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

Journal of Applied Phycology

Volumn 28, Issue 5, 2016, Pages 3091-3100

  Wan, Alex H L ^a   Soler Vila, Anna ^a   O’Keeffe, Damien ^a   Casburn, Paul ^a   Fitzgerald, Richard ^a   Johnson, Mark P ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Atlantic salmon; Blood parameters; Dillisk; Macroalgae; Palmaria palmata; Seaweed

Indexed keywords

EID: 84960336787     PISSN: 09218971     EISSN: 15735176     Source Type: Journal    
DOI: 10.1007/s10811-016-0821-8     Document Type: Article

References (72)

1. AOAC (1995) Official methods of analysis of the Association of Official Analytical Chemists, 5th edn. Association of Official Analytical Chemists, Inc., USA
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 28:679–689
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 42:525–533
4. Bain BJ, Lewis SM, Bates I (2006) Basic haematological techniques. In: Dacie and Lewis practical haematology, 10th edn. Churchill Livingstone, New York, pp 26–59
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 23:115–127
6. Bansemir A, Blume M, Schröder S, Lindequist U (2006) Screening of cultivated seaweeds for antibacterial activity against fish pathogenic bacteria. Aquaculture 252:79–84
7. Boettcher AA, Target NM (1993) Role of polyphenolic molecular size in reduction of assimilation efficiency in Xiphister mucosus. Ecology 74:891–903
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 72:248–254
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 316:68–76
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 152:249–258
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 7:305–308
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 17:355–361
13. FAO (2009) How to feed the world by 2050. URL: http://www.fao.org/fileadmin/templates/wsfs/docs/expert_paper/How_to_Feed_the_World_in_2050.pdf Accessed 23 June 2013
14. FAO (2014) The State of World Fisheries and Aquaculture 2014. www.fao.org/3/a-i3720e.pdf Accessed 23 Dec 2015
15. Fleurence J (1999) Seaweed proteins: biochemical, nutritional aspects and potential uses. Trends Food Sci Tech 10:25–28
16. Francis G, Makkar HP, Becker K (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199:197–227
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 10:353–9
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 356–357:73–79
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 38:551–579
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 11:1176–1183
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 174:223–232
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 21:605–615
23. Halver JE, Hardy RW (2002) Fish nutrition. Academic Press, Elsevier Science, USA
24. Hardy R (2010) Utilization of plant proteins in fish diets: effects of global demand and supplies of fishmeal. Aquacult Res 41:770–776
25. Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597
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 42:1135–1141
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 28:377–84
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 308:136–144
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 9:361–371
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 185:870–880
31. Macartain P, Gill CIR, Brooks M, Campbell R, Rowland IR (2007) Nutritional value of edible seaweeds. Nutr Rev 65:535–543
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 47:339–344
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 17:99–102
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) 96:474–481
35. Morgan K, Wright J, Simpson F (1980) Review of chemical constituents of the red alga Palmaria palmata (dulse). Econ Bot 34:27–50
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 25:1777–1791
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 12:67–72
38. Nakagawa S (2004) A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15:1044–1045
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 43:1570–1573
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 106:15103–10
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–e436
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 61:443–52
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 10:1920–1935
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 49:144–151
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 15:596–607
46. Rao BS, Deshpande V (2005) Experimental biochemistry: a student companion. I K International Pvt Ltd, Tunbridge Wells, Kent, pp 218–222
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 10:14–22
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 79:331–345
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 1–53
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 205:345–358
51. Ruperez P (2002) Mineral content of edible marine seaweeds. Food Chem 79:23–26
52. Saha D, Bhattacharya S (2010) Hydrocolloids as thickening and gelling agents in food: critical review. J Food Sci Techol 47:587–597
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 35:137–51
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 127:41–48
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 27:1671–1680
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 105–112
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 21:617–624
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 14:105–115
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 19:64–73
60. Storebakken T, Austreng E (1987) Binders in fish feeds: II. Effect of different alginates on the digestibility of macronutrients in rainbow trout. Aquaculture 60:121–131
61. Sturmbauer C (1991) Different enzymes for laminarine digestion in Chondrostoma nasus (cyprinidae) and Oreochromis sp. (cichlidae). Comp Biochem Physiol A 100:199–202
62. Trinder P (1969) Determination of glucose using glucose oxidase with an alternative oxygen acceptor. Ann Clin Biochem 6:24–27
63. Underwood AJ (1996) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge
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 252:85–91
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
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 71:39–45
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 25:1369–1376
68. Wiegertjes GF, Stet RJM, Parmentier HK, Van Muiswinkel WB (1996) Immunogenetics of disease resistance in fish: a comparative approach. Dev Comp Immunol 20:365–381
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 131–141
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 43:1073–1081
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 112:321–328
72. Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice and Hall, New Jersey, p 187