Journal of Applied Phycology

, Volume 28, Issue 5, pp 3091–3100 | Cite as

The inclusion of Palmaria palmata macroalgae in Atlantic salmon (Salmo salar) diets: effects on growth, haematology, immunity and liver function

  • Alex H. L. Wan
  • Anna Soler-Vila
  • Damien O’Keeffe
  • Paul Casburn
  • Richard Fitzgerald
  • Mark P. Johnson


A feeding study was carried out for fourteen weeks to evaluate the effects of partial inclusion of 5, 10 and 15 % of dillisk, Palmaria palmata, into formulated Atlantic salmon (Salmo salar) diets. A further fourth diet was produced without the presence of algae and was used as a basal reference diet. All the four diets were formulated to be iso-nitrogenous (40 %), iso-lipidic (25 %) and iso-energetic (26 MJ kg−1). Salmon growth (final body weight, weight gain, feed conversion ratio (FCR), specific growth rate (SGR)) were comparable across algal and control diets, with no significant differences amongst the treatments (P > 0.05). Comparisons of liver weight, viscera weight and viscerosomatic index (VSI) also suggested that the macroalgal inclusion did not affect fish growth (P > 0.05). Fish health indicators across haematological, immunological and hepatic function were generally similar between the experimental diets. The exceptions to this pattern included a significant decrease in alanine transaminase activity (P < 0.05) in the diet with 5 and 15 % P. palmata inclusion compared to other experimental diets. This may indicate that higher P. palmata inclusion improved hepatic function. Seaweed inclusion at 5 % also had positive effects on body lipid content when compared to the control diets. In conclusion, the findings demonstrated that P. palmata can be a suitable feed supplement in Atlantic salmon (S. salar) diets.


Atlantic salmon Seaweed Macroalgae Dillisk Palmaria palmata Blood parameters 



This project (Grant-Aid Agreement No. MFFRI/07/01) is carried out under the Sea Change Strategy with the support of the Marine Institute and the Department of Agriculture, Food and the Marine, funded under the National Development Plan 2007–2013. We would like to express our thanks to Dr Majbritt Bolton-Warberg for her editorial assistance. The authors would like to thank the members of the Irish Seaweed Research Group, in particular Dr Monica Moniz, Dr Jazmin Hernández-Kantún, Celine Raud and Jeremy Bidault for their assistance in seaweed collection, sample collection and proximate analysis. In addition, special thanks are also given to the Steve Amey, Ken Maher and Kieran O’ Halloran at Carna research station for their assistance during the feeding trial.


  1. AOAC (1995) Official methods of analysis of the Association of Official Analytical Chemists, 5th edn. Association of Official Analytical Chemists, Inc., USAGoogle Scholar
  2. Araújo M, Rema P, Sousa-Pinto I, Cubha LM, Peixoto MJ, Pires MA, Seixas F, Brotas V, Beltran C, Valente LMP (2016) 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 28:679–689CrossRefGoogle Scholar
  3. Asino H, Ai Q, Mai K (2011) Evaluation of Enteromorpha prolifera as a feed component in large yellow croaker (Pseudosciaena crocea, Richardson, 1846) diets. Aquacult Res 42:525–533CrossRefGoogle Scholar
  4. Bain BJ, Lewis SM, Bates I (2006) Basic haematological techniques. In: Dacie and Lewis practical haematology, 10th edn. Churchill Livingstone, New York, pp 26–59Google Scholar
  5. Bakke-McKellep AM, Press C, Baeverfjord G, Krogdahl A, Landsverk T (2000) Changes in immune and enzyme histochemical phenotypes of cells in the intestinal mucosa of Atlantic salmon, Salmo salar L., with soybean meal induced enteritis. J Fish Dis 23:115–127CrossRefGoogle Scholar
  6. Bansemir A, Blume M, Schröder S, Lindequist U (2006) Screening of cultivated seaweeds for antibacterial activity against fish pathogenic bacteria. Aquaculture 252:79–84CrossRefGoogle Scholar
  7. Boettcher AA, Target NM (1993) Role of polyphenolic molecular size in reduction of assimilation efficiency in Xiphister mucosus. Ecology 74:891–903CrossRefGoogle Scholar
  8. Bradford M (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
  9. Costas B, Conceição LEC, Aragão C, Martos JA, Ruiz-Jarabo I, Mancera JM, Afonso A (2011) Physiological responses of Senegalese sole (Solea senegalensis Kaup, 1858) after stress challenge: effects on non-specific immune parameters, plasma free amino acids and energy metabolism. Aquaculture 316:68–76CrossRefGoogle Scholar
  10. Davies SJ, Brown MT, Camilleri M (1997) Preliminary assessment of the seaweed Porphyra purpurea in artificial diets for thick-lipped grey mullet (Chelon labrosus). Aquaculture 152:249–258CrossRefGoogle Scholar
  11. Diler I, Tekinay AA, Gliroy D, Gliroy BK, Soyutllrk M (2007) Effects of Ulva rigida on the growth, feed intake and body composition of common carp, Cyprinus carpio L. J Biol Sci 7:305–308CrossRefGoogle Scholar
  12. Ergün S, Soyutürk M, Güroy B, Güroy D, Merrifield D (2008) Influence of Ulva meal on growth, feed utilization, and body composition of juvenile Nile tilapia (Oreochromis niloticus) at two levels of dietary lipid. Aquacult Int 17:355–361CrossRefGoogle Scholar
  13. FAO (2009) How to feed the world by 2050. URL: Accessed 23 June 2013
  14. FAO (2014) The State of World Fisheries and Aquaculture 2014. Accessed 23 Dec 2015
  15. Fleurence J (1999) Seaweed proteins: biochemical, nutritional aspects and potential uses. Trends Food Sci Tech 10:25–28CrossRefGoogle Scholar
  16. Francis G, Makkar HP, Becker K (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199:197–227CrossRefGoogle Scholar
  17. Galland-Irmouli AV, Fleurence J, Lamghari R, Luçon M, Rouxel C, Barbaroux O, Bronowicki JP, Villaume C, Guéant JL (1999) Nutritional value of proteins from edible seaweed Palmaria palmata (dulse). J Nutr Biochem 10:353–9CrossRefPubMedGoogle Scholar
  18. Gao J, Koshio S, Ishikawa M, Yokoyama S, Mamauag REP, Han Y (2012) Effects of dietary oxidized fish oil with vitamin E supplementation on growth performance and reduction of lipid peroxidation in tissues and blood of red sea bream Pagrus major. Aquaculture 356–357:73–79CrossRefGoogle Scholar
  19. Gatlin DM III, Barrows FT, Brown P, Dabrowski K, Gaylord TG, Hardy RW, Herman E, Hu G, Krogdahl A, Nelson R, Overturf K, Rust M, Sealey W, Skonberg D, Souza EJ, Stone D, Wilson R, Wurtele E (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquac Res 38:551–579CrossRefGoogle Scholar
  20. Gérard-Monnier D, Erdelmeier I, Régnard K, Moze-Henry N, Yadan J-C, Chaudiére J (1998) Reactions of 1-methyl-2-phenylindole with malondialdehyde and 4-hydroxyalkenals. Analytical applications to a colorimetric assay of lipid peroxidation. Chem Res Toxcol 11:1176–1183CrossRefGoogle Scholar
  21. Guedes EAC, Araújo MA, Souza AK, de Souza LI, de Barros LD, Maranhão FC, Sant'Ana AE (2012) Antifungal activities of different extracts of marine macroalgae against dermatophytes and Candida species. Mycopathologia 174:223–232CrossRefPubMedGoogle Scholar
  22. Güroy B, Ergün S, Merrifield DL, Güroy D (2012) Effect of autoclaved Ulva meal on growth performance, nutrient utilization and fatty acid profile of rainbow trout, Oncorhynchus mykiss. Aquac Int 21:605–615CrossRefGoogle Scholar
  23. Halver JE, Hardy RW (2002) Fish nutrition. Academic Press, Elsevier Science, USAGoogle Scholar
  24. Hardy R (2010) Utilization of plant proteins in fish diets: effects of global demand and supplies of fishmeal. Aquacult Res 41:770–776CrossRefGoogle Scholar
  25. Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597CrossRefGoogle Scholar
  26. Hutson KS, Mata L, Paul NA, De Nys R (2012) Seaweed extracts as a natural control against the monogenean ectoparasite, Neobenedenia sp., infecting farmed barramundi (Lates calcarifer). Int J Parasitol 42:1135–1141CrossRefPubMedGoogle Scholar
  27. Jahanbin K, Hedayati A, Moini S, Gohari AR, Emam-Djomeh Z, Esposito A, Bagheri T (2012) The first application of a new polysaccharide from Acanthophyllum bracteatum for the health improvement of Atlantic salmon exposed to mercury chloride. Toxicol Ind Health 28:377–84CrossRefPubMedGoogle Scholar
  28. Kader MA, Koshio S, Ishikawa M, Yokoyama S, Bulbul M (2010) Supplemental effects of some crude ingredients in improving nutritive values of low fishmeal diets for red sea bream, Pagrus major. Aquaculture 308:136–144CrossRefGoogle Scholar
  29. Krogdahl A, Bakke-McKellep AM, Baeverfjord G (2003) Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.). Aquacult Nutr 9:361–371CrossRefGoogle Scholar
  30. Li Z-H, Velisek J, Zlabek V, Grabic R, Machova J, Kolarova J, Li P, Randak T (2011) Chronic toxicity of verapamil on juvenile rainbow trout (Oncorhynchus mykiss): effects on morphological indices, hematological parameters and antioxidant responses. J Hazard Mater 185:870–880CrossRefPubMedGoogle Scholar
  31. Macartain P, Gill CIR, Brooks M, Campbell R, Rowland IR (2007) Nutritional value of edible seaweeds. Nutr Rev 65:535–543CrossRefPubMedGoogle Scholar
  32. Marrion O, Schwertz A, Fleurence J, Guéant JL, Villaume G (2003) Improvement of the digestibility of the proteins of the red alga Palmaria palmata by physical processes and fermentation. Food Nahrung 47:339–344CrossRefPubMedGoogle Scholar
  33. Marrion O, Fleurence J, Schwertz A, Guéant J-L, Mamelouk L, Ksouri J, Villaume C (2005) Evaluation of protein in vitro digestibility of Palmaria palmata and Gracilaria verrucosa. J Appl Phycol 17:99–102CrossRefGoogle Scholar
  34. Mehrabi Z, Firouzbakhsh F, Jafarpour A (2012) Effects of dietary supplementation of synbiotic on growth performance, serum biochemical parameters and carcass composition in rainbow trout (Oncorhynchus mykiss) fingerlings. J Anim Physiol Anim Nutr (Berl) 96:474–481CrossRefGoogle Scholar
  35. Morgan K, Wright J, Simpson F (1980) Review of chemical constituents of the red alga Palmaria palmata (dulse). Econ Bot 34:27–50CrossRefGoogle Scholar
  36. Mouritsen OG, Dawczynski C, Duelund L, Jahreis G, Vetter W, Schröder M (2013) On the human consumption of the red seaweed dulse (Palmaria palmata (L.) Weber & Mohr). J Appl Phycol 25:1777–1791CrossRefGoogle Scholar
  37. Mustafa MG, Wakamatsu S, Takeda T et al (1995) Effect of algae as a feed additive on growth performance in red sea bream, Pagrus major. Proc 12th Symp Trace Nutr Res 12:67–72Google Scholar
  38. Nakagawa S (2004) A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15:1044–1045CrossRefGoogle Scholar
  39. Nakano T, Tosa M, Takeuchi M (1995) Improvement of biochemical features in fish health by red yeast and synthetic astaxanthin. J Agr Food Chem 43:1570–1573CrossRefGoogle Scholar
  40. Naylor RL, Hardy RW, Bureau DP et al (2009) Feeding aquaculture in an era of finite resources. Proc Natl Acad Sci U S A 106:15103–10CrossRefPubMedPubMedCentralGoogle Scholar
  41. Olsvik PA, Torstensen BE, Hemre G-I, Sanden M, Waagbø R (2011) Hepatic oxidative stress in Atlantic salmon (Salmo salar L.) transferred from a diet based on marine feed ingredients to a diet based on plant ingredients. Aquacult Nutr 17:e424–e436CrossRefGoogle Scholar
  42. Ortiz-Ordoñez E, Uría-Galicia E, Ruiz-Picos RA, Duran AGS, Trejo YH, Sedeño-Díaz JE, López-López E (2011) Effect of Yerbimat herbicide on lipid peroxidation, catalase activity, and histological damage in gills and liver of the freshwater fish Goodea atripinnis. Arch Environ Contam Toxicol 61:443–52CrossRefPubMedGoogle Scholar
  43. Pereira H, Barreira L, Figueiredo F, Custódio L, Vizetto-Duarte C, Polo C, Rešek E, Engelen A, Varela J (2012) Polyunsaturated fatty acids of marine macroalgae: potential for nutritional and pharmaceutical applications. Mar Drugs 10:1920–1935CrossRefPubMedPubMedCentralGoogle Scholar
  44. Perez-Lorenzo S, Levy-Benshimol A, Gomez-Acevedo S (1998) Presence of lectins, tannins and protease inhibitors in Venezuelan marine algae. Acta Cient Venez 49:144–151PubMedGoogle Scholar
  45. Petropoulos IK, Thompson KD, Morgan A, Dick JR, Tocher DR, Bell JG (2009) Effects of substitution of dietary fish oil with a blend of vegetable oils on liver and peripheral blood leucocyte fatty acid composition, plasma prostaglandin E2 and immune parameters in three strains of Atlantic salmon (Salmo salar). Aquacult Nutr 15:596–607CrossRefGoogle Scholar
  46. Rao BS, Deshpande V (2005) Experimental biochemistry: a student companion. I K International Pvt Ltd, Tunbridge Wells, Kent, pp 218–222Google Scholar
  47. Rathmann R, Szklo A, Schaeffer R (2010) Land use competition for production of food and liquid biofuels: an analysis of the arguments in the current debate. Renew Energ 10:14–22CrossRefGoogle Scholar
  48. Refstie S, Svihus B, Shearer KD, Storebakken T (1999) Nutrient digestibility in Atlantic salmon and broiler chickens related to viscosity and non-starch polysaccharide content in different soybean products. Aquaculture 79:331–345Google Scholar
  49. Rindi F, Soler-Vila A, Guiry MD (2012) Taxonomy of marine macroalgae used as sources of bioactive compounds. In: Hayes M (ed) Marine bioactive compounds: taxonomy of marine macroalgae used as sources of bioactive compounds. Springer, Berlin, pp 1–53CrossRefGoogle Scholar
  50. Robb DHF, Kestin SC, Warriss PD, Nute GR (2002) Muscle lipid content determines the eating quality of smoked and cooked Atlantic salmon (Salmo salar). Aquaculture 205:345–358CrossRefGoogle Scholar
  51. Ruperez P (2002) Mineral content of edible marine seaweeds. Food Chem 79:23–26CrossRefGoogle Scholar
  52. Saha D, Bhattacharya S (2010) Hydrocolloids as thickening and gelling agents in food: critical review. J Food Sci Techol 47:587–597CrossRefGoogle Scholar
  53. Saksida SM, Marty GD, Jones SRM, Manchester H, Diamond CL, Bidulka J, St-Hilaire S (2012) Parasites and hepatic lesions among pink salmon, Oncorhynchus gorbuscha (Walbaum), during early seawater residence. J Fish Dis 35:137–51CrossRefPubMedGoogle Scholar
  54. Shiau S-Y, Liang S-H (1994) Nutrient digestibility and growth of hybrid tilapia, Oreochromis niloticus x O. aureus, as influenced by agar supplementation at two dietary protein levels. Aquaculture 127:41–48CrossRefGoogle Scholar
  55. Silva DM, Valente LMP, Sousa-Pinto I, Pereira R, Pires MA, Seaxas F, Rema P (2015) Evaluation of IMTA-produced seaweeds (Gracilaria, Porphyra, and Ulva) as dietary ingredients in Nile tilapia, Oreochromis niloticus L., juveniles. Effects on growth performance and gut histology. J Appl Phycol 27:1671–1680Google Scholar
  56. Siwicki AK, Anderson DP (1993) Non-specific defense mechanisms assay in fish. II. Potential killing activity of neutrophils and macrophages, lysozyme activity in serum and organs and total immunoglobulin (Ig) level in serum. In: Siwicki AK, Anderson DP, Waluga J (eds) Fish disease diagnosis and preventions methods. Olsztyn, Poland, pp 105–112Google Scholar
  57. Soler-Vila A, Coughlan S, Guiry MD, Kraan S (2009) The red alga Porphyra dioica as a fish-feed ingredient for rainbow trout (Oncorhynchus mykiss): effects on growth, feed efficiency, and carcass composition. J Appl Phycol 21:617–624CrossRefGoogle Scholar
  58. Spencer K, Price CP (1977) Influence of reagent quality and reaction conditions on the determination of serum albumin by the bromocresol green dye-binding method. Ann Clin Biochem 14:105–115CrossRefPubMedGoogle Scholar
  59. Stadtlander T, Khalil WKB, Focken U, Becker K (2013) Effects of low and medium levels of red alga Nori (Porphyra yezoensis Ueda) in the diets on growth, feed utilization and metabolism in intensively fed Nile tilapia, Oreochromis niloticus (L.). Aquac Nutr 19:64–73CrossRefGoogle Scholar
  60. Storebakken T, Austreng E (1987) Binders in fish feeds: II. Effect of different alginates on the digestibility of macronutrients in rainbow trout. Aquaculture 60:121–131CrossRefGoogle Scholar
  61. Sturmbauer C (1991) Different enzymes for laminarine digestion in Chondrostoma nasus (cyprinidae) and Oreochromis sp. (cichlidae). Comp Biochem Physiol A 100:199–202CrossRefGoogle Scholar
  62. Trinder P (1969) Determination of glucose using glucose oxidase with an alternative oxygen acceptor. Ann Clin Biochem 6:24–27CrossRefGoogle Scholar
  63. Underwood AJ (1996) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  64. Valente LMP, Gouveia A, Rema P, Matos J, Gomes EF, Pinto IS (2006) Evaluation of three seaweeds Gracilaria bursa-pastoris, Ulva rigida and Gracilaria cornea as dietary ingredients in European sea bass (Dicentrarchus labrax) juveniles. Aquaculture 252:85–91CrossRefGoogle Scholar
  65. Vizcaíno AJ, Mendes SI, Varela JL, Ruiz-Jarabo I, Rico R, Figueroa FL, Abdala R, Morinogo MA, Mancera JM, Alacon FJ (2015) Growth, tissue metabolites and digestive functionality in Sparus aurata juveniles fed different levels of macroalgae, Gracilaria cornea and Ulva rigida. Aquac Res. doi: 10.1111/are.12774 Google Scholar
  66. Walker AB, Fournier HR, Neefus CD, Nardi GC, Berlinsky DL (2009) Partial replacement of fish meal with laver Porphyra spp. in diets for Atlantic cod. N Am J Aquacult 71:39–45CrossRefGoogle Scholar
  67. Wassef EA, El-Sayed A-FM, Sakr EM (2013) Pterocladia (Rhodophyta) and Ulva (Chlorophyta) as feed supplements for European seabass, Dicentrarchus labrax L., fry. Appl Phycol 25:1369–1376CrossRefGoogle Scholar
  68. Wiegertjes GF, Stet RJM, Parmentier HK, Van Muiswinkel WB (1996) Immunogenetics of disease resistance in fish: a comparative approach. Dev Comp Immunol 20:365–381CrossRefPubMedGoogle Scholar
  69. Yano T (1992) Assays for haemolytic complement activity. In: Stolen JS, Fletcher TC, Anderson DP, Kaattari SL, Rowley AF (eds) Techniques in fish immunology. FITC2 SOS Publications, Fairhaven, pp 131–141Google Scholar
  70. Yuan YV, Carrington MF, Walsh N (2005) Extracts from dulse (Palmaria palmata) are effective antioxidants and inhibitors of cell proliferation in vitro. Food Chem Toxicol 43:1073–1081CrossRefPubMedGoogle Scholar
  71. Yuan YV, Westcott ND, Hu C, Kitts DD (2009) Mycosporine-like amino acid composition of the edible red alga, Palmaria palmata (dulse) harvested from the west and east coasts of Grand Manan Island, New Brunswick. Food Chem 112:321–328CrossRefGoogle Scholar
  72. Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice and Hall, New Jersey, p 187Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Alex H. L. Wan
    • 1
  • Anna Soler-Vila
    • 1
  • Damien O’Keeffe
    • 2
  • Paul Casburn
    • 2
  • Richard Fitzgerald
    • 2
  • Mark P. Johnson
    • 1
  1. 1.Irish Seaweed Research Group, Ryan Institute and School of Natural SciencesNational University of IrelandGalwayIreland
  2. 2.Carna Research Station, Ryan InstituteNational University of IrelandGalwayIreland

Personalised recommendations