Nutrient composition and protein quality of microalgae meals produced from the marine prymnesiophyte Pavlova sp. 459 mass-cultivated in enclosed photobioreactors for potential use in salmonid aquafeeds

  • Sean M. TibbettsEmail author
  • Shane J. J. Patelakis
  • Crystal G. Whitney-Lalonde
  • Laura L. Garrison
  • Cheryl L. Wall
  • Scott P. MacQuarrie


Pavlova sp. 459 has been used as a high-quality liquid live-feed for cultivated bivalves, while this is its first evaluation as a low-trophic dry aquafeed ingredient. Pav459 was batch-cultivated in photobioreactors and prepared as an intact-cell meal (direct freeze-drying) and a cell-ruptured meal (freeze-drying following microfluidic high-pressure homogenization) and evaluated for nutritional characteristics relevant for salmonid aquafeeds. Protein quality was based on essential amino acid (EAA) profiles, chemical scores, and in vitro 2-phase gastric/pancreatic digestion (GPD) for salmonids. Nutrients were well-preserved after processing and meals contained 66% protein, 16% lipid, 7% carbohydrate, 24 MJ kg-1 DW energy, and 11% ash. Protein quality of the meals was good as indicated by their high EAA/non-EAA ratios (0.91), high EAA indices of 0.82–1.06 (relative to egg albumin, premium fish meal, and soy protein), high chemical scores (1.4–2.2) for most EAAs (calculated against published salmonid dietary requirements), and high in vitro GPD (82%), irrespective of cell-rupture. Pav459 meals contained health-promoting compounds (fucoxanthin, 358–368 mg (100 g)-1 DW; lutein, 101–162 mg (100 g)-1 DW; total phenolic compounds, 33 mg gallic acid equivalents g1 DW) with negligible contaminating heavy metals (< 1 ppm) and anti-nutritional factors (ANFs) (1 TUI mg1 DW trypsin inhibition; < 10 mg g1DW phytate). Pav459 lipid was highest in PUFA (> 60% of FAME), most of which was nutritionally superior n-3 series (50–52% of FAME) relative to n-6 series (10% of FAME). In addition, the vast majority of n-3 PUFA (81%) was comprised of essential LC-PUFA, eicosapentaenoic acid (EPA, 20:5n-3) at 3% of the meals and docosahexaenoic acid (DHA, 22:6n-3) at 2% of the meals.


Composition Haptophyta In vitro digestibility Microalgae Pavlova Salmonids 



The authors thank all of those who kindly provided valuable expertise and assistance during the study. In particular, Sabahudin Hrapovic, Roumiana Stefanova, and Fang Huang kindly provided the SEM images, carotenoid composition, and ANFs data, respectively. Technical consultations and logistical support of Drs. Patrick McGinn and Fabrice Berrué are greatly appreciated and the helpful reviews of Ms. Kathryn Dickinson and Dr. Stefanie Colombo are acknowledged. This is ACRD publication no. 56444.

Funding information

This work was financially supported by NRC’s Algal Carbon Conversion and AgriFood programs.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Acién FG, Molina E, Fernández-Sevilla JM, Barbosa M, Gouveia L, Sepúlveda C, Bazaes J, Arbib Z (2018) Economics of microalgae production. In: Gonzalez-Fernandez C, Muñoz R (eds) Microalgae-Based Biofuels and Bioproducts. From Feedstock Cultivation to End-Products, Woodhead Publishing, pp 485–503Google Scholar
  2. Agboola JO, Teuling E, Wierenga PA, Gruppen H, Schrama JW (2019) Cell wall disruption: an effective strategy to improve the nutritive quality of microalgae in African catfish (Clarias gariepinus). Aquacult Nutr. CrossRefGoogle Scholar
  3. Ahmed F, Zhou W, Schenk PM (2015) Pavlova lutheri is a high-level producer of phytosterols. Algal Res 10:210–217CrossRefGoogle Scholar
  4. AOCS Official Method Ba 6a-05 (2005) Official Methods and Recommended Practices of the AOCS. The American Oil Chemists' Society, ChampaignGoogle Scholar
  5. Barone RSC, Sonoda DY, Lorenz EK, Cyrino JEP (2018) Digestibility and pricing of Chlorella sorokiniana meal for use in tilapia feeds. Scientia Agricola 75:184–190CrossRefGoogle Scholar
  6. Becker EW (2013a) Microalgae for human and animal nutrition. In: Richmond A, Hu Q (eds) Handbook of microalgal culture: applied phycology and biotechnology, 2nd edn. Blackwell Publishing Ltd., Oxford, pp 461–503CrossRefGoogle Scholar
  7. Becker EW (2013b) Microalgae for aquaculture: nutritional aspects. In: Richmond A, Hu Q (eds) Handbook of microalgal culture: applied phycology and biotechnology, 2nd edn. Blackwell Publishing Ltd., Oxford, pp 671–691CrossRefGoogle Scholar
  8. Ben-Amotz A, Torabene TG, Thomas WH (1985) Chemical profiles of selected species of microalgae with emphasis on lipids. J Phycol 21:72–81CrossRefGoogle Scholar
  9. Bou M, Berge GM, Baeverfjord G, Sigholt T, Østbye TK, Ruyter B (2017a) Low levels of very-long-chain n-3 PUFA in Atlantic salmon (Salmo salar) diet reduce fish robustness under challenging conditions in sea cages. J Nutr Sci 6:1–14CrossRefGoogle Scholar
  10. Bou M, Berge GM, Baeverfjord G, Sigholt T, Østbye TK, Romarheim OH, Hatlen B, Leeuwis R, Venegas C, Ruyter B (2017b) Requirements of n-3 very long-chain PUFA in Atlantic salmon (Salmo salar L): Effects of different dietary levels of EPA and DHA on fish performance and tissue composition and integrity. Br J Nutr 117:30–47PubMedCrossRefGoogle Scholar
  11. Bowzer J, Jackson C, Trushenski J (2016) Hybrid striped bass feeds based on fish oil, beef tallow, and eicosapentaenoic acid/docosahexaenoic acid supplements: insights regarding fish oil sparing and demand for n-3 long-chain polyunsaturated fatty acids. J Anim Sci 94:978–988PubMedCrossRefGoogle Scholar
  12. Brody T (1994) Protein. In: Brody T (ed) Nutritional biochemistry. Academic Press Inc, New York, pp 295–354Google Scholar
  13. Brown MR (1991) The amino-acid and sugar composition of 16 species of microalgae used for mariculture. J Exp Mar Biol Ecol 145:79–99CrossRefGoogle Scholar
  14. Brown MR, Garland CD, Jeffrey SW, Jameson ID, Leroi JM (1993) The gross and amino acid compositions of batch and semi-continuous cultures of Isochrysis sp. (clone T.ISO), Pavlova lutheri and Nannochloropsis oculata. J Appl Phycol 5:285–296CrossRefGoogle Scholar
  15. Carter CG, Bransden MP, Lewis TE, Nichols PD (2003) Potential of Thraustochytrids to partially replace fish oil in Atlantic salmon feeds. Mar Biotechnol 5:480–492PubMedCrossRefGoogle Scholar
  16. Cerezuela R, Fumanal M, Tapia-Paniagua ST, Meseguer J, Moriñigo MA, Esteban MA (2012) Histological alterations and microbial ecology of the intestine in gilthead seabream (Sparus aurata L.) fed dietary probiotics and microalgae. Cell Tissue Res 350:477–489PubMedCrossRefGoogle Scholar
  17. Chang YK, Wang SS (1999) Advances in extrusion technology: aquaculture/animal feeds and foods. Technomic Publishing Company Inc., Lancaster, 422 ppGoogle Scholar
  18. Cheng K, Bou M, Ruyter B, Pickova J, Ehtesham E, Du L, Venegas C, Moazzami AA (2018) Impact of reduced dietary levels of eicosapentaenoic acid and docosahexaenoic acid on the composition of skin membrane lipids in Atlantic salmon (Salmo salar L.). J Agric Food Chem. PubMedCrossRefGoogle Scholar
  19. Cherniack EP (2011) Polyphenols: planting the seeds of treatment for the metabolic syndrome. Nutrition 27:617–623PubMedCrossRefGoogle Scholar
  20. Coccia E, Varricchio E, Vito P, Turchini GM, Francis DS, Paolucci M (2014) Fatty acid-specific alterations in leptin, PPAR alpha, and CPT-1 gene expression in the rainbow trout. Lipids 49:1033–1046PubMedCrossRefGoogle Scholar
  21. Collins S (2014) Antinutritional factors in modelling plant-based rainbow trout diets, PhD Dissertation. University of Saskatchewan, Saskatoon 215 ppGoogle Scholar
  22. Colombo SM, Wacker A, Parrish CC, Kainz MJ, Arts MT (2017) A fundamental dichotomy in long-chain polyunsaturated fatty acid abundance between and within marine and terrestrial ecosystems. Env Rev 25:163–174CrossRefGoogle Scholar
  23. Colombo SM, Parrish CC, Wijekoon MPA (2018) Optimizing long chain-polyunsaturated fatty acid synthesis in salmonids by balancing dietary inputs. PLoS One 13:0205347Google Scholar
  24. Crampton EW, Harris LE (1969) Applied Animal Nutrition, 2nd edn. W.H. Freeman and Company, San Francisco 753 ppGoogle Scholar
  25. Crampton VO, Nanton DA, Ruohonen K, Skjervold PO, El-Mowafi A (2010) Demonstration of salmon farming as a net producer of fish protein and oil. Aquacult Nutr 16:437–446CrossRefGoogle Scholar
  26. Custódio L, Justo T, Silvestre L, Barradas A, Duarte CV, Pereira H, Barreira L, Rauter AP, Alberício F, Varela J (2012) Microalgae of different phyla display antioxidant, metal chelating and acetylcholinesterase inhibitory activities. Food Chem 131:134–140CrossRefGoogle Scholar
  27. de Roos B, Sneddon AA, Sprague M, Horgan GW, Brouwer IA (2017) The potential impact of compositional changes in farmed fish on its health-giving properties: Is it time to reconsider current dietary recommendations? Public Health Nutr. 20:2042–2049PubMedCrossRefGoogle Scholar
  28. Dickinson KE, Lalonde CGE, McGinn PJ (2019) Effects of spectral light quality and carbon dioxide on the physiology of Micractinium inermum: growth, photosynthesis and biochemical composition. J Appl Phycol.
  29. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356CrossRefGoogle Scholar
  30. Dunstan GA, Volkman JK, Barrett SM, Garland CD (1993) Changes in the lipid composition and maximisation of the polyunsaturated fatty acid content of three microalgae grown in mass culture. J Appl Phycol 5:71–83CrossRefGoogle Scholar
  31. Emery JA, Norambuena F, Trushenski J, Turchini GM (2016) Uncoupling EPA and DHA in fish nutrition: dietary demand is limited in Atlantic salmon and effectively met by DHA alone. Lipids 51:399–412PubMedCrossRefGoogle Scholar
  32. Environmental Protection Agency (2007) Test methods for evaluating solid waste physical/chemical methods, Methods EPA 6010C and 7471B.Google Scholar
  33. Espinosa EP, Allam B (2006) Comparative growth and survival of juvenile hard clams, Mercenaria mercenaria, fed commercially available diets. Zoo Biol 25:513–525CrossRefGoogle Scholar
  34. European Union (2002) Directive 2002/32/EC of the European parliament and of the council of May 2002 on undesirable substances in animal feed. Off J Eur Commun 2:10–21Google Scholar
  35. Feindel SC (2000) Optimization of hatchery culture of the sea scallop, Placopecten magellanicus (Gmelin, 1791): Dietary lipid quality and fatty acid requirements. Memorial University of Newfoundland, MSc Dissertation, 215 pGoogle Scholar
  36. Fernandes B, Dragone G, Abreu AP, Geada P, Teixeira J, Vicente A (2012) Starch determination in Chlorella vulgaris - a comparison between acid and enzymatic methods. J Appl Phycol 24:1203–1208CrossRefGoogle Scholar
  37. Francis G, Makkar HPS, Becker K (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199:197–227CrossRefGoogle Scholar
  38. Fry JP, Love DC, MacDonald GK, West PC, Engstrom PM, Nachman KE, Lawrence RS (2016) Environmental health impacts of feeding crops to farmed fish. Environ Int 91:201–214PubMedCrossRefGoogle Scholar
  39. Galloway AWE, Winder M (2015) Partitioning the relative importance of phylogeny and environmental conditions on phytoplankton fatty acids. PLoS One 10:e0130053PubMedPubMedCentralCrossRefGoogle Scholar
  40. Goh SH, Yusoff FM, Loh SP (2010) A comparison of the antioxidant properties and total phenolic content in a diatom, Chaetoceros sp. and a green microalga, Nannochloropsis sp. J Agric Sci 2:123–130Google Scholar
  41. Goiris K, Muylaert K, Fraeye I, Foubert I, Brabanter J, Cooman L (2012) Antioxidant potential of microalgae in relation to their phenolic and carotenoid content. J Appl Phycol 24:1477–1486CrossRefGoogle Scholar
  42. Gong Y, Guterres HADS, Huntley M, Sørensen M, Kiron V (2018) Digestibility of the defatted microalgae Nannochloropsis sp. and Desmodesmus sp. when fed to Atlantic salmon, Salmo salar. Aquacult Nutr 24:56–64CrossRefGoogle Scholar
  43. Gourtay C, Chabot D, Audet C, Le Delliou H, Quazuguel P, Claireaux G, Zambonino-Infante JL (2018) Will global warming affect the functional need for essential fatty acids in juvenile sea bass (Dicentrarchus labrax)? A first overview of the consequences of lower availability of nutritional fatty acids on growth performance. Mar Biol 165:143–115CrossRefGoogle Scholar
  44. Green JC (1980) The fine structure of Pavlova pinguis Green and a preliminary survey of the order Pavlovales (Prymnesiophyceae). Br Phycol J 15:151–191CrossRefGoogle Scholar
  45. Guedes AC, Meireles LA, Amaro HM, Malcata FX (2010) Changes in lipid class and fatty acid composition of cultures of Pavlova lutheri, in response to light intensity. J Am Oil Chem Soc 87:791–801CrossRefGoogle Scholar
  46. Guiry MD (2012) How many species of algae are there? J Phycol 48:1057–1063PubMedCrossRefGoogle Scholar
  47. Haas S, Bauer JL, Adakli A, Meyer S, Lippemeier S, Schwarz K, Schulz C (2016) Marine microalgae Pavlova virdis and Nannochloropsis sp. as n-3 PUFA source in diets for juvenile European sea bass (Dicentrarchus labrax L.). J Appl Phycol 28:1011–1021CrossRefGoogle Scholar
  48. Hajimahmoodi M, Faramarzi M, Mohammadi N, Soltani N, Oveisi M, Nafissi-Varcheh N (2010) Evaluation of antioxidant properties and total phenolic contents of some strains of microalgae. J Appl Phycol 22:43–50CrossRefGoogle Scholar
  49. Heinriksen RL, Meredith SC (1984) Amino acid analysis by reverse-phase high-performance liquid chromatography: precolumn derivatization with phenylisothiocyanate. Anal Biochem 136:65–74CrossRefGoogle Scholar
  50. Hertrampf JW, Piedad-Pascual F (2000) Handbook on ingredients for aquaculture feeds. Kluwer Academic Publishers, Boston 573 ppCrossRefGoogle Scholar
  51. Hites RA, Foran JA, Schwager SJ, Knuth BA, Hamilton MC, Carpenter DO (2004) Global assessment of polybrominated diphenyl ethers in farmed and wild salmon. Environ Sci Technol 38:4945–4949PubMedCrossRefGoogle Scholar
  52. Jamroz D, Orda J, Kamel C, Wiliczkiewicz A, Wertelecki T, Skorupinska J (2003) The influence of phytogenic extracts on performance, nutrient digestibility, carcass characteristics, and gut microbial status in broiler chickens. J Anim Feed Sci 12:583–596CrossRefGoogle Scholar
  53. Jimenez-Alvarez D, Giuffrida F, Vanrobaeys F, Golay PA, Cotting C, Lardeau A, Keely BJ (2008) High-throughput methods to assess lipophilic and hydrophilic antioxidant capacity of food extracts in vitro. J Agric Food Chem 56:3470–3477PubMedCrossRefGoogle Scholar
  54. Julkunen-Tiitto R (1985) Phenolic constituents in the leaves of Northern willows: methods for the analysis of certain phenolics. J Agric Food Chem 33:213–217CrossRefGoogle Scholar
  55. Kakade ML, Rackis JJ, McGhee JE, Puski G (1974) Determination of trypsin inhibitor activity of soy products: a collaborative analysis of an improved procedure. Cereal Chemistry 51:376–382Google Scholar
  56. Kato M, Hajiro-Nakanishi K, Sano H, Miyachi S (1995) Polyunsaturated fatty acids and betaine lipids from Pavlova lutheri. Plant Cell Physiol 36:1607–1611Google Scholar
  57. Khozin-Goldberg I, Leu S, Boussiba S (2016) Microalgae as a source for VLC-PUFA production. Subcell Biochem 86:471–510PubMedCrossRefGoogle Scholar
  58. Kiron V, Phromkunthong W, Huntley M, Archibald I, de Scheemaker G (2012) Marine microalgae from biorefinery as a potential feed protein source for Atlantic salmon, common carp and whiteleg shrimp. Aquacult Nutr 18:521–531CrossRefGoogle Scholar
  59. Kousoulaki K, Østbye TKK, Krasnov A, Torgersen JS, Mørkøre T et al (2015) Metabolism, health and fillet nutritional quality in Atlantic salmon (Salmo salar) fed diets containing n-3-rich microalgae. J Nutr Sci 4:e24PubMedPubMedCentralCrossRefGoogle Scholar
  60. Króliczewska B, Miśta D, Zawadzki W, Wypchlo A, Króliczewski J (2011) Effects of a skullcap root supplement on haematology, serum parameters and antioxidant enzymes in rabbits on a high-cholesterol diet. J Anim Physiol Anim Nutr 95:114–124CrossRefGoogle Scholar
  61. Lall SP (2010) The health benefits of farmed salmon: fish oil decontamination processing removes persistent organic pollutants. Br J Nutr 103:1391–1392PubMedCrossRefGoogle Scholar
  62. Lall SP, Anderson S (2005) Amino acid nutrition of salmonids: dietary requirements and bioavailability, In: Montero D, Basurco B, Nengas I, Alexis M, Izquierdo M (eds). Mediterranean fish nutrition, Cahiers Options Méditerranéennes 63:73–90Google Scholar
  63. Lang IK, Hodac L, Friedl T, Feussner I (2011) Fatty acid profiles and their distribution patterns in microalgae: a comprehensive analysis of more than 2000 strains from the SAG culture collection. BMC Plant Biol 11:124PubMedPubMedCentralCrossRefGoogle Scholar
  64. Lazard J (2017) Aquaculture systems facing climate change. Cah Agric 26.
  65. Letsche N, Lammers PJ (2014) Bulk density of bio-fuel by-products, Iowa State University Animal Industry Report, A.S. Leaflet R24592009 ( (accessed July 24, 2014).
  66. Li HB, Cheng KW, Wong CC, Fan KW, Chen F, Jiang Y (2007) Evaluation of antioxidant capacity and total phenolic content of different fractions of selected microalgae. Food Chem 102:771–776CrossRefGoogle Scholar
  67. Li-Beisson Y, Thelen JJ, Fedosejevs E, Harwood JL (2019) The lipid biochemistry of eukaryotic algae. Prog Lipid Res 74:31–68PubMedCrossRefGoogle Scholar
  68. Lourenço SO, Barbarino E, Lavín PL, Marquez UML, Aidar E (2004) Distribution of intracellular nitrogen in marine microalgae: calculation of new nitrogen-to-protein conversion factors. Eur J Phycol 39:17–32CrossRefGoogle Scholar
  69. MacDougall KM, McNichol J, McGinn PJ, O’Leary SJB, Melanson JE (2011) Triacylglycerol profiling of microalgae strains for biofuel feedstock by liquid chromatography-high-resolution mass spectrometry. Anal Bioanal Chem 401:2609–2616PubMedPubMedCentralCrossRefGoogle Scholar
  70. Malcorps W, Kok B, van’t Land M, Fritz M, van Doren D, Servin K, van der Heijden P, Palmer R, Auchterlonie NA, Rietkerk M, Santos MJ, Davies SJ (2019) The sustainability conundrum of fishmeal substitution by plant ingredients in shrimp feeds. Sustainability 11. CrossRefGoogle Scholar
  71. Martin-Creuzburg D, Merkel P (2016) Sterols of freshwater microalgae: potential implications for zooplankton nutrition. J Plankton Res 38:865–877CrossRefGoogle Scholar
  72. Martínez-Fernández E, Acosta-Salmón H, Rangel-Dávalos C (2004) Ingestion and digestion of 10 species of microalgae by winged pearl oyster Pteria sterna (Gould, 1851) larvae. Aquaculture 230:417–423CrossRefGoogle Scholar
  73. Martins DA, Custódio L, Barreira L, Pereira H, Ben-Hamadou R, Varela J, Abu-Salah KM (2013) Alternative sources of n-3 long-chain polyunsaturated fatty acids in marine microalgae. Mar Drugs 11:2259–2281PubMedPubMedCentralCrossRefGoogle Scholar
  74. Maynard LA, Loosli JK, Hintz HF, Warner RG (1979) Animal Nutrition, 7th edn. McGraw-Hill, New York 603 ppGoogle Scholar
  75. McGinn PJ, Dickinson KE, Park KC, Whitney CG, MacQuarrie SP, Black FJ, Frigon J, Guiot SR, O'Leary SJB (2012) Assessment of the bioenergy and bioremediation potentials of the microalga Scenedesmus sp. AMDD cultivated in municipal wastewater effluent in batch and continuous mode. Algal Res 1:155–165CrossRefGoogle Scholar
  76. Milke LM, Bricelj VM, Parrish CC (2004) Growth of postlarval sea scallops, Placopecten magellanicus, on microalgal diets, with emphasis on the nutritional role of lipids and fatty acids. Aquaculture 234:293–317CrossRefGoogle Scholar
  77. Milke LM, Bricelj VM, Parrish CC (2006) Comparison of early life history stages of the bay scallop, Argopecten irradians: effects of microalgal diets on growth and biochemical composition. Aquaculture 260:272–289CrossRefGoogle Scholar
  78. Milke LM, Bricelj VM, Parrish CC (2008) Biochemical characterization and nutritional value of three Pavlova spp. in unialgal and mixed diets with Chaetoceros muelleri for postlarval sea scallops, Placopecten magellanicus. Aquaculture 276:130–142CrossRefGoogle Scholar
  79. Montero D, Izquierdo M (2011) Welfare and health of fish fed vegetable oil. In: Turchini GM, Ng WK, Tocher DR (eds) Fish Oil replacement and alternative lipid sources in aquaculture feeds. CRC Press, Boca Raton, pp 439–485Google Scholar
  80. Moomaw W, Berzin I, Tzachor A (2017) Cutting out the middle fish: Marine microalgae as the next sustainable omega-3 fatty acids and protein source. Ind Biotechnol 13:234–243CrossRefGoogle Scholar
  81. National Center for Marine Algae and Microbiota (2018) CCMP459. (Accessed 2018 August 21).
  82. National Centre for Biotechnology Information (2019) Genome information by organism - algae.!/overview/algae (Accessed 2019 July 17).
  83. National Research Council (2011) Nutrient Requirements of Fish and Shrimp. National Academy Press, Washington 376 ppGoogle Scholar
  84. Norambuena F, Lewis M, Hamid NKA, Hermon K, Donald JA, Turchini GM (2013) Fish oil replacement in current aquaculture feed: is cholesterol a hidden treasure for fish nutrition? PLoS One 8:e0081705CrossRefGoogle Scholar
  85. Norambuena F, Hermon K, Skrzypczyk V, Emery JA, Sharon Y et al (2015) Algae in fish feed: Performances and fatty acid metabolism in juvenile Atlantic salmon. PLoS One 10:e0124042PubMedPubMedCentralCrossRefGoogle Scholar
  86. Oliveira MN, Freitas ALP, Carvalho AFU, Sampaio TMT, Farias DF, Teixeira DIA, Gouvia ST, Pereira JG, Sena M (2009) Nutritive and non-nutritive attributes of washed-up seaweeds from the coast of Ceará, Brazil. Food Chem 115:254–259CrossRefGoogle Scholar
  87. Oser BL (1951) Method for integrating essential amino acid content in the nutritional evaluation of protein. J Am Diet Assoc 27:396–402PubMedGoogle Scholar
  88. Pahlow M, van Oel PR, Mekonnen MM, Hoekstra AY (2015) Increasing pressure on freshwater resources due to terrestrial feed ingredients for aquaculture production. Sci Total Env 536:847–857CrossRefGoogle Scholar
  89. Parrish CC, Milke LM, Bricelj VM (2011) Characterization of 4α-methyl sterols in Pavlova spp. and postlarval sea scallops, Placopecten magellanicus. Aquaculture 311:261–262CrossRefGoogle Scholar
  90. Pernet F, Bricelj VM, Parrish CC (2005) Effect of varying dietary levels of ω6 polyunsaturated fatty acids during the early ontogeny of the sea scallop, Placopecten magellanicus. J Exp Mar Biol Ecol 327:115–133CrossRefGoogle Scholar
  91. Pernet F, Bricelj VM, Cartier S (2006) Lipid class dynamics during larval ontogeny of sea scallops, Placopecten magellanicus, in relation to metamorphic success and response to antibiotics. J Exp Mar Biol Ecol 329:265–280CrossRefGoogle Scholar
  92. Plourde M, Cunnane SC (2007) Extremely limited synthesis of long chain polyunsaturates in adults: Implications for their dietary essentiality and use as supplements. Appl Physiol Nutr Metab 32:619–634PubMedCrossRefGoogle Scholar
  93. Ponis E, Probert I, Véron B, Le Coz JR, Mathieu M, Robert R (2006) Nutritional value of six Pavlovophyceae for Crassostrea gigas and Pecten maximus larvae. Aquaculture 254:544–553CrossRefGoogle Scholar
  94. Reitan KI, Rainuzzo JR, Olsen Y (1994) Effect of nutrient limitation on fatty acid and lipid content of marine microalgae. J Phycol 30:972–979CrossRefGoogle Scholar
  95. Rombenso AN, Trushenski JT, Jirsa D, Drawbridge M (2015) Successful fish oil sparing in White seabass feeds using saturated fatty acid-rich soybean oil and 22:6n-3 (DHA) supplementation. Aquaculture 448:176–185CrossRefGoogle Scholar
  96. Sarker PK, Kapuscinski AR, Bae AY, Donaldson E, Sitek AJ, Fitzgerald DS, Edelson OF (2018) Towards sustainable aquafeeds: Evaluating substitution of fishmeal with lipid-extracted microalgal co-product (Nannochloropsis oculata) in diets of juvenile Nile tilapia (Oreochromis niloticus). PLoS One 13:e0201315PubMedPubMedCentralCrossRefGoogle Scholar
  97. Schüler LM, Schulze PSC, Pereira H, Barreria L, León R, Varela J (2017) Trends and strategies to enhance triacylgylcerols and high-value compounds in microalgae. Algal Res 25:263–273CrossRefGoogle Scholar
  98. Silveira RC, Silva FC, Gomes CHM, Ferreira JF, Melo CMR (2011) Larval settlement and spat recovery rates of the oyster Crassostrea brasiliana (Lamarck, 1819) using different systems to induce metamorphosis. Braz J Biol 71:557–562PubMedCrossRefGoogle Scholar
  99. Singh J, Dhar DW (2019) Overview of carbon capture technology: Microalgal biorefinery concept and state-of-the-art. Front Mar Sci 6:00029CrossRefGoogle Scholar
  100. Skrede A, Mydland LT, Ahlstrøm Ø, Reitan KI, Gislerød HR, Øverland M (2011) Evaluation of microalgae as sources of digestible nutrients for monogastric animals. J Anim Feed Sci 20:131–142CrossRefGoogle Scholar
  101. Sørensen M, Berge GM, Reitan KI, Ruyter B (2016) Microalga Phaeodactylum tricornutum in feed for Atlantic salmon (Salmo salar) - effect on nutrient digestibility, growth and utilization of feed. Aquaculture 460:116–123CrossRefGoogle Scholar
  102. Sprague M, Walton J, Campbell PJ, Strachan F, Dick JR, Bell JG (2015) Replacement of fish oil with a DHA-rich algal meal derived from Schizochytrium sp. on the fatty acid and persistent organic pollutant levels in diets and flesh of Atlantic salmon (Salmo salar, L.) post-smolts. Food Chem 185:413–421PubMedCrossRefGoogle Scholar
  103. Sprague M, Dick JR, Tocher DR (2016) Impact of sustainable feeds on omega-3 long-chain fatty acid levels in farmed Atlantic salmon, 2006-2015. Sci Rep 6:21892PubMedPubMedCentralCrossRefGoogle Scholar
  104. Sukenik A, Zmora O, Carmeli Y (1993) Biochemical quality of marine unicellular algae with special emphasis on lipid composition. II. Nannochloropsis sp. Aquaculture 117:313–326CrossRefGoogle Scholar
  105. Tacon AGJ, Metian M (2015) Feed matters: Satisfying the feed demand of aquaculture. Rev Fish Sci Aquacult 23:1–10CrossRefGoogle Scholar
  106. Teuling E, Schrama JW, Gruppen H, Wierenga PA (2017) Effect of cell wall characteristics on algae nutrient digestibility in Nile tilapia (Oreochromis niloticus) and African catfish (Clarus gariepinus). Aquaculture 479:490–500CrossRefGoogle Scholar
  107. Teuling E, Wierenga PA, Agboola JO, Gruppen H, Schrama JW (2019) Cell wall disruption increases bioavailability of Nannochloropsis gaditana nutrients for juvenile Nile tilapia (Oreochromis niloticus). Aquaculture 499:269–282CrossRefGoogle Scholar
  108. Thompson PA, Guo M, Harrison PJ, Whyte JNC (1992) Effects of variation in temperature. II. On the fatty acid composition of eight species of marine phytoplankton. J Phycol 28:488–497CrossRefGoogle Scholar
  109. Tibbetts SM (2018) The potential for ‘next-generation’, microalgae-based feed ingredients for salmonid aquaculture in context of the blue revolution. In: Jacob-Lopes E, Zepka LQ, Queiroz MI (eds) Microalgal biotechnology. InTech Open Publishing, Riejeka pp 151–175Google Scholar
  110. Tibbetts SM, Milley JE, Lall SP (2015a) Chemical composition and nutritional properties of freshwater and marine microalgal biomass cultured in photobioreactors. J Appl Phycol 27:1109–1119CrossRefGoogle Scholar
  111. Tibbetts SM, Whitney CG, MacPherson MJ, Bhatti S, Banskota AH, Stefanova R, McGinn PJ (2015b) Biochemical characterization of microalgal biomass from freshwater species isolated in Alberta, Canada for animal feed applications. Algal Res 11:435–447CrossRefGoogle Scholar
  112. Tibbetts SM, Melanson RJ, Park KC, Banskota AH, Stefanova R, McGinn PJ (2015c) Nutritional evaluation of whole and lipid-extracted biomass of the microalga Scenedesmus sp. AMDD isolated in Saskatchewan, Canada for animal feeds: proximate, amino acid, fatty acid, carotenoid and elemental composition. Curr Biotechnol 4:530–546CrossRefGoogle Scholar
  113. Tibbetts SM, MacPherson T, McGinn PJ, Fredeen AH (2016a) In vitro digestion of microalgal biomass from freshwater species isolated in Alberta, Canada for monogastric and ruminant animal feed applications. Algal Res 19:324–332CrossRefGoogle Scholar
  114. Tibbetts SM, Milley JE, Lall SP (2016b) Nutritional quality of some wild and cultivated seaweeds: Nutrient composition, total phenolic content and in vitro digestibility. J Appl Phycol 28:3575–3585CrossRefGoogle Scholar
  115. Tibbetts SM, Yasumaru F, Lemos D (2017a) In vitro prediction of digestible protein content of marine microalgae (Nannochloropsis granulata) meals for Pacific white shrimp (Litopenaeus vannamei) and rainbow trout (Oncorhynchus mykiss). Algal Res 21:76–80CrossRefGoogle Scholar
  116. Tibbetts SM, Mann J, Dumas A (2017b) Apparent digestibility of nutrients, energy, essential amino acids and fatty acids of juvenile Atlantic salmon (Salmo salar L.) diets containing whole-cell or cell-ruptured Chlorella vulgaris meals at five dietary inclusion levels. Aquaculture 481:25–39CrossRefGoogle Scholar
  117. Tocher DR, Bell JG, Dick JR, Crampton VO (2003) Effects of dietary vegetable oil on Atlantic salmon hepatocyte fatty acid desaturation and liver fatty acid composition. Lipids 38:723–732PubMedCrossRefGoogle Scholar
  118. Tocher DR, Betancor MB, Sprague M, Olsen RE, Napier JA (2019) Omega-3 long-chain polyunsaturated fatty acids, EPA and DHA: Bridging the gap between supply and demand. Nutrients 11. PubMedCentralCrossRefPubMedGoogle Scholar
  119. Turchini GM, Francis DS (2009) Fatty acid metabolism (desaturation, elongation and beta-oxidation) in rainbow trout fed fish oil- or linseed oil-based diets. Br J Nutr 102:69–81PubMedCrossRefGoogle Scholar
  120. Turchini GM, Torstensen BE, Ng WK (2009) Fish oil replacement in finfish nutrition. Rev Aquacult 1:10–57CrossRefGoogle Scholar
  121. Turchini GM, Ng WK, Tocher DR (2011) fish oil replacement and alternative lipid sources in aquaculture feeds. CRC Press, Boca Raton 533 ppGoogle Scholar
  122. Turchini GM, Trushenski J, Glencross BD (2018) Thoughts on the future of aquaculture nutrition: realigning perspectives to reflect contemporary issues related to the judicious use of marine resources in aquafeeds. N Am J Aquacult. CrossRefGoogle Scholar
  123. Van Parys A, Boyen F, Dewulf J, Haesebrouck F, Pasmans F (2010) The use of tannins to control Salmonella typhimurium infection in pigs. Zoonoses Public Health 57:423–428PubMedCrossRefGoogle Scholar
  124. Vernon B, Dauguet JC, Billard C (1998) Sterolic biomarkers in marine phytoplankton. II. Free and conjugated sterols of seven species used in mariculture. J Phycol 34:273–279CrossRefGoogle Scholar
  125. Vizcaíno AJ, López G, Sáez MI, Jiménez JA, Barros A, Hidalgo L, Camacho-Rodríguez J, Martínez TF, Cerón-García MC, Alarcón FJ (2014) Effects of the microalga Scenedesmus almeriensis as fishmeal alternative in diets for gilthead sea bream, Sparus auratus, juveniles. Aquaculture 431:34–43CrossRefGoogle Scholar
  126. Volkman JK, Dunstan GA, Jeffrey SW, Kearney PS (1991) Fatty acids from microalgae of the genus Pavlova. Phytochemistry 30:1855–1859CrossRefGoogle Scholar
  127. Volkman JK, Barrett SM, Dunstan GA, Jeffrey SW (1992) C30-C32 alkyl diols and unsaturated alcohols in microalgae of the class Eustigmatophyceae. Org Geochem 18:131–138CrossRefGoogle Scholar
  128. White JA, Hart RJ, Fry JC (1986) An evaluation of the Waters Pico-Tag system for the amino-acid analysis of food materials. J Clin Lab Auto 8:170–177Google Scholar
  129. Yuan YV (2008) Marine algal constituents. In: Barrow C, Shahidi F (eds) Marine nutraceuticals and functional foods. CRC Press Inc., Boca Raton, pp 259–296Google Scholar
  130. Zhang C (2013) Determination of the digestibility of a whole-cell DHA-rich algal product and its effect on the lipid composition of rainbow trout and Atlantic salmon. MSc Dissertation, University of Saskatchewan 87 ppGoogle Scholar

Copyright information

© Crown 2019

Authors and Affiliations

  1. 1.National Research Council of CanadaAquatic and Crop Resource Development Research CentreHalifaxCanada

Personalised recommendations