In vitro prediction of digestible protein content of marine microalgae (Nannochloropsis granulata) meals for Pacific white shrimp (Litopenaeus vannamei) and rainbow trout (Oncorhynchus mykiss)

Tibbetts, Sean M.; Yasumaru, Fanny; Lemos, Daniel

doi:10.1016/j.algal.2016.11.010

Cited by 64Aquaculture Nutrition and GrowthAlgal biology and biofuel productionAquaculture disease management and microbiota

In vitro prediction of digestible protein content of marine microalgae (Nannochloropsis granulata) meals for Pacific white shrimp (Litopenaeus vannamei) and rainbow trout (Oncorhynchus mykiss)

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Tibbetts, Sean M., Yasumaru, Fanny, Lemos, Daniel·2017·Algal Research

DOI 10.1016/j.algal.2016.11.010

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Due to variations in eating patterns and digestive physiologies among various fish species, the nutritional benefits of a microalga in one target animal species do not generally guarantee the same in others.
“Due to variations in eating patterns and digestive physiologies among various fish species, the nutritional benefits of a microalga in one target animal species do not generally guarantee the same in others.”
From Potential of microalgae as a sustainable feed ingredient for aquaculture (2021) · cites this paper as Tibbetts et al., 2017

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Nutrient Requirements of Fish and Shrimp
National Research Council (2011) · National Academies Press eBooks · doi:10.17226/13039 · Cited by 3,229 · see citing works
The State of World Fisheries and Aquaculture 2026
Alder, J., Ryder, J., Friedman, K., Beveridge, M., Barange, M., Taconet, M., Camilleri, M., Franz, N., Barros, P., Mannini, P., et al. (2013) · FAO eBooks · doi:10.4060/cd8357en · Cited by 2,094 · see citing works
Feeding aquaculture in an era of finite resources
Naylor, R. L., Hardy, R. W., Bureau, D., Chiu, A., Elliott, M., Farrell, A. P., Forster, I. P., Gatlin, D. M., Goldburg, R. J., Hua, K., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0905235106 · Cited by 1,532 · see citing works
Ultrastructure and Composition of the Nannochloropsis gaditana Cell Wall
Scholz, M. J., Weiss, T. L., Jinkerson, R. E., Jia, J., Roth, R. A., Goodenough, U. W., Posewitz, M. C., & Gerken, H. G. (2014) · Eukaryotic Cell · doi:10.1128/ec.00183-14 · Cited by 439 · see citing works
Chemical composition and nutritional properties of freshwater and marine microalgal biomass cultured in photobioreactors
Tibbetts, S. M., Milley, J. E., & Lall, S. P. (2014) · Journal of Applied Phycology · doi:10.1007/s10811-014-0428-x · Cited by 423 · see citing works
Self-citation
Supercritical Fluid Extraction of Nutraceuticals and Bioactive Compounds
Martínez, J. L. (2007) · CRC Press eBooks · doi:10.1201/9781420006513 · Cited by 296 · see citing works
Influence of microalgae cell wall characteristics on protein extractability and determination of nitrogen-to-protein conversion factors
Safi, C., Charton, M., Pignolet, O., Silvestre, F., Vaca-Garcia, C., & Pontalier, P.-Y. (2013) · Journal of Applied Phycology · doi:10.1007/s10811-012-9886-1 · Cited by 283 · see citing works
Integration of microalgae cultivation with industrial waste remediation for biofuel and bioenergy production: opportunities and limitations
McGinn, P. J., Dickinson, K. E., Bhatti, S., Frigon, J.-C., Guiot, S. R., & O’Leary, S. J. B. (2011) · Photosynthesis Research · doi:10.1007/s11120-011-9638-0 · Cited by 230 · see citing works
Effects of the microalga Scenedesmus almeriensis as fishmeal alternative in diets for gilthead sea bream, Sparus aurata, juveniles
Vizcaíno, A. J., López, G., Sáez, M. I., Jiménez, J. A., Barros, A. M., Hidalgo, L., Camacho-Rodríguez, J., Martínez, T. F., Cerón-García, M. C., & Alarcón, F. J. (2014) · Aquaculture · doi:10.1016/j.aquaculture.2014.05.010 · Cited by 214 · see citing works
Binders in fish feeds
Storebakken, T. (1985) · Aquaculture · doi:10.1016/0044-8486(85)90004-3 · Cited by 195 · see citing works
Optimizing protein isolation from defatted and non-defatted Nannochloropsis microalgae biomass
Gerde, J. A., Wang, T., Yao, L., Jung, S., Johnson, L. A., & Lamsal, B. P. (2013) · Algal Research · doi:10.1016/j.algal.2013.02.001 · Cited by 165 · see citing works
Growth performance and quality traits of European sea bass (D. labrax) fed diets including increasing levels of freeze-dried Isochrysis sp. (T-ISO) biomass as a source of protein and n-3 long chain PUFA in partial substitution of fish derivatives
Tibaldi, E., Zittelli, G. C., Parisi, G., Bruno, M., Giorgi, G., Tulli, F., Venturini, S., Tredici, M. R., & Poli, B. M. (2015) · Aquaculture · doi:10.1016/j.aquaculture.2015.02.002 · Cited by 161 · see citing works
Vitamin E (α-tocopherol) production by the marine microalgae Nannochloropsis oculata (Eustigmatophyceae) in nitrogen limitation
Durmaz, Y. (2007) · Aquaculture · doi:10.1016/j.aquaculture.2007.07.213 · Cited by 160 · see citing works
Supercritical fluid extraction of valuable compounds from microalgal biomass
Yen, H., Yang, S.-C., Chen, C.-H., Jesisca, & Chang, J. (2014) · Bioresource Technology · doi:10.1016/j.biortech.2014.10.030 · Cited by 155 · see citing works
Triacylglycerol profiling of microalgae strains for biofuel feedstock by liquid chromatography–high-resolution mass spectrometry
MacDougall, K. M., McNichol, J. C., McGinn, P. J., O’Leary, S. J. B., & Melanson, J. E. (2011) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-011-5376-6 · Cited by 143 · see citing works
Screening microalgae strains for their productivity in methane following anaerobic digestion
Frigon, J., Lebrun, F. M., Abdou, R. H., McGinn, P. J., O’Leary, S. J. B., & Guiot, S. R. (2013) · Applied Energy · doi:10.1016/j.apenergy.2013.02.051 · Cited by 131 · see citing works
Potential and Limitation of a New Defatted Diatom Microalgal Biomass in Replacing Soybean Meal and Corn in Diets for Broiler Chickens
Austic, R. E., Mustafa, A., Jung, B., Gatrell, S. K., & Lei, X. G. (2013) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf401957z · Cited by 110 · see citing works
Evaluation of microalgae as sources of digestible nutrients for monogastric animals
Skrede, A., Mydland, L., Ahlstrøm, Ø., Reitan, K., Gislerød, H., & Øverland, M. (2011) · Journal of Animal and Feed Sciences · doi:10.22358/jafs/66164/2011 · Cited by 104 · see citing works
NONRUMINANT NUTRITION SYMPOSIUM: Potential of defatted microalgae from the biofuel industry as an ingredient to replace corn and soybean meal in swine and poultry diets12
Gatrell, S., Lum, K., Kim, J., & Lei, X. G. (2014) · Journal of Animal Science · doi:10.2527/jas.2013-7250 · Cited by 102 · see citing works
Heat treatment increases the protein bioaccessibility in the red seaweed dulse (Palmaria palmata), but not in the brown seaweed winged kelp (Alaria esculenta)
Maehre, H. K., Edvinsen, G. K., Eilertsen, K.-E., & Elvevoll, E. O. (2016) · Journal of Applied Phycology · doi:10.1007/s10811-015-0587-4 · Cited by 102 · see citing works
Evaluation of whole and lipid-extracted algae meals in the diets of juvenile red drum (Sciaenops ocellatus)
Patterson, D., & Gatlin, D. M. (2013) · Aquaculture · doi:10.1016/j.aquaculture.2013.08.033 · Cited by 95 · see citing works
Effect of Dietary Marine Microalgae (Schizochytrium) Powder on Egg Production, Blood Lipid Profiles, Egg Quality, and Fatty Acid Composition of Egg Yolk in Layers
Park, J. H., Upadhaya, S. D., & Kim, I. H. (2015) · Asian-Australasian Journal of Animal Sciences · doi:10.5713/ajas.14.0463 · Cited by 91 · see citing works
Marine microalgae Pavlova viridis and Nannochloropsis sp. as n-3 PUFA source in diets for juvenile European sea bass (Dicentrarchus labrax L.)
Haas, S., Bauer, J. L., Adaklı, A., Meyer, S., Lippemeier, S., Schwarz, K., & Schulz, C. (2015) · Journal of Applied Phycology · doi:10.1007/s10811-015-0622-5 · Cited by 90 · see citing works
Prediction of apparent protein digestibility of ingredients and diets by in vitro pH-stat degree of protein hydrolysis with species-specific enzymes for juvenile Pacific white shrimp Litopenaeus vannamei
Lemos, D., Lawrence, A. L., & Siccardi, A. J. (2009) · Aquaculture · doi:10.1016/j.aquaculture.2009.06.011 · Cited by 87 · see citing works
Self-citation
A Comparison of the Antioxidant Properties and Total Phenolic Content in a Diatom, Chaetoceros sp. and a Green Microalga, Nannochloropsis sp.
Goh, S. H., Yusoff, F. M., & Loh, S. P. (2010) · Journal of Agricultural Science · doi:10.5539/jas.v2n3p123 · Cited by 85 · see citing works
Species specific in vitro protein digestion (pH-stat) for fish: method development and application for juvenile rainbow trout (Oncorhynchus mykiss), cobia (Rachycentron canadum), and Nile tilapia (Oreochromis niloticus)
Yasumaru, F., & Lemos, D. (2014) · Aquaculture · doi:10.1016/j.aquaculture.2014.01.012 · Cited by 70 · see citing works
Self-citation
Biochemical composition and amino acid profiles of Nannochloropsis granulata algal biomass before and after supercritical fluid CO2 extraction at two processing temperatures
Tibbetts, S. M., Bjornsson, W. J., & McGinn, P. J. (2015) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2015.04.006 · Cited by 67 · see citing works
Self-citation
High pressure homogenization of Nannochloropsis oculata for the extraction of intracellular components: Effect of process conditions and culture age
Shene, C., Monsalve, M. T., Vergara, D., Lienqueo, M. E., & Rubilar, M. (2015) · European Journal of Lipid Science and Technology · doi:10.1002/ejlt.201500011 · Cited by 66 · see citing works
Ultrastructure, pigment composition, and 18S rRNA gene sequence for Nannochloropsis granulata sp. nov. (Monodopsidaceae, Eustigmatophyceae), a marine ultraplankter isolated from the Skagerrak, northeast Atlantic Ocean
Karlson, B., Potter, D., Kuylenstierna, M., et al. (1996) · Phycologia · doi:10.2216/i0031-8884-35-3-253.1 · Cited by 62 · see citing works
Mono- and digalactosyldiacylglycerols: potent nitric oxide inhibitors from the marine microalga Nannochloropsis granulata
BANSKOTA, A. H., Stefanova, R., Gallant, P., & McGinn, P. J. (2012) · Journal of Applied Phycology · doi:10.1007/s10811-012-9869-2 · Cited by 61 · see citing works
Some methods for processing of single‐cell protein
Hedenskog, G., & Mogren, H. (1973) · Biotechnology and Bioengineering · doi:10.1002/bit.260150110 · Cited by 61 · see citing works
New diacylglyceryltrimethylhomoserines from the marine microalga Nannochloropsis granulata and their nitric oxide inhibitory activity
BANSKOTA, A. H., Stefanova, R., Sperker, S. A., & McGinn, P. J. (2013) · Journal of Applied Phycology · doi:10.1007/s10811-012-9967-1 · Cited by 51 · see citing works
Individual-Based Model of Young-of-the-Year Striped Bass Population Dynamics. II. Factors Affecting Recruitment in the Potomac River, Maryland
Cowan, J. H., Rose, K. A., Rutherford, E. S., & Houde, E. D. (1993) · Transactions of the American Fisheries Society · doi:10.1577/1548-8659(1993)122 · Cited by 44 · see citing works
Pilot-scale supercritical carbon dioxide extractions for the recovery of triacylglycerols from microalgae: a practical tool for algal biofuels research
Bjornsson, W. J., MacDougall, K. M., Melanson, J. E., O’Leary, S. J. B., & McGinn, P. J. (2011) · Journal of Applied Phycology · doi:10.1007/s10811-011-9756-2 · Cited by 43 · see citing works
Protein Fractions with Techno-Functional and Antioxidant Properties from Nannochloropsis gaditana Microalgal Biomass
Medina, C., Rubilar, M., Shene, C., Torres, S., & Verdugo, M. (2015) · Journal of Biobased Materials and Bioenergy · doi:10.1166/jbmb.2015.1534 · Cited by 42 · see citing works
In vitrodigestibility of flaxseed ( L inum usitatissimumL.) protein: effect of seed mucilage, oil and thermal processing
Marambe, H. K., Shand, P. J., & Wanasundara, J. P. D. (2012) · International Journal of Food Science & Technology · doi:10.1111/ijfs.12008 · Cited by 41 · see citing works
Functional Foods Enriched with Marine Microalga Nannochloropsis oculata as a Source of ω-3 Fatty Acids
Srinivasan, B., Krishnan, K. R., Babu, P. A. S., Sivarajan, M., & Sukumar, M. (2014) · DOAJ (DOAJ: Directory of Open Access Journals) · Cited by 35 · see citing works
Bioaccessibility of Carotenoids and Tocopherols in Marine Microalgae, Nannochloropsis sp. and Chaetoceros sp.
Goh, L. P., Loh, S. P., Fatimah, M. Y., & Perumal, K. (2009) · PubMed · Cited by 28 · see citing works
Practical equivalence of laboratory and field measurements of gut passage time in two penaeid shrimp species
BESERES, J. J., Lawrence, A. L., & Feller, R. J. (2006) · Marine Ecology Progress Series · doi:10.3354/meps309221 · Cited by 21 · see citing works
DRY BIOMASS OF FRESH WATER ALGAE OF CHLORELLA GENUS IN THE COMBINED FORAGES FOR LAYING HENS
Grigorova (2006) · University of Zagreb University Computing Centre (SRCE) · doi:10.5513/jcea.v6i4.345 · Cited by 12 · see citing works
Effects of Inorganic Sulfur on Potassium Nitrate Utilization by Lambs2
Sokołowski, J. H., Hatfield, E. E., & Garrigus, U. S. (1969) · Journal of Animal Science · doi:10.2527/jas1969.283391x · Cited by 10 · see citing works
Functional anatomy of penaeid shrimp
Martin, G. G., & Hose, J. E. (2012) · Nottingham University Press eBooks · doi:10.7313/upo9781907284939.004 · Cited by 1 · see citing works

Flagged first, then by citations

Research works printed but not linked: 6

Taylor, L.T. (1996) Applications of analytical supercritical fluid extraction. In: Taylor, L.T. (Ed.), Supercritical Fluid Extraction, Techniques in Analytical Chemistry. John Wiley and Sons, Inc., pp. 127- 166.
Mendes, R.L. (2008) Supercritical fluid extraction of active compounds from algae. In: Martínez, J.L. (Ed.), Supercritical Fluid Extraction of Nutraceuticals and Bioactive Compounds. CRC Press, Taylor and Francis Group, pp. 189-213.
Adler-Nissen, J. (1986) Enzymatic hydrolysis of food proteins. Elsevier, New York, NY. 427 p.
Cavonius, L.R. (2016) Fractionation of lipids and proteins from the microalga Nannochloropsis oculata. pH-shift process characterization and in vitro accessibility. PhD Thesis, Chalmers University of Technology, Gothenburg, Sweden, 67 p.
Bastos, D.M., Monaro, E., Siguemoto, E., Séfora, M. (2012) Maillard reaction products in processed food: pros and cons. In: Valdez, B. (Ed.), Food Industrial Processes -Methods and Equipment. InTech Open Science, Rijeka, Croatia, pp. 281-300.
McDonald, P., Edwards, R.A., Greenhalgh, J.F.D., Morgan, C.A., Sinclair, L.A. (2010) Animal Nutrition, seventh edition. Prentice Hall, New York, 692 p.

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The potential of microalgae in biodiesel production
Chen, J., Li, J., Dong, W., Zhang, X., Tyagi, R. D., Drogui, P., & Surampalli, R. Y. (2018) · Renewable and Sustainable Energy Reviews · doi:10.1016/j.rser.2018.03.073 · Cited by 330 · see citing works
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Glencross, B. D., Huyben, D., & Schrama, J. W. (2020) · Fishes · doi:10.3390/fishes5030022 · Cited by 203 · see citing works
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Singh, S., Verma, D. K., Thakur, M., Tripathy, S., Patel, A. R., Shah, N., Utama, G. L., Srivastav, P. P., Benavente-Valdés, J. R., Chávez-González, M. L., et al. (2021) · Food Research International · doi:10.1016/j.foodres.2021.110746 · Cited by 98 · see citing works

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Li, L., Ren, W., Dong, S., et al. (2017) · Aquaculture Research · doi:10.1111/are.13551 · Cited by 23 · see citing works
Effects of Diet and Water Source on the Nursery Production of Pacific White Shrimp Litopenaeus vannamei
Otoshi, C. A., Montgomery, A. D., Look, A. M., et al. (2001) · Journal of the World Aquaculture Society · doi:10.1111/j.1749-7345.2001.tb01102.x · Cited by 46 · see citing works
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Aprilia, T., Agustama, Y., Rakhmawati, R., et al. (2023) · DEPIK · doi:10.13170/depik.12.3.30546 · Cited by 1 · see citing works
Feeding of effects on metabolism of white Pacific shrimp(Litopenaeus vannamei)
Song-qing, L., & Xiao-tao, L. (2006) · Redai haiyang xuebao · Cited by 3 · see citing works
Seleksi Bakteri Probiotik dari Saluran Pencernaan untuk Meningkatkan Kinerja Pertumbuhan Udang Vaname Litopenaeus vannamei
Nopitawati, T. (2010) · IPB Scientific Repository (Bogor Agricultural University.) · Cited by 5 · see citing works

Authors: Tibbetts, S. M., Yasumaru, F., & Lemos, D.
Affiliations: National Research Council Canada (CA)
Universidade de São Paulo (BR)
Corresponding author: Tibbetts, Sean M.
ORCID: Tibbetts, Sean M.
Yasumaru, Fanny
Lemos, Daniel
Venue: Algal Research
Publisher: Elsevier BV
Published: 2017-01
Volume: 21
Pages: 76-80
ISSN: 2211-9264 (ISSN-L)
DOI: 10.1016/j.algal.2016.11.010
OpenAlex: W2549653310
Cited by: 64
References: 42
Citations by year: 2026: 5 · 2025: 8 · 2024: 8 · 2023: 6 · 2022: 10 · 2021: 11 · 2020: 5 · 2019: 6 · 2018: 4 · 2017: 1
FWCI: 4.63
Type: journal article
Language: en
Open access: green
www.sciencedirect.com
Licence: other-oa
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Algal Research (publishedVersion)
LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (publishedVersion, other-oa)
ResearchOnline at James Cook University (James Cook University) (submittedVersion)
NPARC (submittedVersion)
Funders: National Bioproducts Program
Natural Resources Canada
National Research Council Canada
Materials Transfer Agreement between NRC and LAM
Topics: Life Sciences › Agricultural and Biological Sciences › Aquatic Science › Aquaculture Nutrition and Growth
Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Algal biology and biofuel production
Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
Keywords: digestible protein, Litopenaeus vannamei, rainbow trout, apparent digestibility coefficients, supercritical fluid extraction, fish feed ingredients, degree of hydrolysis

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In vitro prediction of digestible protein content of marine microalgae (Nannochloropsis granulata) meals for Pacific white shrimp (Litopenaeus vannamei) and rainbow trout (Oncorhynchus mykiss)

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