Journal of Applied Phycology

, Volume 27, Issue 4, pp 1671–1680 | Cite as

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

  • D. M. Silva
  • L. M. P. Valente
  • I. Sousa-Pinto
  • R. Pereira
  • M. A. Pires
  • F. Seixas
  • P. Rema


The present study evaluated the effects of the inclusion of three seaweeds, Gracilaria vermiculophylla (GRA), Porphyra dioica (POR), and Ulva spp. (ULV), as dietary ingredients for Nile tilapia (Oreochromis niloticus) juveniles, on the growth performance, body composition, and gut histology. Three experimental diets (GRA, POR, and ULV) were formulated to replace 10 % of whole diet by each of the three seaweeds. A control diet (CTRL) was used, without inclusion of any seaweed. Diets were fed to triplicate groups of 25 Nile tilapia juveniles, with an average body weight (ABW) of 12.1 g, in an 84-day trial. At the end of the trial, growth performance was significantly reduced (P < 0.05) in fish fed the GRA diet, whereas the feed conversion ratio increased significantly in those fish. None of the treatments caused adverse effects on body composition. The inclusion of the three seaweeds in the diet led to evident changes in the fish digestive system morphology with significant reduction of villi length on GRA diet. The results obtained in this study suggest the usefulness of P. dioica and Ulva spp. to partially replace fishmeal in practical diets for tilapia juveniles up to 10 %, as no negative consequences on growth performance or body composition were observed. However, the inclusion of 10 % G. vermiculophylla seems to have a negative effect in diet palatability, reducing fish feed intake and growth performance.


Nile tilapia Alternative feed ingredients Seaweeds Gracilaria vermiculophylla Porphyra dioica Ulva spp. 



This work was funded by the “European fund for regional development” (FEDER), in the context of the Operational Competitiveness Programme (COMPETE), by “Fundação para a Ciência e a Tecnologia” (FCT), under the Project Benefits (PTDC/MAR/105229/2008) n. FCOMP-01-0124-FEDER-010622 and Project Pest-OE/AGR/UI0772/2014.


  1. Abdel-Tawwab M, Ahmad MH, Khattab YAE, Shalaby AME (2010) Effect of dietary protein level, initial body weight, and their interaction on the growth, feed utilization, and physiological alterations of Nile tilapia, Oreochromis niloticus (L.). Aquaculture 298:267–274CrossRefGoogle Scholar
  2. 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
  3. Alexis MN (1997) Fishmeal and fish oil replacers in Mediterranean marine fish diets. In: Tacon A, Barsureo B (eds) Feeding tomorrow’s fish. Proceedings of the Workshop of the CIHEAM Network on Technology of Aquaculture in the Mediterranean. CIHEAM, Zaragoza, pp 183–204Google Scholar
  4. AOAC, Association of Official Analytical Chemists (2006) Official Methods of Analysis, 18th edn. USA, Washington DCGoogle Scholar
  5. Azaza MS, Mensi F, Ksouri J, Dhraief MN, Brini B, Abdelmouleh A, Kraïem MM (2008) Growth of Nile tilapia (Orechromis niloticus L.) fed with diets containing graded levels of green algae Ulva meal (Ulva rigida) reared in geothermal waters of southern waters of southern Tunisia. J Appl Ichthyol 24:202–207CrossRefGoogle Scholar
  6. Azaza MS, Wassim K, Mensi F, Abdelmouleh A, Brimi B, Kraïem MM (2009) Evaluation of faba beans (Vicia faba L. var. minuta) as a replacement for soybean meal in practical diets of juvenile Nile tilapia Oreochromis niloticus. Aquaculture 287:174–179CrossRefGoogle Scholar
  7. Bajpai S, Sharma A, Gupta MN (2005) Removal and recovery of antinutritional factors from soybean flour. Food Chem 89:497–501CrossRefGoogle Scholar
  8. Bardocz S, Ewen SWB, Grant G, Pusztai A (1995) Lectins as growth factors for the small intestine and the gut. In: Pusztai A, Bardocz S (eds) Lectins—biomedical perspectives. Taylor & Francis, London, pp 103–116Google Scholar
  9. Benevides N, Silva S, Magalhães S, Melo F, Freitas A, Vasconcelos M (1998) Proximate analysis, toxic and antinutritional factors of ten Brazilian marine algae. Rev Brasil Fisiol Veg 10:31–36Google Scholar
  10. Briand X, Morand P (1997) Anaerobic digestion of Ulva sp. 1 Relationship between Ulva composition and methanisation. J Appl Phycol 9:511–524Google Scholar
  11. Buschmann AH, Troell M, Kautsky N (2001) Integrated algal farming: a review. Cah Biol Mar 42:83–90Google Scholar
  12. Buschmann AH, Varela DA, Hernández-González MC, Huovinen P (2008) Opportunities and challenges for the development of an integrated seaweed-based aquaculture activity in Chile: determining the physiological capabilities of Macrocystis and Gracilaria as biofilters. J Appl Phycol 20:571–577CrossRefGoogle Scholar
  13. Bunker FStPD, Brodie JA, Maggs CA and Bunker AR (2010) “Seasearch” guide to seaweeds of Britain and Ireland. Marine Conservation Society, Ross-on-WyeGoogle Scholar
  14. Carmona R, Kraemer GP, Yarish C (2006) Exploring Northeast American and Asian species of Porphyra for use in an integrated finfish-algal aquaculture system. Aquaculture 252:54–65CrossRefGoogle Scholar
  15. Caspary WF (1992) Physiology and pathophysiology of intestinal absorption. Am J Clin Nutr 55:2995–3085Google Scholar
  16. Chopin T, Yarish C, Wilkes R, Belyea E, Lu S, Mathieson A (1999) Developing Porphyra/salmon integrated aquaculture for bioremediation and diversification of the aquaculture industry. J Appl Phycol 11:463–472CrossRefGoogle Scholar
  17. Chopin T, Buschmann AH, Halling C, Troell M, Kautsky N, Neori A, Kraemer GP, Zertuche-Gonzalez JA, Yarish C, Neefus C (2001) Integrating seaweeds into marine aquaculture systems: a key toward sustainability. J Phycol 37:975–986CrossRefGoogle Scholar
  18. Chopin T, Robinson SMC, Troell M, Neori A, Buschmann AH, Fang J (2008) Multitrophic integration for sustainable marine aquaculture. In: Jorgensen S, Fath B (eds) Encyclopedia of ecology. Ecological engineering, vol 3. Elsevier, Oxford: 2463–2475Google Scholar
  19. Dallaire V, Lessard P, Vandenberg G, de la Noüe J (2007) Effect of algal incorporation on growth, survival and carcass composition of rainbow trout (Oncorhynchus mykiss) fry. Bioresourc Technol 98:1433–1439CrossRefGoogle Scholar
  20. Darcy-Vrillon B (1993) Nutritional aspects of the developing use of marine macroalgae for the human food industry. Int J Food Sci Nutr 44:23–35Google Scholar
  21. 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
  22. Dawczynski C, Schubert R, Jahreis G (2007) Amino acids, fatty acids, and dietary fibre in edible seaweed products. Food Chem 103:891–899CrossRefGoogle Scholar
  23. Díaz-Rosales P, Burmeister A, Aguilera J, Korbee N, Moriñigo MA, Figueroa FL, Chabrillón M, Arijo S, Lindequist U, Balebona MC (2005) Screening of algal extracts as potential stimulants of chemotaxis and respiratory burst activity of phagocytes from sole (Solea senegalensis). Bull Europ Assoc Fish Pathol 25:9–19Google Scholar
  24. Diler I, Tekinay A, Güroy D, Güroy B, Soyuturk M (2007) Effects of Ulva rigida on the growth, feed intake and body composition of common carp, Cyprinus carpio. J Biol Sci 7:305–308CrossRefGoogle Scholar
  25. Dworjanyn I, Pirozzi I, Liu W (2007) The effect of the addition of algae feeding stimulants to artificial diets for the sea urchin Tripneustes gratilla. Aquaculture 273:624–633CrossRefGoogle Scholar
  26. El-Saidy D, Gaber M (2003) Replacement of fish meal with a mixture of different plant protein sources in juvenile Nile tilapia, Oreochromis niloticus (L.) diets. Aquac Res 34:1119–1127CrossRefGoogle Scholar
  27. El-Sayed AFM (1998) Total replacement of fish meal with animal protein sources in Nile tilapia, Oreochromis niloticus (L.), feeds. Aquac Res 29:275–280CrossRefGoogle Scholar
  28. Ergün S, Soytürk M, Güroy B, Güroy D, Merrifield D (2009) 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
  29. FAO (2012) The state of world fisheries and aquaculture 2012. FAO, RomeGoogle Scholar
  30. Feldlite M, Juanicó M, Karplus I, Milstein A (2008) Towards a safe standard for heavy metals in reclaimed water used for fish aquaculture. Aquaculture 284:115–126CrossRefGoogle Scholar
  31. Fiogbé ED, Micha JC, Van Hove C (2004) Use of a natural aquatic fern, Azolla microphylla, as a main component in food for the omnivorous-phytoplanktonophagous tilapia, Oreochromis niloticus L. J Appl Ichthyol 20:517–520CrossRefGoogle Scholar
  32. Fleurence J (1999) Seaweed proteins: biochemical, nutritional aspects and potential uses. Trends Food Sci Tech 10:25–28CrossRefGoogle Scholar
  33. Fleurence J (2004) Seaweed proteins. In: Yada RY (ed) Proteins in food processing. Woodhead Publishing, Cambridge, pp 197–213CrossRefGoogle Scholar
  34. Fleurence J, Morançais M, Dumay J, Decottignies P, Turpin V, Munier M, Garcia-Bueno N, Jaouen P (2012) What are the prospects for using seaweed in human nutrition and for marine animals raised through aquaculture? Trends Food Sci Tech 27:57–61CrossRefGoogle Scholar
  35. Francis G, Makkar HPS, Becker K (2001) Antinutritional factors present in plant derived alternative fish feed ingredients and their effects in fish. Aquaculture 199:197–227CrossRefGoogle Scholar
  36. García-Casal MN, Pereira AC, Leets I, Ramírez J, Quiroga MF (2007) High iron content and bioavailability in humans from four species of marine algae. J Nutr 137:2691–2695PubMedGoogle Scholar
  37. Güroy BK, Cirik S, Güroy D, Sanver F, Tekinay AA (2007) Effets of Ulva rigida and Cystoseira barbata meals as a feed additive on growth performance, feed utilization, and body composition of Nile tilapia, Oreochromis niloticus. Turk J Vet Anim Sci 31:91–97Google Scholar
  38. Güroy D, Güroy B, Merrifield DL, Ergün S, Tekinay AA, Yigit M (2011) Effects of dietary Ulva and Spirulina on weight loss and body composition of rainbow trout, Oncorhynchus mykiss (Walbaum), during a starvation period. J Anim Physiol Anim Nutr 95:320–327CrossRefGoogle Scholar
  39. Güroy B, Ergün S, Merrifield DL, Güroy D (2013) Effect of autoclaved Ulva meal on growth performance, nutrient utilization and fatty acid profile of rainbow trout, Oncorhynchus mykiss. Aquacult Int 21:605–615CrossRefGoogle Scholar
  40. Heidarieh M, Mirvaghefi AR, Akbari M, Farahmand H, Sheikhzadeh N, Shahbazfar AA, Behgar M (2012) Effect of dietary Ergosan on growth performance, digestive enzymes, intestinal histology, hematological parameters and body composition of rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 38:1169–1174PubMedCrossRefGoogle Scholar
  41. Holdt SL, Edwards MD (2014) Cost-effective IMTA: a comparison of the production efficiencies of mussels and seaweed. J Appl Phycol 26:933–945CrossRefGoogle Scholar
  42. Horie Y, Sugase K, Horie K (1995) Physiological difference of soluble and insoluble dietary fibre fractions of brown algae and mushrooms in pepsin activity in vitro and protein digestibility. Asia Pac J Clin Nutr 4:251–255PubMedGoogle Scholar
  43. Khotimchenko SV, Vaskovsky VE, Titlyanova TV (2002) Fatty acids of marine algae from the Pacific coast of North California. Bot Mar 45:17–22CrossRefGoogle Scholar
  44. Klurfeld DM (1999) Nutritional regulation of gastrointestinal growth. Front Biosci 4:299–302CrossRefGoogle Scholar
  45. Krogdahl A, Nordrum S, Sørensen M, Brudeseth L, Røsjø C (1999) Effects of diet composition on apparent nutrient absorption along the intestinal tract and of subsequent fasting on mucosal disaccharidase activities and plasma nutrient concentration in Atlantic salmon, Salmo salar L. Aquacult Nutr 5:121–133CrossRefGoogle Scholar
  46. Kumar V, Akinleye AO, Makkar HPS, Angulo-Escalante MA, Becker K (2012) Growth performance and metabolic efficiency in Nile tilapia (Oreochromis niloticus L.) fed on a diet containing Jatropha platyphylla kernel meal as a protein source. J Anim Physiol Anim Nutr 96:37–46CrossRefGoogle Scholar
  47. Li P, Mai K, Trushenski J, Wu G (2009) New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino Acids 37:43–53PubMedCrossRefGoogle Scholar
  48. Liener IE (1994) Implications of antinutritional components in soybean foods. CRC Crit Rev Food Sci Nutr 34:31–67CrossRefGoogle Scholar
  49. Lovell RT (2002) Diet and fish husbandry. In: Halver JE, Hardy RW (eds) Fish Nutrition. Academic, San Diego, pp 703–754Google Scholar
  50. Lupatsch I (2009) Quantifying nutritional requirements in aquaculture—the factorial approach. In: Burnell G, Allan G (eds) New technologies in aquaculture: improving, production efficiency, quality and environmental management. Woodhead Publishing, Cambridge, pp 417–439CrossRefGoogle Scholar
  51. Mai K, Zhang L, Ai Q, Duan Q, Zhang C, Li H, Wan J, Liufu Z (2006a) Dietary lysine requirement of juvenile seabass (Lateolabrax japonicas). Aquaculture 258:535–542CrossRefGoogle Scholar
  52. Mai K, Wan J, Ai Q, Xu W, Liufu Z, Zhang L, Zhang C, Li H (2006b) Dietary methionine requirement of juvenile yellow croaker Pseudosciaena crocea R. Aquaculture 251:564–572CrossRefGoogle Scholar
  53. Marinho G, Nunes C, Sousa-Pinto I, Pereira R, Rema P, Valente LMP (2013) The IMTA-cultivated Chlorophyta Ulva spp. as a sustainable ingredient in Nile tilapia (Oreochromis niloticus) diets. J Appl Phycol 25:1359–1367CrossRefGoogle Scholar
  54. Mata L, Schuenhoff A, Santos R (2010) A direct comparison of the performance of the seaweed biofilters, Asparagopsis armata and Ulva rigida. J Appl Phycol 22:639–644CrossRefGoogle Scholar
  55. Merrifield DL, Harper GM, Mustafa S, Carnevali O, Picchietti S, Davies SJ (2011) Effect of dietary alginic acid on juvenile tilapia (Oreochromis niloticus) intestinal microbial balance, intestinal histology and growth performance. Cell Tissue Res 344:135–146PubMedCrossRefGoogle Scholar
  56. Moldal T, Løkka G, Wiik-Nielsen J, Austbø L, Torstensen BE, Rosenlund G, Dale OB, Kaldhusdal M, Koppang EO (2014) Substitution of dietary fish oil with plant oils is associated with shortened mid intestinal folds in Atlantic salmon (Salmo salar). BMC Vet Res 10:60PubMedCentralPubMedCrossRefGoogle Scholar
  57. Moyano FJ, Diaz MI, Diaz M, Alarcon FJ (1999) Inhibition of digestive proteases by vegetable meals in three fish species: seabream (Sparus aurata), tilapia (Oreochromis niloticus) and African sole (Solea senegalensis). Comp Biochem Phys B 122:327–332CrossRefGoogle Scholar
  58. Mustafa MG, Nakagawa H (1995) A review: dietary benefits of algae as an additive in fish feed. The Bamidgeh 47:155–162Google Scholar
  59. Nakagawa H, Umino T, Tasaka Y (1997) Usefulness of Ascophyllum meal as feed additive for red sea bream, Pagrus major. Aquaculture 151:275–281CrossRefGoogle Scholar
  60. Naylor RL, Goldburg RJ, Primavera JH, Kautsky N, Beveridge MC, Clay J, Folke C, Lubchenco J, Mooney H, Troell M (2000) Effect of world aquaculture on world fish supplies. Nature 405:1017–1024PubMedCrossRefGoogle Scholar
  61. Neori A, Shpigel M, Ben-Ezra D (2000) A sustainable integrated system for culture of fish, seaweed and abalone. Aquaculture 186:279–291CrossRefGoogle Scholar
  62. Neori A, Chopin T, Troell M, Buschmann AH, Kraemer GP, Halling C, Shpigel M, Yarish C (2004) Integrated aquaculture: rationale, evolution and state of the art emphasizing seaweed biofiltration in modern mariculture. Aquaculture 231:361–391CrossRefGoogle Scholar
  63. Nobre AM, Robertson-Andersson D, Neori A, Sankar K (2010) Ecological–economic assessment of aquaculture options: comparison between abalone monoculture and integrated multi-trophic aquaculture of abalone and seaweeds. Aquaculture 306:116–126CrossRefGoogle Scholar
  64. Norziah MH, Ching CY (2000) Nutritional composition of edible seaweed Gracilaria raggi—an edible species of nori from Nova Scotia. Food Chem 68:69–76CrossRefGoogle Scholar
  65. NRC (1993) Nutrients requirements of fish. National Academy Press, Washington DC, USAGoogle Scholar
  66. Nyberg CD, Wallentinus I (2009) Long-term survival of an introduced red alga in adverse conditions. Mar Biol Res 5:304–308CrossRefGoogle Scholar
  67. Nyberg CD, Thomsen MS, Wallentinus I (2009) Flora and fauna associated with the introduced red alga Gracilaria vermiculophylla. Eur J Phycol 44:395–403CrossRefGoogle Scholar
  68. Oliveira M, Freitas A, Carvalho A, Sampaio T, Farias D, Teixeira D, Gouveia S, Pereira J, Sena M (2009) Nutritive and non-nutritive attributes of washed-up seaweeds from the coast of Ceará, Brazil. Food Chem 115:254–259CrossRefGoogle Scholar
  69. Olvera-Novoa MA, Olivera-Castillo L, Martinez-Palacios CA (2002) Sunflower seed meal as a protein source in diets for Tilapia rendalli (Boulanger, 1896) fingerlings. Aquacult Res 33:223–229CrossRefGoogle Scholar
  70. Ortiz J, Romero N, Robert P, Araya J, Lopez-Hernández J, Bozzo C, Navarrete E, Osorio A, Rios A (2006) Dietary fiber, amino acid, fatty acid and tocopherol contents of the edible seaweeds Ulva lactuca and Durvillacea antarctica. Food Chem 99:98–104CrossRefGoogle Scholar
  71. Patarra RF, Paiva L, Neto AI, Lima E, Baptista J (2011) Nutritional value of selected macroalgae. J Appl Phycol 23:205–208CrossRefGoogle Scholar
  72. Peinado MJ, Ruiz R, Echávarri A, Rubio LA (2012) Garlic derivative propyl propane thiosulfonate is effective against broiler enteropathogens in vivo. Poultry Sci 91:2148–2157CrossRefGoogle Scholar
  73. Peng C, Hong-BO S, Di X, Song Q (2009) Progress in Gracilaria biology and developmental utilization: main issues and prospective. Rev Fish Sci 17:494–504CrossRefGoogle Scholar
  74. Pereira R, Sousa-Pinto I, Yarish C (2004) Field and culture studies of the life history of Porphyra dioica (Bangiales, Rhodophyta) from Portugal. Phycologia 43:756–767CrossRefGoogle Scholar
  75. Pereira R, Yarish C, Sousa-Pinto I (2006) The influence of stocking density, light and temperature on the growth, production and nutrient removal capacity of Porphyra dioica (Bangiales, Rhodophyta). Aquaculture 252:66–78CrossRefGoogle Scholar
  76. Pereira R, Valente LMP, Sousa-Pinto I, Rema P (2012) Apparent nutrient digestibility of seaweeds by rainbow trout (Oncorhynchus mykiss) and Nile tilapia (Oreochromis niloticus). Algal Res 1:77–82CrossRefGoogle Scholar
  77. Pirarat N, Pinpimai K, Endo M, Katagiri T, Ponpornpisit A, Chansue N, Maiata M (2011) Modulation of intestinal morphology and immunity in Nile tilapia (Oreochromis niloticus) by Lactobacillus rhamnosus GG. Res Vet Sci 91:92–97CrossRefGoogle Scholar
  78. Rinchard J, Mbahinzireki G, Dabrowski K, Lee KJ, Garcia-Abiado MA, Ottobre J (2002) Effects of dietary cottonseed meal protein level on growth, gonad development and plasma sex steroid hormones of tropical fish tilapia Oreochromis sp. Aquacult Int 10:11–28CrossRefGoogle Scholar
  79. Reyes-Becerril M, Guardiola F, Rojas M, Ascencio-Valle F, Esteban MA (2013) Dietary administration of microalgae Navicula sp. affects immune status and gene expression of gilthead seabream (Sparus aurata). Fish Shellfish Immunol 35:883–889PubMedCrossRefGoogle Scholar
  80. Robaina L, Izquierdo MS, Moyano FJ, Socorro J, Vergara JM, Montero D, Fernández-Palacios H (1995) Soybean and lupin seed meals as protein sources in diets for gilthead seabream (Sparus aurata): nutritional and histological implications. Aquaculture 130:219–233CrossRefGoogle Scholar
  81. Sáez MI, Barros AM, Martinez TF, Rico RM, Tapia S T, Mancera JM, Lopez-Figueroa F, Abdala R, Morioigo MA, Alarcon FJ (2012) Effect of dietary inclusion of seaweeds on intestinal proteolytic activity of juvenile seabream, Sparus aurata. Paper presented in 15th Int. Symp. of Nutrition and Feeding of Fish, P6, Book of abstracts, Molde, Norway, 4–7 June 2012Google Scholar
  82. Schuenhoff A, Sphigel M, Lupatsch I, Ashkenazi A, Msuya FE, Neori A (2003) A semi-recirculating, integrated system for the culture of fish and seaweed. Aquaculture 221:167–181CrossRefGoogle Scholar
  83. Sitjà-Bobadilla A, Padrós F, Aguilera C, Alvarez-Pellitero P (2005) Epidemiology of Cryptosporidium molnari in Spanish gilthead sea bream (Sparus aurata L.) and European sea bass (Dicentrarchus labrax L.) cultures: from hatchery to market size. Appl Environ Microbiol 71:131–139PubMedCentralPubMedCrossRefGoogle Scholar
  84. 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
  85. 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.). Aquacult Nutr 19:64–73CrossRefGoogle Scholar
  86. Sugiura SH, Raboy V, Young KA, Dong FM, Hardy RW (1999) Availability of phosphorus trace elements in low-phytate varieties of barley and corn for rainbow trout (Oncorhynchus mykiss). Aquaculture 70:285–296CrossRefGoogle Scholar
  87. Tacon AG (1995) Fishmeal replacers: review of antinutrients within oilseeds and pulses. A limiting factor for the aquafeed green revolution, Feed Ingredients, Asia, SingaporeGoogle Scholar
  88. Tacon A, Hasan M, Subasinghe R (2006) Use of fishery resources as feed inputs for aquaculture development: trends and policy implications. FAO Fisheries Circular No. 1018. 99Google Scholar
  89. Thomsen MS, Glathery M (2007) Stress tolerance of the invasive macroalgae Codium fragile and Gracilaria vermiculophylla in a soft-bottom turbid lagoon. Biol Invasions 9:499–513CrossRefGoogle Scholar
  90. Thompson KR, Velasquez A, Patterson JT, Metts LS, Webster CD, Brady YJ, Gannam AL, Twibell RG, Ostrand SL (2012) Evaluation of plant and animal protein sources as partial or total replacement of fish meal in diets for Nile tilapia fry and juvenile stages. N Am J Aquacult 74(3):365–375CrossRefGoogle Scholar
  91. Troell M, Halling C, Neori A, Chopin T, Buschmann AH, Kautsky N, Yarish C (2003) Integrated mariculture: asking the right questions. Aquaculture 226:69–90CrossRefGoogle Scholar
  92. Troell M, Joyce A, Chopin T, Neori A, Buschmann AH, Fang JG (2009) Ecological engineering in aquaculture —potential for integrated multi-trophic aquaculture (IMTA) in marine offshore systems. Aquaculture 297:1–9CrossRefGoogle Scholar
  93. Valente LMP, Gouveia A, Rema P, Matos J, Gomes EF, Sousa-Pinto I (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
  94. Walker AB, Berlinsky DL (2011) Effects of partial replacement of fishmeal protein by microalgae on growth, feed intake, and body composition of Atlantic cod. N Am J Aquac 73:76–83Google Scholar
  95. Wassef EA, El Masry MH, Mikhail FR (2001) Growth enhancement and muscle structure of striped mullet, Mugil cephalus L., fingerlings by feeding algal meal-based diets. Aquacult Res 32:315–322CrossRefGoogle Scholar
  96. Xuan X, Wen X, Li S, Zhu D, Li Y (2013) Potential use of macro-algae Gracilaria lemaneiformis in diets for the black sea bream, Acanthopagrus schlegelii, juvenile. Aquaculture 412–413:167–172CrossRefGoogle Scholar
  97. Yarish C, Pereira R (2008) Mass production of marine macroalgae. In: Jørgensen SE, Fath BD (eds) Ecological engineering. Encyclopedia of ecology vol 3. Elsevier, Oxford, pp 2236–2247Google Scholar
  98. Yldirim Ö, Ergün S, Yaman S, Türker A (2009) Effects of two seaweeds (Ulva lactuca and Enteromorpha linza) as a feed additive in diets on growth performance, feed utilization, and body composition of rainbow trout (Oncorhynchus mykiss). Kafkas Univ Vet Fak Derg 15(3):455–460Google Scholar
  99. Yokoyama H, Ishihi Y (2010) Bioindicator and biofilter function of Ulva spp. (Chlorophyta) for dissolved inorganic nitrogen discharged from a coastal fish farm—potential role in integrated multi-trophic aquaculture. Aquaculture 310:74–83CrossRefGoogle Scholar
  100. Zar J (1999) Biostatistical analysis, 4th edn. Prentice Hall, USA., 663pGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • D. M. Silva
    • 1
  • L. M. P. Valente
    • 1
    • 2
  • I. Sousa-Pinto
    • 1
    • 3
  • R. Pereira
    • 1
    • 4
  • M. A. Pires
    • 5
  • F. Seixas
    • 5
  • P. Rema
    • 5
  1. 1.CIIMAR/CIMAR–Centro Interdisciplinar de Investigação Marinha e AmbientalPortoPortugal
  2. 2.ICBAS—Instituto Ciências Biomédicas Abel SalazarUniversidade do PortoPortoPortugal
  3. 3.Departamento de Biologia, Faculdade de CiênciasUniversidade do PortoPortoPortugal
  4. 4.AlgaPlusÍlhavoPortugal
  5. 5.CECAV/UTAD, Universidade de Trás-os-Montes e Alto DouroVila RealPortugal

Personalised recommendations