila S, Rebecca LJ (2014) Isolation and partial purification of lipase and protease from marine algae. J Chem Pharm Res 6:1153–1156Google Scholar
  10. Bernfeld P (1951) Enzymes of starch degradation and synthesis. Adv Enzymol Relat Subj Biochem 12:379–428PubMedGoogle Scholar
  11. Blier P (2014) Fish health: an oxidative stress perspective. Fish Aquac J 5, e105CrossRefGoogle Scholar
  12. Boel M, Aarestrup K, Baktoft H, Larsen T, Sondergaard Madsen S, Malte H, Skov C, Svendsen JC, Koed A (2014) The physiological basis of the migration continuum in brown trout (Salmo trutta). Physiol Biochem Zool 87:334–345CrossRefPubMedGoogle 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 72:248–254CrossRefPubMedGoogle Scholar
  14. Burton T, Killen SS, Armstrong JD, Metcalfe NB (2011) What causes intraspecific variation in resting metabolic rate and what are its ecological consequences? Proc R Soc B 278:3465–3473CrossRefPubMedPubMedCentralGoogle Scholar
  15. Chandini SK, Ganesan P, Suresh P, Bhaskar N (2008) Seaweeds as a source of nutritionally beneficial compounds—a review. J Food Sci Technol 45:1–13Google Scholar
  16. Clairborne A (1985) Catalase activity. In: CRC handbook of methods in oxygen radical research. CRC Press, Boca Raton, pp 283–284Google Scholar
  17. Claireaux G, Couturier C, Groison AL (2006) Effect of temperature on maximum swimming speed and cost of transport in juvenile European seabass (Dicentrarchus labrax). J Exp Biol 209:3420–3428CrossRefPubMedGoogle Scholar
  18. Clark TD, Sandblom E, Jutfelt F (2013) Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations. J Exp Biol 216:2771–2782CrossRefPubMedGoogle Scholar
  19. Cribb AE, Leeder JS, Spielberg SP (1989) Use of a microplate reader in an assay of glutathione reductase using 5,5'-dithiobis(2-nitrobenzoic acid). Anal Biochem 183:195–196CrossRefPubMedGoogle Scholar
  20. Cuesta A, Angeles Esteban M, Meseguer J (2006) Cloning, distribution and up-regulation of the teleost fish MHC class II alpha suggests a role for granulocytes as antigen-presenting cells. Mol Immunol 43:1275–1285CrossRefPubMedGoogle Scholar
  21. Cutts CJ, Metcalfe NB, Taylor AC (2002) Juvenile Atlantic salmon (Salmo salar) with relatively high standard metabolic rates have small metabolic scopes. Funct Ecol 16:73–78CrossRefGoogle Scholar
  22. de Almeida CLF, Falcão HS, Lima GRM, Montenegro CA, Lira NS, de Athayde-Filho PF, Rodrigues LC, de Souza MFV, Barbosa-Filho JM, Batista LM (2011) Bioactivities from marine algae of the genus Gracilaria. Int J Mol Sci 12:4550–4573CrossRefPubMedPubMedCentralGoogle Scholar
  23. Dias J, Alvarez MJ, Arzel J, Corraze G, Diez A, Bautista JM, Kaushik SJ (2005) Dietary protein source affects lipid metabolism in the European seabass (Dicentrarchus labrax). Comp Biochem Physiol A 142:19–31CrossRefGoogle Scholar
  24. Downs CJ, Brown JL, Wone B, Donovan ER, Hunter K, Hayes JP (2013) Selection for increased mass-independent maximal metabolic rate suppresses innate but not adaptive immune function. Proc R Soc B 280:20122636CrossRefPubMedPubMedCentralGoogle Scholar
  25. Dupont-Prinet A, Chatain B, Grima L, Vandeputte M, Claireaux G, McKenzie DJ (2010) Physiological mechanisms underlying a trade-off between growth rate and tolerance of feed deprivation in the European seabass (Dicentrarchus labrax). J Exp Biol 213:1143–1152CrossRefPubMedGoogle Scholar
  26. Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95CrossRefPubMedGoogle Scholar
  27. El-Said G, El-Sikaily A (2013) Chemical composition of some seaweed from Mediterranean sea coast, Egypt. Environ Monit Assess 185:6089–6099CrossRefPubMedPubMedCentralGoogle Scholar
  28. Eroglu A, Dogan Z, Kanak E, Atli G, Canli M (2014) Effects of heavy metals (Cd, Cu, Cr, Pb, Zn) on fish glutathione metabolism. Environ Sci Pollut Res 22:3229–3237CrossRefGoogle Scholar
  29. Eroldoğan OT, Suzer C, Taşbozan O, Tabakoğlu S (2008) The Effects of rate-restricted feeding regimes in cycles on digestive enzymes of gilthead sea-bream, Sparus aurata. Turk J Fish Aquat Sci 8:49–54Google Scholar
  30. Faten M, Elalla A, Elalla E, Shalaby A (2009) Antioxidant activity of extract and semi- purified fractions of marine red macroalga, Gracilaria verrucosa. Aust J Basic Appl Sci 3:3179–3185Google Scholar
  31. Forstner H (1983) An automated multiple-chamber intermittent-flow respirometer. In: Gnaiger E, Forstner H (eds) Polarographic oxygen sensors. Springer, Berlin, pp 111–126CrossRefGoogle Scholar
  32. Gravato C, Teles M, Oliveira M, Santos MA (2006) Oxidative stress, liver biotransformation and genotoxic effects induced by copper in Anguilla anguilla L.—the influence of pre-exposure to β-naphthoflavone. Chemosphere 65:1821–1830CrossRefPubMedGoogle Scholar
  33. Guardiola FA, Cuesta A, Abellán E, Meseguer J, Esteban MA (2014) Comparative analysis of the humoral immunity of skin mucus from several marine teleost fish. Fish Shellfish Immunol 40:24–31CrossRefPubMedGoogle Scholar
  34. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139PubMedGoogle Scholar
  35. Hamauzu K, Yamanaka M (1997) Usefulness of the meal of a sterile mutant of Ulva pertusa as a feed supplement for cultured yellowtail. Aquaculture Sci 45:357–363Google Scholar
  36. Hartviksen M, Bakke A, Vecino J, Ringø E, Krogdahl Å (2014) Evaluation of the effect of commercially available plant and animal protein sources in diets for Atlantic salmon (Salmo salar L.): digestive and metabolic investigations. Fish Physiol Biochem 40:1621–1637CrossRefPubMedGoogle Scholar
  37. Herskin J, Steffensen JF (1998) Energy savings in seabass swimming in a school: measurements of tail beat frequency and oxygen consumption at different swimming speeds. J Fish Biol 53:366–376CrossRefGoogle Scholar
  38. Hidalgo MC, Urea E, Sanz A (1999) Comparative study of digestive enzymes in fish with different nutritional habits. Proteolytic and amylase activities. Aquaculture 170:267–283CrossRefGoogle Scholar
  39. Kadam SU, Prabhasankar P (2010) Marine foods as functional ingredients in bakery and pasta products. Food Res Int 43:1975–1980CrossRefGoogle Scholar
  40. Killen SS, Marras S, McKenzie DJ (2011) Fuel, fasting, fear: routine metabolic rate and food deprivation exert synergistic effects on risk-taking in individual juvenile European seabass. J Anim Ecol 80:1024–1033CrossRefPubMedGoogle Scholar
  41. Killen SS, Marras S, Ryan MR, Domenici P, McKenzie DJ (2012a) A relationship between metabolic rate and risk-taking behaviour is revealed during hypoxia in juvenile European seabass. Funct Ecol 26:134–143CrossRefGoogle Scholar
  42. Killen SS, Marras S, Steffensen JF, McKenzie DJ (2012b) Aerobic capacity influences the spatial position of individuals within fish schools. Proc R Soc B 279:357–364CrossRefPubMedPubMedCentralGoogle Scholar
  43. Krogdahl Å, Penn M, Thorsen J, Refstie S, Bakke AM (2010) Important antinutrients in plant feedstuffs for aquaculture: an update on recent findings regarding responses in salmonids. Aquac Res 41:333–344CrossRefGoogle Scholar
  44. Lailvaux SP, Husak JF (2014) The life history of whole-organism performance. Q Rev Biol 89:285–318CrossRefPubMedGoogle Scholar
  45. Le Boucher R, Vandeputte M, Dupont-Nivet M, Quillet E, Ruelle F, Vergnet A, Kaushik S, Allamellou JM, Médale F, Chatain B (2013) Genotype by diet interactions in European sea bass (Dicentrarchus labrax L.): nutritional challenge with totally plant-based diets. J Anim Sci 91:44–56CrossRefPubMedGoogle Scholar
  46. Leal E, Fernández-Durán B, Guillot R, Ríos D, Cerdá-Reverter J (2011) Stress-induced effects on feeding behavior and growth performance of the seabass (Dicentrarchus labrax): a self-feeding approach. J Comp Physiol B 181:1035–1044CrossRefPubMedGoogle Scholar
  47. Leaver MJ, Scott K, George SG (1993) Cloning and characterization of the major hepatic glutathione S-transferase from a marine teleost flatfish, the plaice (Pleuronectes platessa), with structural similarities to plant, insect and mammalian Theta class isoenzymes. Biochem J 292:189–195CrossRefPubMedPubMedCentralGoogle Scholar
  48. Liu J, Yeo HC, Övervik-Douki E, Hagen T, Doniger SJ, Chu DW, Brooks GA, Ames BN (2000) Chronically and acutely exercised rats: biomarkers of oxidative stress and endogenous antioxidants. J Appl Physiol 89:21–28PubMedGoogle Scholar
  49. Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98CrossRefGoogle Scholar
  50. Lordan S, Ross RP, Stanton C (2011) Marine bioactives as functional food ingredients: potential to reduce the incidence of chronic diseases. Mar Drugs 9:1056–1100CrossRefPubMedPubMedCentralGoogle Scholar
  51. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275PubMedGoogle Scholar
  52. Luna-Acosta A, Lefrançois C, Millot S, Chatain B, Bégout ML (2011) Physiological response in different strains of seabass (Dicentrarchus labrax): swimming and aerobic metabolic capacities. Aquaculture 317:162–167CrossRefGoogle Scholar
  53. McClelland GB (2004) Fat to the fire: the regulation of lipid oxidation with exercise and environmental stress. Comp Biochem Physiol B 139:443–460CrossRefPubMedGoogle Scholar
  54. Mohamed S, Hashim SN, Rahman HA (2012) Seaweeds: a sustainable functional food for complementary and alternative therapy. Trends Food Sci Tech 23:83–96CrossRefGoogle Scholar
  55. Mohandas J, Marshall JJ, Duggin GG, Horvath JS, Tiller DJ (1984) Differential distribution of glutathione and glutathione-related enzymes in rabbit kidney. Possible implications in analgesic nephropathy. Biochem Pharmacol 33:1801–1807CrossRefPubMedGoogle Scholar
  56. Newsholme P, Newsholme EA (1989) Rates of utilization of glucose, glutamine and oleate and formation of end-products by mouse peritoneal macrophages in culture. Biochem J 261:211–218CrossRefPubMedPubMedCentralGoogle Scholar
  57. Norin T, Malte H (2011) Repeatability of standard metabolic rate, active metabolic rate and aerobic scope in young brown trout during a period of moderate food availability. J Exp Biol 214:1668–1675CrossRefPubMedGoogle Scholar
  58. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358CrossRefPubMedGoogle Scholar
  59. Okuzumi J, Takahashi T, Yamane T, Kitao Y, Inagake M, Ohya K, Nishino H, Tanaka Y (1993) Inhibitory effects of fucoxanthin, a natural carotenoid, on N-ethyl-N′-nitro-N-nitrosoguanidine-induced mouse duodenal carcinogenesis. Cancer Lett 68:159–168CrossRefPubMedGoogle Scholar
  60. Ots I, Kerimov AB, Ivankina EV, Ilyina TA, Hõrak P (2001) Immune challenge affects basal metabolic activity in wintering great tits. Proc R Soc B 268:1175–1181CrossRefPubMedPubMedCentralGoogle Scholar
  61. Owen JB, Butterfield DA (2010) Measurement of oxidized/reduced glutathione ratio. Methods Mol Biol 648:269–277CrossRefPubMedGoogle Scholar
  62. Plaza M, Cifuentes A, Ibáñez E (2008) In the search of new functional food ingredients from algae. Trends Food Sci Tech 19:31–39CrossRefGoogle Scholar
  63. Quade MJ, Roth JA (1997) A rapid, direct assay to measure degranulation of bovine neutrophil primary granules. Vet Immunol Immunopathol 58:239–248CrossRefPubMedGoogle Scholar
  64. Råberg L, Vestberg M, Hasselquist D, Holmdahl R, Svensson E, Nilsson JÅ (2002) Basal metabolic rate and the evolution of the adaptive immune system. Proc R Soc Lond B 269:817–821CrossRefGoogle Scholar
  65. Roche DG, Binning SA, Bosiger Y, Johansen JL, Rummer JL (2013) Finding the best estimates of metabolic rates in a coral reef fish. J Exp Biol 216:2103–2110CrossRefPubMedGoogle Scholar
  66. Rodrigues AP, Gravato C, Guimaraes L (2013) Involvement of the antioxidant system in differential sensitivity of Carcinus maenas to fenitrothion exposure. Environ Sci: Processes Impacts 15:1938–1948Google Scholar
  67. Rosewarne PJ, Wilson JM, Svendsen JC (2015) Measuring maximum and standard metabolic rates using intermittent flow respirometry: a student laboratory investigation of aerobic metabolic scope and environmental hypoxia in aquatic breathers. J Fish BiolGoogle Scholar
  68. Rungruangsak-Torrissen K (2007) Digestive efficiency, growth and qualities of muscle and oocyte in Atlantic salmon (Salmo salar L.) fed on diets with krill meal as an alternative protein source. J Food Biochem 31:509–540CrossRefGoogle Scholar
  69. Rungruangsak-Torrissen K, Sundby A (2000) Protease activities, plasma free amino acids and insulin at different ages of Atlantic salmon (Salmo salar L.) with genetically different trypsin isozymes. Fish Physiol Biochem 22:337–347CrossRefGoogle Scholar
  70. Samad R (2013) Effects of dietary supplementation of Spirulina and Quercetin on growth, innate immune responses, disease resistance against Edwardsiella tarda, and dietary antioxidant capacity in the juvenile olive flounder Paralichthys olivaceus. J Fish Aquat Sci 16:7–14Google Scholar
  71. Scapigliati G, Romano N, Buonocore F, Picchietti S, Baldassini MR, Prugnoli D, Galice A, Meloni S, Secombes CJ, Mazzini M, Abelli L (2002) The immune system of sea bass, Dicentrarchus labrax, reared in aquaculture. Dev Comp Immunol 26:151–160CrossRefPubMedGoogle Scholar
  72. Schurmann H, Steffensen JF (1997) Effects of temperature, hypoxia and activity on the metabolism of juvenile Atlantic cod. J Fish Biol 50:1166–1180Google Scholar
  73. Shao JT, Wang MY, Zheng LB (2013) Antifatigue effect of Gracilaria eucheumoides in mice. Exp Ther Med 6:1512–1516PubMedPubMedCentralGoogle Scholar
  74. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321CrossRefPubMedGoogle Scholar
  75. Skinner LA, Schulte PM, Balfry SK, McKinley RS, LaPatra SE (2010) The association between metabolic rate, immune parameters, and growth performance of rainbow trout, Oncorhynchus mykiss (Walbaum), following the injection of a DNA vaccine alone and concurrently with a polyvalent, oil-adjuvanted vaccine. Fish Shellfish Immunol 28:387–393CrossRefPubMedGoogle Scholar
  76. Souza BWS, Cerqueira MA, Bourbon AI, Pinheiro AC, Martins JT, Teixeira JA, Coimbra MA, Vicente AA (2012) Chemical characterization and antioxidant activity of sulfated polysaccharide from the red seaweed Gracilaria birdiae. Food Hydrocoll 27:287–292CrossRefGoogle Scholar
  77. Srikanth K, Pereira E, Duarte AC, Ahmad I (2013) Glutathione and its dependent enzymes’ modulatory responses to toxic metals and metalloids in fish—a review. Environ Sci Pollut Res Int 20:2133–2149CrossRefPubMedGoogle Scholar
  78. Steffensen J (1989) Some errors in respirometry of aquatic breathers: how to avoid and correct for them. Fish Physiol Biochem 6:49–59CrossRefPubMedGoogle Scholar
  79. Sunyer JO, Tort L (1995) Natural hemolytic and bactericidal activities of sea bream Sparus aurata serum are effected by the alternative complement pathway. Vet Immunol Immunopathol 45:333–345CrossRefPubMedGoogle Scholar
  80. Svendsen JC, Steffensen JF, Aarestrup K, Frisk M, Etzerodt A, Jyde M (2012) Excess posthypoxic oxygen consumption in rainbow trout (Oncorhynchus mykiss): recovery in normoxia and hypoxia. Can J Zool 90:1–11CrossRefGoogle Scholar
  81. Svendsen JC, Banet AI, Christensen RHB, Steffensen JF, Aarestrup K (2013) Effects of intraspecific variation in reproductive traits, pectoral fin use and burst swimming on metabolic rates and swimming performance in the Trinidadian guppy (Poecilia reticulata). J Exp Biol 216:3564–3574CrossRefPubMedGoogle Scholar
  82. Svendsen JC, Genz J, Anderson WG, Stol JA, Watkinson DA, Enders EC (2014) Evidence of circadian rhythm, oxygen regulation capacity, metabolic repeatability and positive correlations between forced and spontaneous maximal metabolic rates in lake sturgeon Acipenser fulvescens. PLoS One 9(4), e94693CrossRefPubMedPubMedCentralGoogle Scholar
  83. Svendsen JC, Tirsgaard B, Cordero GA, Steffensen JF (2015) Intraspecific variation in aerobic and anaerobic locomotion: gilthead sea bream (Sparus aurata) and Trinidadian guppy (Poecilia reticulata) do not exhibit a trade-off between maximum sustained swimming speed and minimum cost of transport. Front Physiol 6:1–12CrossRefGoogle Scholar
  84. Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184CrossRefGoogle Scholar
  85. Tort L, Gómez E, Montero D, Sunyer JO (1996) Serum haemolytic and agglutinating activity as indicators of fish immunocompetence: their suitability in stress and dietary studies. Aquac Int 4:31–41CrossRefGoogle Scholar
  86. Valente LP, Araújo M, Batista S, Peixoto M, Sousa-Pinto I, Brotas V, Cunha L, Rema P (2015) Carotenoid deposition, flesh quality and immunological response of Nile tilapia fed increasing levels of IMTA-cultivated Ulva spp. J Appl Phycol. doi: 10.1007/s10811-015-0590-9 Google Scholar
  87. Valero Y, Garcia-Alcazar A, Esteban MA, Cuesta A, Chaves-Pozo E (2014) Seasonal variations of the humoral immune parameters of European seabass (Dicentrarchus labrax L.). Fish Shellfish Immunol 39:185–187CrossRefPubMedGoogle Scholar
  88. Webster CD, Lim C (2002) Nutrient requirements and feeding of finfish for Aquaculture. CABIGoogle Scholar
  89. Wieser W (1985) Developmental and metabolic constraints of the scope for activity in young rainbow trout (Salmo gairdneri). J Exp Biol 118:133–142Google Scholar
  90. Winkler UK, Stuckmann M (1979) Glycogen, hyaluronate, and some other polysaccharides greatly enhance the formation of exolipase by Serratia marcescens. J Bacteriol 138:663–670PubMedPubMedCentralGoogle Scholar
  91. Woo MS, Choi HS, Lee OH, Lee BY (2013) The edible red alga, Gracilaria verrucosa, inhibits lipid accumulation and ROS production, but improves glucose uptake in 3T3-L1 cells. Phytother Res 27:1102–1105CrossRefPubMedGoogle Scholar
  92. Yan X, Chuda Y, Suzuki M, Nagata T (1999) Fucoxanthin as the major antioxidant in Hijikia fusiformis, a common edible seaweed. Biosci Biotechnol Biochem 63:605–607CrossRefPubMedGoogle Scholar
  93. Zar JH (1999) Biostatistical analysis. Prentice Hall, New YorkGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Maria J. Peixoto
    • 1
    • 2
  • Jon C. Svendsen
    • 1
    • 3
    • 4
  • Hans Malte
    • 5
  • Luis F. Pereira
    • 1
  • Pedro Carvalho
    • 2
  • Rui Pereira
    • 6
  • José F. M. Gonçalves
    • 1
    • 2
  • Rodrigo O. A. Ozório
    • 1
    • 2
  1. 1.CIIMAR – Centro Interdisciplinar de Investigação Marinha e AmbientalUniversidade do PortoPortoPortugal
  2. 2.ICBAS – Instituto de Ciências Biomédicas de Abel SalazarUniversidade do PortoPortoPortugal
  3. 3.National Institute of Aquatic Resources, Section for Freshwater Fisheries and EcologyTechnical University of DenmarkSilkeborgDenmark
  4. 4.National Institute of Aquatic Resources, Section for Ecosystem Based Marine ManagementTechnical University of DenmarkCharlottenlundDenmark
  5. 5.Department of Bioscience, ZoophysiologyAarhus UniversityAarhus CDenmark
  6. 6.ALGAPlus, LdaÍlhavoPortugal

Personalised recommendations