Effect of 4 microalgal diets on the proximal composition, chlorophyll concentration, and total carotenoid content in Artemia franciscana
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Microalgae are the primary source of food for Artemia franciscana. In turn, Artemia serve as live food for various species in culture. The chemical composition of Artemia is of great importance because it affects the nutritional quality of the organisms produced in aquaculture systems. For this reason, the present study aimed to characterize the nutritional value, proximal composition, concentration of chlorophyll a and b, and total carotenoid content in the microalgae Thalassiosira weissflogii, Chaetoceros muelleri, Tetraselmis suecica, and Nannochloropsis sp., which were used to feed juvenile A. franciscana for 6 h. Artemia juveniles fed with these microalgae species exhibited higher concentrations of proteins, carbohydrates, lipids, chlorophyll a and b, and total carotenoids than those in the control. The organisms fed with Tetraselmis suecica presented the highest content of chlorophyll b, while those fed with Thalassiosira weissflogii and Chaetoceros muelleri showed the highest values of total carotenoids and chlorophyll a.
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Abdollahi Y, Ahmadifard N, Agh N, Rahmanifarah K, Amin-Hejazi M. 2019. β-Carotene-enriched Artemia as a natural carotenoid improved skin pigmentation and enhanced the mucus immune responses of platyfish Xiphophorus maculatus. Aquac Int. 27(6):1847-1858. https://doi.org/10.1007/s10499-019-00437-8 DOI: https://doi.org/10.1007/s10499-019-00437-8
Abiusi F, Sampietro G, Marturano G, Biondi N, Rodolfi L, D’Ottavio M, Tredici MR. 2013. Growth, photosynthetic efficiency, and biochemical composition of Tetraselmis suecica F&M-M33 grown with LEDs of different colors. Biotechnol Bioeng. 111(5):956-964. https://doi.org/10.1002/bit.25014 DOI: https://doi.org/10.1002/bit.25014
Ahmed F, Fanning K, Netzel M, Turner W, Li Y, Schenk PM. 2014. Profiling of carotenoids and antioxidant capacity of microalgae from subtropical coastal and brackish waters. Food Chem. 165:300-306. http://dx.doi.org/10.1016/j.foodchem.2014.05.107 DOI: https://doi.org/10.1016/j.foodchem.2014.05.107
Aranda-Burgos JA, da Costa F, Nóvoa S, Ojea J, Martínez-Patiño D. 2014. Effects of microalgal diet on growth, survival, biochemical and fatty acid composition of Ruditapes decussatus larvae. Aquaculture. 420–421:38-48. http://doi.org/10.1016/j.aquaculture.2013.10.032 DOI: https://doi.org/10.1016/j.aquaculture.2013.10.032
Azimirad M, Meshkini S, Ahmadifard N, Hoseinifar SH. 2016. The effects of feeding with synbiotic (Pediococcus acidilactici and fructooligosaccharide) enriched adult Artemia on skin mucus immune responses, stress resistance, intestinal microbiota and performance of angelfish (Pterophyllum scalare). Fish Shellfish Immunol. 54:516-522. https://doi.org/10.1016/j.fsi.2016.05.001 DOI: https://doi.org/10.1016/j.fsi.2016.05.001
Bhattacharjya R, Marella TK, Tiwari A, Saxena A, Singh PK, Mishra B. 2020. Bioprospecting of marine diatoms Thalassiosira, Skeletonema and Chaetoceros for lipids and other value-added products. Bioresour Technol. 318:124073. https://doi.org/10.1016/j.biortech.2020.124073 DOI: https://doi.org/10.1016/j.biortech.2020.124073
Bhuvaneshwari M, Thiagarajan V, Nemade P, Chandrasekaran N, Mukherjee A. 2018. Toxicity and trophic transfer of P25 TiO2 NPs from Dunaliella salina to Artemia salina: effect of dietary and waterborne exposure. Environ Res. 160:39-46. https://doi.org/10.1016/j.envres.2017.09.022 DOI: https://doi.org/10.1016/j.envres.2017.09.022
Bligh EG, Dyer WJ. 1959. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 37(8):911-917. https://doi.org/10.1139/o59-099 DOI: https://doi.org/10.1139/o59-099
Carbajal-López A. 2008. Producción en masa del rotífero Brachionus plicatilis alimentado con 4 diferentes microalgas, para su uso como alimento vivo de larvas de peces marinos. [Mass production of Brachionus plicatilis rotifer fed with 4 different microalgae, for use as live food for marine fish larvae] [BSc thesis]. [Guadalajara (Jalisco, Mexico)]: Universidad de Guadalajara. 48 p.
Chaisutyakorn P, Praiboon J, Kaewsuralikhit C. 2018. The effect of temperature on growth and lipid and fatty acid composition on marine microalgae used for biodiesel production. J Appl Phycol. 30:37-45. https://doi.org/10.1007/s10811-017-1186-3 DOI: https://doi.org/10.1007/s10811-017-1186-3
Chakraborty RD, Chakraborty K, Radhakrishnan EV. 2007. Variation in fatty acid composition of Artemia salina nauplii enriched with microalgae and baker’s yeast for use in larviculture. J Agric Food Chem. 55(10):4043-4051. https://doi.org/10.1021/jf063654l DOI: https://doi.org/10.1021/jf063654l
Cheban L, Khudyi O, Prusińska M, Duda A, Khuda L, Wiszniewski G, Kushniryk O, Kapusta A. 2020. Survival, proximate composition, and proteolytic activity of Artemia salina bioencapsulated with different algal monocultures. Fish Aquat Life. 28(4):205-215. https://doi.org/10.2478/aopf-2020-0025 DOI: https://doi.org/10.2478/aopf-2020-0025
De la Vega-Naranjo M. 2014. Aislamiento, caracterización y manipulación genética de microalgas marinas para la producción de compuestos de alto valor añadido [Isolation, characterization, and genetic manipulation of marine microalgae for the production of high added value compounds] [dissertation]. [Spain]: Universidad de Huelva. 204 p.
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. 1956. Colorimetric method for the determination of sugars and related substances. Anal Chem. 28(3):350-356. https://doi.org/10.1021/ac60111a017 DOI: https://doi.org/10.1021/ac60111a017
Fábregas J, Otero A, Domínguez A, Patiño M. 2001. Growth rate of the microalga Tetraselmis suecica changes the biochemical composition of Artemia species. Mar Biotechnol. 3(3):256-263. https://doi.org/10.1007/s101260000074 DOI: https://doi.org/10.1007/s101260000074
Franz AK, Danielewicz MA, Wong DM, Anderson LA, Boothe JR. 2013. Phenotypic screening with oleaginous microalgae reveals modulators of lipid productivity. ACS Chem Biol. 8:1053-1062. https://doi.org/10.1021/cb300573r DOI: https://doi.org/10.1021/cb300573r
García N, López-Elías JA, Miranda A, Martínez-Porchas M, Huerta N, García A. 2012. Effect of salinity on growth and chemical composition of the diatom Thalassiosira weissflogii at three culture phases. Lat Am J Aquat Res. 40(2):435-440. http://doi.org/10.3856/vol40-issue2-fulltext-18 DOI: https://doi.org/10.3856/vol40-issue2-fulltext-18
Gerken HG, Donohoe B, Knoshaug EP. 2013. Enzymatic cell wall degradation of Chlorella vulgaris and other microalgae for biofuels production. Planta: 237:239-253. https://doi.org/10.1007/s00425-012-1765-0 DOI: https://doi.org/10.1007/s00425-012-1765-0
Goiris K, Muylaert K, Fraeye I, Foubert I, de Brabanter J, de Cooman L. 2012. Antioxidant potential of microalgae in relation to their phenolic and carotenoid content. J Appl Phycol. 24:1477-1486. https://doi.org/10.1007/s10811-012-9804-6 DOI: https://doi.org/10.1007/s10811-012-9804-6
Gómez-Loredo A, Benavides J, Rito-Palomares M. 2016. Growth kinetics and fucoxanthin production of Phaeodactylum tricornutum and Isochrysis galbana cultures at different light and agitation conditions. J Appl Phycol. 28:849-860. https://doi.org/10.1007/s10811-015-0635-0 DOI: https://doi.org/10.1007/s10811-015-0635-0
Guillard RRL, Ryther JH. 1962. Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt and Detonula confervacea (Cleve). Rev Microbiol. 8:229-325. https://doi.org/10.1139/m62-029 DOI: https://doi.org/10.1139/m62-029
Hamed I. 2016. The evolution and versatility of microalgal biotechnology: a review. Compr Rev Food Sci Food Saf. 15(6):1104-1123. https://doi.org/10.1111/1541-4337.12227 DOI: https://doi.org/10.1111/1541-4337.12227
Hindersin S, Leupold M, Kerner M, Hanelt D. 2014. Key parameters for outdoor biomass production of Scenedesmus obliquus in solar tracked photobioreactors. J Appl Phycol. 26:2315-2325. https://doi.org/10.1007/s10811-014-0261-2 DOI: https://doi.org/10.1007/s10811-014-0261-2
Jeffrey SW, Wright SW. 2005. Photosynthetic pigments in marine microalgae: insights from cultures and the sea. In: Subba-Rao DV (ed.), Algal Cultures, Analogues of Blooms and Applications. New Hampshire (USA): Science Publishers. p. 33-90.
Ju ZY, Forster IP, Dominy WG. 2009. Effects of supplementing two species of marine algae or their fractions to a formulated diet on growth, survival and composition of shrimp (Litopenaeus vannamei). Aquaculture. 292:237-243. https://doi.org/10.1016/j.aquaculture.2009.04.040 DOI: https://doi.org/10.1016/j.aquaculture.2009.04.040
Léger P, Bengston DA, Simpson KL, Sorgeloos P. 1986. The use and nutritional value of Artemia as a food source. Oceanogr Mar Biol Annu Rev. 24:521-623.
Lichtenthaler HK, Wellburn AR. 1983. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans. 11(5):591-592. https://doi.org/10.1042/bst0110591 DOI: https://doi.org/10.1042/bst0110591
Long M, Tallec K, Soudant P, Le Grand F, Donval A, Lambert C, Sarthou G, Jolley DF, Hégaret H. 2018. Allelochemicals from Alexandrium minutum induce rapid inhibition of metabolism and modify the membranes from Chaetoceros muelleri. Algal Res. 35:508-518. https://doi.org/10.1016/j.algal.2018.09.023 DOI: https://doi.org/10.1016/j.algal.2018.09.023
Lowry OH, Rosebrough NJ, Farr AL, Randall RL. 1951. Protein measurement with the folin phenol reagent. J Biol Chem. 193(1):265-275. https://doi.org/10.1016/S0021-9258(19)52451-6 DOI: https://doi.org/10.1016/S0021-9258(19)52451-6
Madkour K, Dawood MAO, Sewilam H. 2022. The use of Artemia for aquaculture industry: An updated overview. Ann Anim Sci. 23(1):3-10. https://doi.org/10.2478/aoas-2022-0041 DOI: https://doi.org/10.2478/aoas-2022-0041
Maldonado-Montiel TDNJ, Rodríguez-Canché LG. 2005. Biomass production and nutritional value of Artemia sp. (Anostraca: Artemiidae) in Campeche, México. Rev Biol Trop. 53(3–4):447-454. https://doi.org/10.15517/rbt.v53i3-4.14613 DOI: https://doi.org/10.15517/rbt.v53i3-4.14613
Marella TK, Tiwari A. 2020. Marine diatom Thalassiosira weissflogii based biorefinery for co-production of eicosapentaenoic acid and fucoxanthin. Bioresour Technol. 307:123245. https://doi.org/10.1016/j.biortech.2020.123245 DOI: https://doi.org/10.1016/j.biortech.2020.123245
Martínez-Córdova LR, Martínez-Porchas M, López-Elías JA, Enríquez-Ocaña LF. 2014. Uso de microorganismos en el cultivo de crustáceos = Use of microorganisms in crustacean culture. Biotecnia. 16(3):50-55. https://doi.org/10.18633/bt.v16i3.141 DOI: https://doi.org/10.18633/bt.v16i3.141
Méndez-Martínez Y, García-Guerrero MU, Lora-Vilchis MC, Martínez-Córdova LR, Arcos-Ortega FG, Alpuche JJ, Cortés-Jacinto E. 2018. Nutritional effect of Artemia nauplii enriched with Tetraselmis suecica and Chaetoceros calcitrans microalgae on growth and survival on the river prawn Macrobrachium americanum larvae. Aquac Int. 26:1001-1015. https://doi.org/10.1007/s10499-018-0264-0 DOI: https://doi.org/10.1007/s10499-018-0264-0
Millán-Almaraz MI, Nieves-Soto M, López-Peraza DJ, Peraza-Yee MM. 2021. Effect of light and feed density on ingestion rate, protein and lipid content of Artemia franciscana juveniles. Lat Am J Aquat. 49(5):717-724. https://doi.org/10.3856/vol49-issue5-fulltext-2695
Paliwal C, Ghosh T, George B, Pancha I, Maurya R, Chokshi K, Ghosh A, Mishra S. 2016. Microalgal carotenoids: Potential nutraceutical compounds with chemotaxonomic importance. Algal Res. 15:24-31. http://doi.org/10.1016/j.algal.2016.01.017 DOI: https://doi.org/10.1016/j.algal.2016.01.017
Pande SV, Khan RP, Venkitasubramanian TA. 1963. Microdetermination of lipids and serum total fatty acid. Anal Biochem. 6(5):415-423. https://doi.org/10.1016/0003-2697(63)90094-0 DOI: https://doi.org/10.1016/0003-2697(63)90094-0
Pangestuti R, Kim, SK. 2011. Biological activities and health benefit effects of natural pigments derived from marine algae. J Funct Foods. 3(4):255-266. https://doi.org/10.1016/j.jff.2011.07.001 DOI: https://doi.org/10.1016/j.jff.2011.07.001
Panis G, Carreon JR. 2016. Commercial astaxanthin production derived by green alga Haematococcus pluvialis: a microalgae process model and a techno-economic assessment all through production line. Algal Res. 18:175-190. https://doi.org/10.1016/j.algal.2016.06.007 DOI: https://doi.org/10.1016/j.algal.2016.06.007
Pérez-Rodríguez JC, Yamasaki-Granados S, García-Guerrero MU, Martínez-Porchas M, Méndez-Martínez Y, Latournerié-Cervera JR, Cortés-Jacinto E. 2018. Growth and survival of juvenile cauque river prawn Macrobrachium americanum fed with diets containing different protein levels. Lat Am J Aquat Res. 46(3):534-542. http://doi.org/10.3856/vol46-issue3-fulltext-6 DOI: https://doi.org/10.3856/vol46-issue3-fulltext-6
Pugkaew W, Meetam M, Yokthongwattana K, Leeratsuwan N, Pokethitiyook P. 2019. Effects of salinity changes on growth, photosynthetic activity, biochemical composition, and lipid productivity of marine microalga Tetraselmis suecica. J Appl Phycol. 31:969-979. https://doi.org/10.1007/s10811-018-1619-7 DOI: https://doi.org/10.1007/s10811-018-1619-7
Ra CH, Sirisuk P, Jung JH, Jeong GT, Kim SK. 2018. Effects of light-emitting diode (LED) with a mixture of wavelengths on the growth and lipid content of microalgae. Bioprocess Biosyst Eng. 41:457-465. https://doi.org/10.1007/s00449-017-1880-1 DOI: https://doi.org/10.1007/s00449-017-1880-1
Ramírez-Mérida LG, Ragagnin de Menezes C, Queiroz Zepka L, Jacob-Lopes E. 2015. Microalgas: potencial para la producción de compuestos bioactivos nanoencapsulados [Microalgae: potential for the production of nanoencapsulated bioactive compounds]. Ciencia e Natura. 37(5):7-17. https://doi.org/10.5902/2179-460X19690 DOI: https://doi.org/10.5902/2179460X19690
Rasdi NW, Qin JG. 2015. Effect of N:P ratio on growth and chemical composition of Nannochloropsis oculata and Tisochrysis lutea. J Appl Phycol. 27:2221-2230. https://doi.org/10.1007/s10811-014-0495-z DOI: https://doi.org/10.1007/s10811-014-0495-z
Renaud SM, Thinh LV, Parry DL. 1999. The gross chemical composition and fatty acid composition of 18 species of tropical Australian microalgae for possible use in mariculture. Aquaculture 170(2):147-159. https://doi.org/10.1016/S0044-8486(98)00399-8 DOI: https://doi.org/10.1016/S0044-8486(98)00399-8
Rigane G, Bouaziz M, Sayadi S, Salem RB. 2013. Effect of storage on refined olive oil composition: stabilization by addition of chlorophyll pigments and squalene. J Oleo Sci. 62(12):981-987. https://doi.org/10.5650/jos.62.981 DOI: https://doi.org/10.5650/jos.62.981
Ruiz-Soto A. 2017. Implementación de una metodología por cromatografía líquida de alta resolución para la determinación del carotenoide all-trans-β-caroteno en la microalga Arthrospira platensis [Implementation of a high performance liquid chromatography methodology for the all-trans-B-carotene carotenoid determination o in the microalgae Arthrospira platensis] [Bsc thesis]. [Lima (Peru)]: Universidad Nacional de Ingeniería. 125 p.
Sainz-Escudero L, López-Estrada EK, Rodríguez-Flores PC, García-París M. 2021. Settling taxonomic and nomenclatural problems in brine shrimps, Artemia (Crustacea: Branchiopoda: Anostraca), by integrating mitogenomics, marker discordances and nomenclature rules. PeerJ. 9:e10865. https://doi.org/10.7717/peerj.10865 DOI: https://doi.org/10.7717/peerj.10865
Sánchez-Saavedra MP, Paniagua-Chávez C. 2017. Potential of refrigerated marine cyanobacterium Synechococcus elongatus used as food for Artemia franciscana. Lat Am J Aquat Res. 45(5):937-947. http://doi.org/10.3856/vol45-issue5-fulltext-9 DOI: https://doi.org/10.3856/vol45-issue5-fulltext-9
Saxena A, Mishra B, Tiwari A. 2022. Cost-effective mass cultivation of marine diatoms with local salts and its impact on growth and productivity. Bioresour Technol. 352:127128. http://doi.org/10.2139/ssrn.4035281 DOI: https://doi.org/10.1016/j.biortech.2022.127128
Shanmugam S, Rajendran R. 2018. Influence of different diets on the growth, survival, fecundity and proximate composition of brine shrimp Artemia franciscana (Kellog, 1906). Aquac Res. 50(2):1-14. https://doi.org/10.1111/are.13882 DOI: https://doi.org/10.1111/are.13882
Sorgeloos P, Lavens P, Leger P, Tackaert W, Versichele D. 1986. Manual for the culture and use of brine shrimp Artemia in aquaculture. Belgium: Belgian Development Agency; FAO. 319 p.
Tlusty MF, Goldstein JS, Fiore DR. 2005. Hatchery performance of early benthic juvenile American lobsters (Homarus americanus) fed enriched frozen adult Artemia diets. Aquac Nutr. 11(3):191-198. https://doi.org/10.1111/j.1365-2095.2005.00339.x DOI: https://doi.org/10.1111/j.1365-2095.2005.00339.x
Vizcaíno-Ochoa V, Lazo JP, Barón-Sevilla B, Drawbridge MA. 2010. The effect of dietary docosahexaenoic acid (DHA) on growth, survival and pigmentation of California halibut Paralichthys californicus larvae (Ayres, 1810). Aquaculture. 302:228-234. https://doi.org/10.1016/j.aquaculture.2010.02.022 DOI: https://doi.org/10.1016/j.aquaculture.2010.02.022
Wang X, Miao J, Pan L, Li Y, Lin Y, Wu J. 2019. Toxicity effects of p-choroaniline on the growth, photosynthesis, respiration capacity and antioxidant enzyme activities of a diatom, Phaeodactylum tricornutu. Ecotoxicol Environ Saf. 169:654-661. https://doi.org/10.1016/j.ecoenv.2018.11.015 DOI: https://doi.org/10.1016/j.ecoenv.2018.11.015
Whyte JNC. 1987. Biochemical composition and energy content of six species of phytoplankton used in mariculture of bivalves. Aquaculture. 60(3–4):231-241. https://doi.org/10.1016/0044-8486(87)90290-0 DOI: https://doi.org/10.1016/0044-8486(87)90290-0
Wongrat L. 1995. Phytoplankton. Bangkok (Thailand): Faculty of Fisheries, Kasetsart University.
Zapata M, Garrido JL, Jeffrey SW. 2006. Chlorophyll c pigments: current status. In: Grimm, B, Porra RJ, Rüdiger W, Scheer, H. (eds.), Chlorophylls and Bacteriochlorophylls: Biochemistry, Biophysics, Functions and Applications. Dordrecht (The Netherlands): Springer: p. 39–53. https://doi.org/10.1007/1-4020-4516-6_3 DOI: https://doi.org/10.1007/1-4020-4516-6_3
Zar JH. 2010. Biostatistical analysis. New Jersey (USA): Prentice Hall. 663 p.
Zazueta-Patrón IE. 2016. Crecimiento, biomasa y composición proximal de microalgas cultivadas en medios limitantes de nitrógeno [Growth, biomass, and proximal composition of microalgae cultured in limiting nitrogen media] [MSc thesis]. [Mazatlan (Sinaloa, Mexico)]: Facultad de Ciencias del Mar de la Universidad Autónoma de Sinaloa (FACIMAR-UAS). 55 p.