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Microalgae in Aquaculture: A Review with


Special References to Nutritional Value and
Fish Dietetics

Article March 2014


DOI: 10.1007/s12595-013-0089-9

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Proc Zool Soc

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DOI 10.1007/s12595-013-0089-9
KO
L K A TA

REVIEW ARTICLE

Microalgae in Aquaculture: A Review with Special References


to Nutritional Value and Fish Dietetics
Sudeshna Sen Roy Ruma Pal

Received: 22 June 2012 / Revised: 25 November 2013 / Accepted: 10 December 2013


Zoological Society, Kolkata, India 2014

Abstract Microalgal biotechnology has gained consid- Introduction


erable importance in recent decades and its use is extending
day by day into several areas like nutraceutical research, Microalgae play a vital role in aquatic food chain and are
renewable energy source, production of essential biomol- popularly used in rearing of aquatic animals like mollusks,
ecules like b-carotene, astaxanthin, PUFA, bio colorant shrimps and fishes at different growth stages (Borowitzka
production, wastewater treatment, bioremediation and 1998). They are required for larvae nutrition during a brief
aquaculture etc. Among all these, microalgae as a source of period of life cycle and are used either for direct con-
nutrition have drawn the attention since long back and are sumption or indirectly as prepared feed. In most instances,
widely used in animal nutrition. Fishmeal is the preferred the whole algae are used as feed or feed supplement. Live
protein ingredient of feed in aquaculture industry, con- algae also improve the water quality. Data on chemical
tributing significantly to the variable production cost. composition of algae give the basic information on the
However, decreasing fishmeal supply and increasing costs nutritive potential of the algae biomass (Brown et al. 1997).
threaten the sustainability and growth of the aquaculture The popularity of microalgae as aquaculture feed is
industry. Therefore, complete or partial substitution of increasing day by day due to their appropriate size, high
fishmeal with alternative proteins is needed to solve the nutritional value, high growth rate, antioxidant property,
problem. Presently, microalgae are used worldwide as an disease resistance power etc. The nutritional value of
alternate protein source replacing fishmeal successfully. In microalgae is influenced by their size, shape, digestibility,
feeding trials with fish, many types of microalgae have and biochemical compositions (Brown et al. 1997). They
been found to be used for increasing growth (protein are used as basic nutrients in one hand and as a source of
accretion), feed utilization, physiological activity, stress pigments to colour the skin on the other. Therefore, gross
response, starvation tolerance, disease resistance, and car- chemical compositions of various microalgae have been
cass quality. In the present communication an attempt has determined by various authors to reveal their nutritional
been taken to review the application of different microal- value for using them successfully as aquaculture feed.
gae in rearing of aquaculture animal especially the fishes. Some of them are mentioned below.

Keywords Microalgae  Nutrition  Aquaculture 


Dietetics Major Nutrient (Protein, Carbohydrate, Lipid)

Several microalgae containing high protein, carbohydrate


and lipid are considered as important feed ingredients.
Renaud et al. (1994) reported more protein in diatoms in
comparison to chlorophycean members. Spirulina, Scene-
S. S. Roy  R. Pal (&)
desmus and Chlorella were considered as source of single
Department of Botany, University of Calcutta, 35, Ballygunge
Circular Road, Kolkata 700019, India cell protein due to 4070 % protein content (Venkataraman
e-mail: rpalcu@rediffmail.com and Becker 1985). For microalgae, nutritional value of

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protein component (protein plus free amino acids) is con- neutral lipid, glycolipid and phospholipid fractions at 7.24,
sidered to be high if their essential amino acid composition 2.45 and 1.48 % level on a dry weight basis, respectively.
is close to the requirement of the feeding animals (Webb The present group has also reported the lipid content and
and Chu 1983). Carbohydrates play an important role in fatty acid profiles of 21 fresh water and brackish water
digestibility of the total algal biomass (Percival and Turvey algae from Sunderban area (Sen Roy et al. 2009; Barman
1974). Carbohydrates of algae are found in the form of et al. 2012).
starch, cellulose, sugars and other polysaccharides. Car- The protein, carbohydrate and lipid contents of some
bohydrate content of twelve species of microalgae was major algae are summarized in Table 1.
reported by Renaud et al. (1994) belonging to Bacillario-
phyceae and Chlorophyceae. Amino Acid
Algal lipids are typically composed of glycerol, sugars
or bases, esterified to fatty acids having carbon numbers in The amino acid pattern of almost all algae compares
the range of C12C22, which may be either saturated or favorably with that of other food proteins, with minor
unsaturated. Triglycerides are the most common storage deficiencies in sulfur containing amino acids methionine
lipids and may constitute up to 80 % of the total lipid and cystein (Becker 2004). Webb and Chu (1983) reported
fraction in cyanobacteria (Tornabene et al. 1983). Other high arginine content in Tetraselmis suecica, T. chuii and
major algal lipids are lecithin, phosphatidyle glycerol and Pavlova lutheri, hence, considered them as superior in
inositol. In addition, more unusual compounds such as the nutritional quality. Elaborate literature are available on
betaine lipids, chlorosulfolipids or various other sulfolipids amino acid profile of different algae viz. Spirulina maxima
may be major components of some species or orders. (Paoletti et al. 1980), Spirulina platensis (Becker and
Lipids are highly significant at various growth stages of Venkataraman 1984), Scenedesmus obliquus (El-Fouly
many aquaculture animals including marine fish larvae, et al. 1980), C. ellipsoidea (Priestly 1976), C. vulgaris (El-
bivalves, mollusks etc. The major cellular lipids of blue Fouly et al. 1980), Dunaliella bardawil (Ben-Amotz and
green algae include monogalactosyldiglyceride, dig- Avron 1980), D. salina (Becker 1994), Aphanizomenon
alactosyldiglyceride and sulfoquinovosyldiglyceride (Nic- flos-aquae (Becker 1994). Spirulina platensis showed
hols 1970). Choi et al. (1987) reported complete lipid almost similar amino acid profile as egg, better in some
profile of Scenedesmus obliquus with 11.7 % total lipid and cases depending on the culture condition (Becker and

Table 1 Protein, carbohydrate and lipid contents of few microalgae


Algae Protein (%) Carbohydrate (%) Lipid (%) Reference

Spirulina platensis 5065 814 49 Venkataraman and Becker (1985), Becker (1994)
Chlorella sp. 5158 1217 1422 (Trubachev et al. (1976), Aaronson et al. (1980), Becker (1994),
Renaud et al. (1994)
Scenedesmus sp. 5056 1052 1214 Hindak and Probil (1968), Becker (1984, 1994)
Dunaliella sp. 4957 432 68 Eddy (1956), Parson et al. (1961)
Synechococcus sp. 63 15 11 Trubachev et al. (1976)
Euglena sp. 3961 1418 1420 Collyer and Fogg (1955), Becker (1994)
Prymnesium sp. 2845 2533 2238 (Ricketts 1966)
Anabaena sp. 48 2530 47 Becker (1994)
Chlamydomonas sp. 4356 2.917 1422 Becker (19940, Renaud et al. (1994)
Porphyridium sp. 2839 5057 Becker (1994)
Spirulina maxima 6071 1316 67 Becker (1994)
Spirogyra 620 3364 1121 Becker (1994)
Tetraselmis 52 15 1645 Becker (1994), Brown (1991)
Pavlova 2429 69 914 Brown (1991), Becker (1994)
Enteromorpha intestinalis 6.15 30.58 7.13 Chakraborty and Santra (2008)
Rhizoclonium riparium 21.09 15.34 3.37 Chakraborty and Santra (2008)
Lola capillaris 40.87 22.32 4.05 Chakraborty and Santra (2008)
Ulva lactuca 8.44 35.27 4.36 Chakraborty and Santra (2008)
Catenella repns 8.42 28.96 5.29 Chakraborty and Santra (2008)
Polysiphonia mollis 16.59 25.81 5.79 Chakraborty and Santra (2008)

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Table 2 List of a few microalgae used in fish aquaculture


Algae Fish Reference

Nannochloropsis oculata, Tetraselmis tetrahele Rotifers and Lim (1991)


and Skeletonema costatum shrimp larvae
Spirulina, Haematococcus Shrimp, salmon Broun (1980), Appler (1985), Zeinhom (2004), El-Hindawy et al.
(2006), Regunathan and Wesley (2006)
Tetraselmis, Isocrysis, Chlorella Rotifers and Villegas et al. (1990)
shrimp larvae
Hydrodictyon, Scenedesmus Tilapia Appler (1985), El-Hindawy et al. (2006), Olvera-Novoa et al. (1998)
Spirulina, Haematococcus Red Sea Bream Mustafa et al. (1994)

Venkataraman 1984). A much recent report has been made carrageenans, agarans, and DL-galactan hybrids (Zibetti
by Chakraborty and Santra (2008) on free amino acid et al. 2005; Estevez et al. 2004, 2008).
content of eight benthic algal genera viz. Enteromorpha
intestinalis, Rhizoclonium riparium, Catenella repens, Fatty Acid
Ulva lactuca, Dictyota ceylinica, Polysiphonia millis,
Gellidiella acerosa and Lola capillaries (Table 2). Fatty acid compositions of microalgae were first studied in
the 1940s (Millner 1948). So far, more than 100 microalgal
Polysaccharide species have been analyzed for their fatty acid composi-
tion. These fatty acids are essential components of the diet
Microalgae have become particularly interesting because of humans and animals and are becoming important feed
of their polysaccharide contents. The first reports about additives in aquaculture (Borowitzka 1988). Triglycerides
agaragar production in Japan can be dated back to the year are the most common storage lipids constituting up to 8- %
1658, although cultivation was only successful from the of the total lipid fraction (Becker 2004). It has been found
middle of the last century (Pulz and Gross 2004). Proper that S. platensis may serve as a valuable source of c
exploration can be dated back to the 1950s when Lewis linolenic acid and about 2030 % of its fatty acids consist
(1956) screened a number of Chlamydomonas spp. for of this compound (Becker 2004). Cyanobacterial lipids
extracellular polysaccharide production. The most useful of tend to have 2560 % of PUFA and are rich in essential
these is C. mexicana, which yields up to 25 % of its total fatty acids such as the C:18 linoleic (18:2) and linolenic
organic production as polysaccharides. Later Ramus (1972) (18:3) acids and their C-20 derivatives, eicosapentaenoic
reported large quantities of extracellular polysaccharides acids (20:5) and arachidonic acid (20:4) (Borowitzka
(EPS) production in green and blue-green algae and uni- 1988). Whereas, pure cultures of green algae contain pri-
cellular red algae Porphyridium cruemtum and P. aerugi- marily C:16, C:18 fatty acids with a high degree of un-
neum respectively. The principal sugars found in the saturation (Thompson 1996). Kenyon (1972) reported
polysaccharides of some microalgae commonly used in complete fatty acid profile of 34 strains of unicellular blue
aquaculture like, Pyramimonas virginica, Pseudoisochrysis green algae belonging to the genera Synechococcus, Ap-
paradoxa, C. vulgaris, P. lutheri and Isochrysis galbana, hanocapsa, Gloeocapsa, Microcystis and Chlorogloea.
are glucose, mannose, ribose/xylose, rhamnose and fucose Volkman et al. (1989) reported PUFA (EPA) in four genera
with glucose being the major constituent and accounted for of diatoms viz. Chaetoceros calcitrans, Chaetoceros
2886 % of the total carbohydrates, while mannose was a gracilis, Skeletonema costatum and Thalassiosira pseudo-
substantial component in all cases (Chu et al. 1982). nana (4.611.1 % of the total fatty acids), the cryptomonad
Extracellular carbohydrate polymer (EPS) production has Chroomonas salina (10.9, 11.9 %) and the prymnesiophyte
been reported for Anabaena cylindrica (Lama et al. 1996), P. lutheri (19.7 %). He also reported high amount of DHA
Nostoc (Flaibani et al. 1989) and Spirulina (Tseng and in C. salina and Nitzschia sp. and also high percentage of
Zhao 1994). The ten monosaccharides commonly found in EPA (44.6 %) (Kates and Volcani 1966; Ben-Amotz et al.
cyanobacterial water soluble polysaccharides are: the 1985). The major fatty acids in Nannochloropsis are 14:0,
hexoseglucose, galactose and mannose, the pentose 16:0, 20:4x6 and 20:5x5 (Schneider and Roessler, 1994)
ribose, arabinose and xylose, the deoxyhexosefucose and and is commonly used as aquaculture feed. Lipid contents
rhamnose and the acidic hexoseglucuronic and galact- of seaweeds Sargasaam wightii (0.1591.551 %), S. hor-
uronic acid (De Philippis et al. 2000). Sulfated galactans neri (1.381.96 %), Gracillaria sp. (0.783.97 %), Cate-
are the most abundant polymers in red seaweeds, including nella linum (1.28.6 %) have also been studied by many

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workers (Sasikumar 2000; Hossain et al. 2003). The red vitamin profiles of several algae are done over the years
alga P. cruentum is one of the richest natural sources of viz. Spirulina platensis (Becker and Venkataraman 1984),
arachidonic acid which constitutes about 36 % of the total S. maxima (Jaya et al. 1980), Scenedesmus obliquus
fatty acid. As the x-3 fatty acids in fish oils derive from the (Becker 1984; Jaleel and Soeder 1978), S. quadricauda
marine phytoplankton, on which the oceanic food chains (Cook 1960), C. pyrenoidosa (Fisher and Burlew 1953),
are based, the production of marine microalgae particularly Aphanizomenon flos aquae (Becker 1994) etc. Brown et al.
of biomass with high x-3 fatty acids was of great interest (1999) reported the vitamin content of few Australian
(Yongmanitchai and Ward 1991). microalgae like Nannochloropsis, Pavlova, Strichococcus,
Tetraselmis, Chaetoceros, Thalassiosira and Isochrysis.
Pigments Concentrations of other vitamins typically show a two- to
four-fold difference between species (Seguineau et al.
One of the most obvious and interesting characteristic of 1996; Brown et al. 1999). Based on these data Brown
the algae is their vast range of pigment content like, (2002) suggested that a carefully selected, mixed-algal diet
chlorophylls, carotenoids, phycobiliproteins, xanthophylls should provide adequate concentrations of the vitamins for
etc. Most of them are important in aquaculture. Lipophilic aquaculture food chains.
pigments such as chlorophylls and carotenoids constitute
35 % of the dry algal biomass (Venkataraman and Becker Microalgae in Fish Aquaculture
1985). Chlorophylls are of mainly five types viz. a, b, c, d
and e and amount usually to about 0.51.5 % of dry weight Gladue and Maxey (1994) commented that due to con-
(Becker 1994). Recently, Kumar et al. (2009) evaluated the current trends of increasing consumption of seafood with
pigment composition of 18 marine microalgae of the Indian decreasing natural harvests, a larger portion of seafood
coast and reported maximum chlorophyll a, b as well as must be derived from aquaculture in the fast approaching
total chlorophyll in most of the species of Chlorophyta 21st century. Fishmeal has long been used as a source of
followed by Phaeophyta and Rhodophyta. The nutritional protein in formulating artificial fish feed. But due to the
and therapeutic relevance of certain carotenoids is due to non-availability as well as the increasing cost of fishmeal,
their ability to act as provitamin A, that is, they can be it has become essential to search for an alternate source of
converted into vitamin A (Gouveia and Empis 2003; Gar- protein to prepare a balanced feed for fish. A large number
ca-Gonzalez et al. 2005). Moreover, carotenoids have of research works have been carried to evaluate various
intrinsic anti-inflammatory properties owing to their alternate protein sources as partial or complete dietary
quenching action on reactive oxygen species. The average replacement of fishmeal for different fish species, like,
carotenoid concentration of algae is 0.12 % of the dry salmon, rainbow trout, chinnok salmon-Onorhynchus spp.
weight though exceptions are there (Becker 1994). The (Higgs et al. 1979; Tacon et al. 1984; Fowler 1991; Stef-
most well-known b-carotene rich microalga is Dunaliella fens 1994; Stickney et al. 1996; Bureau et al. 2000), Java
salina (14 % of DW) (Metting 1996) and astaxanthin rich and Nile tilapiaOryochromis spp. (Jackson et al. 1982;
microalga is Haematococcus pluvialis (1.53 % of DW) Wee and Wang 1987; El-Sayed 1998), Indian major carp
(Todd Lorenz and Cysewski 2000) and their price ranging Labeo rohita (Hasan et al. 1991, 1994, 1997; Hasan and
from US$ 300 to US$ 3000/kg are quite popularly used in Das 1993), India major carpCirrhinus mrigala (Hasan
developed countries (Ben-Amotz 2004; Hejazi and Wijf- et al. 1988) and common carpCyprinus carpio (Atack
fels 2004). The main commercial producers of phycobili- et al. 1979; Capper et al. 1982; Hossain and Jauncey 1989;
proteins (phycoerythrin and phycocyanin), are Yilmaz et al. 2003) etc.
cyanobacterium Arthrospira and rhodophycean member During 1980s1990s, microalgal feeds were used in
Porphyridium (Viskari and Colyer 2003; Bermejo Roman relatively small amounts in aquaculture, mainly for the
et al. 2002). Other important carotenoids include lutein, production of larvae, juvenile shell and finfish as well as for
lutein 5,6-epoxide, antheraxanthin, zeaxanthin, violaxan- raising the zooplanktons required for feeding of juvenile
thin, neoxanthin etc. (Borowitzka and Borowitzka 1988). fishes and other animals etc. (Benemann 1992; Coutteau
and Sorgeloos 1992; Duerr et al. 1998). Possibility of
Vitamins partial replacement of fishmeal with algae has also been
considered by several workers (Broun 1980; Appler 1985;
Microalgae are good source of different vitamins which are Zeinhom 2004; El-Hindawy et al. 2006), especially in
essential in aquaculture. A number of vitamins are present tropical areas where they are found in abundant amounts.
in rather higher concentrations in algae than that of other Spirulina and Haematococcus were used in substantial
traditionally considered rich conventional sources (Brown amount (100 t year-1) as fish, shrimp and salmon feed
and Farmer 1994; Venkataraman et al. 1994). Complete during that period. A report was made by Lim (1991) about

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co-culture of N. oculata, T. tetrahele and S. costatum to Considering the present status of progress made in appli-
feed rotifers and shrimp larvae in singapore. Tetraselmis cation of algal feed in fish dietetics, it would be realistic to
tetrahele and I. galbana improved the food value of rotifers believe that algal biomass would play a positive role in
(B. plicatilis) as live food for the milkfish fry (Villegas enhancement of growth performances of edible fishes, their
et al. 1990). Their high dietary value was related to higher disease resistance and the skin color especially of the
algal protein and fat levels especially x-3 hufa, compared colored fishes. As the nutraceutical properties of different
to B. plicatilis cultured on Chlorella. algal genera can be exploited in aquaculture industry, it is
In feeding trials with fish, many types of microalgae therefore necessary to investigate thoroughly the role of
have been found to increase growth (protein accretion), both micro- and macroalgal biomass as feed supplement
feed utilization, physiological activity, stress response, for different aquaculture animals in a cost effective way.
starvation tolerance, disease resistance, and carcass quality
(Mustafa and Nakagawa 1995). For example, when tested Acknowledgments The first author is thankful to West Bengal State
Council of Science and Technology for financial support.
in fish diets, Spirulina led to enhanced growth and
improved protein digestibility (Mustafa et al. 1994), stress
and disease resistance (Henson 1990; Olvera-Novoa et al. References
1998), improved carcass quality (Belay et al. 1996; Floreto
et al. 1996), and induced early maturation thereby leading Aaronson, S., T. Berner, and Z. Dubinsky. 1980. Microalgae as a
to a shorter breeding cycle and period of cultivation (Braun source of chemicals and natural products. In Algae biomass,
575th ed, ed. G. Shelef, and C.J. Soeder. Amsterdam: Elsevier,
1988). Microalgae biomass was also tested as a carotenoid Biomedical Press.
source for shrimp broodstock (Regunathan and Wesley Appler, H.N. 1985. Evaluation of Hydrodictyon reticulatum as protein
2006) and as a protein or lipid source to partially replace source in feeds for Oreochromis niloticus and Tilapia zillii.
fish meals or fish oil in fish feeds (Olvera-Novoa et al. Journal of Fish Biology 27(3): 327334.
Atack, T.H., K. Jauncey, and A.J. Matty. 1979. The utilization of
1998; Belay et al. 1996; Patnaik et al. 2006). Blue-green some single cell proteins by fingerling mirror carp (Cyprinus
algae are common components in the diet of Oreochromis carpio). Aquaculture 18: 337348.
niloticus and O. mossambicus (Fryer and Iles 1972; Mor- Azaza, M.S., F. Mensi, J. Ksouri, M.N. Dhraief, B. Brini, A.
iarty and Moriarty 1973; Trewevas 1983; Getachew 1987; Abdelmouleh, and M.M. Kraem. 2008. Growth of Nile tilapia
(Oreochromis niloticus L.) fed with diets containing graded
Vonshak 1997). Ulva meal has been successfully used as a levels of green algae Ulva meal (Ulva rigida) reared in
feed ingredient for tilapia. Recent studies have shown geothermal waters of southern Tunisia. Journal of Applied
incorporation of Ulva meal may enhance carcass compo- Ichthyology 24: 202207.
sition (Guroy et al. 2007; Azaza et al. 2008). Barman, N., G.G. Satpati, S. Sen Roy, N. Khatoon, R. Sen, S.
Kanjilal, R.B.N. Prasad, and R. Pal. 2012. Mapping algae of
The present group also tested a number of microalgal sundarban origin as lipid feedstock for potential biodiesel
biomass mix as value added feed employing different algal application. Journal of Algal Biomass Utilisaton 3(2): 4249.
genera like S. platensis, S. subsalsa, Phormidium valde- Becker, E.W. 1984. Biotechnology and exploitation of the green alga
rianum, Phormidium tenue, N. ellipsosporum, N. minima, Scenedesmus obliquus in India. Biomass 4: 1.
Becker, E.W. 1994. Microalgae: Biotechnology and microbiology.
Rhizoclonium fontinale, Rhizoclonium riparium, Spirogyra Cambridge: Cambridge University Press.
sp., Enteromorpha intestinalis, U. lactuca for Prawn, Rohu, Becker, E.W., and L.V. Venkataraman. 1984. Production and
Tilapia and Gold fish (Khatoon et al. 2009, 2010a, b; Sen utilization of the blue green alga Spirulina in India. Biomass 4:
Roy et al. 2011; Mukherjee et al. 2011).The main objective 105.
Becker, E.W. 2004. Micro algae in human and animal nutrition. In
was to use non-conventional local algal genera as supple- Hand book of microalgal culture, ed. A. Richmond, 312351.
mented feed for lowering the production cost of algae Oxford: Blackwell.
based fish feed. The algae based value added feed resulted Belay, A., T. Kato, and Y. Ota. 1996. Spirulina (Arthrospira);
in both growth and reduced PL stage for Prawn, better Potential application as an animal feed supplement. Journal of
Applied Phycology 8: 303311.
growth performance, carcass quality for Rohu and Tilapia Ben-Amotz, A. 2004. Industrial production of microalgal cell-mass
and vibrant skin color for Gold Fishes. and secondary products: Major industrial species: Dunaliella. In
Hand book of microalgal culture, ed. A. Richmond, 273280.
Oxford: Blackwell.
Ben-Amotz, A., and M. Avron. 1980. Glycerol, b-carotene and dry
Conclusions algal meal production by commercial cultivation of Dunaliella.
In Algae biomass, 603rd ed, ed. G. Shalef, and C.J. Soeder.
Use of algal biomass in aquaculture technology is of fun- Amsterdam: Elsevier, Biomedical Press.
damental importance if algal biotechnology is to play a Ben-Amotz, A., T.G. Tornabene, and W.H. Thomas. 1985. Chemical
profiles of selected species of microalgae with emphasis on
central role in aquaculture industry. The aquatic habitat and lipids. Journal of Phycology 21: 7281.
the appropriate size of the microalgae are consumed Benemann, J.R. 1992. Microalgae aquaculture feeds. Journal of
directly by the fishes or indirectly via zooplanktons. Applied Phycology 4: 233245.

123
Proc Zool Soc

Bermejo Roman, R., J.M. Alvarez-Pez, F.G. AcienFernandez, and E. culture collection for the production of polysaccharides of
Molina Grima. 2002. Recovery of pure B-phycoerythrin from the applied interest. Journal of Applied Phycology 12: 401407.
microalga Porphyridium cruentum. Journal of Biotechnology 93: Duerr, E.O., A. Molnar, and V. Sato. 1998. Cultured microalgae as
7385. aquaculture feeds. Journal of Marine Biotechnology 75: 6570.
Borowitzka, M.A. 1988. Microalgae as sources of pharmaceuticals Eddy, B.P. 1956. The suitability of some algae for mass cultivation
and other biologically active compounds. Journal of Applied for food with special reference to Dunaliella bioculata. Journal
Phycology 4: 267279. of Experimental Botany 7: 372.
Borowitzka, M.A. 1998. Algae as food. In Microbiology of fermented El-Fouly, M.M., F.E. Abdalla, F.K. El-Baz and A.F.A. Fawzi. 1980.
foods, 2nd ed, ed. B.J.B. Wood, 585602. London: Blackie Mass production of microalgae in the national research centre.
Academic and Professional. Proceedings of the 2nd Egypt. Cairo: Algae Symposium Cairo.
Borowitzka, M.A., and L.J. Borowitzka. 1988. Limits to growth and El-Hindawy, M.M., M.A. Abd-Razic, H.A. Gaber and M.M. Zenhom.
carotenogenesis in laboratory and large-scale outdoor cultures of 2006. Effect of various level of dietary algae Scenedesmus spp.
Dunaliella salina. In Algal biotechnology, ed. T. Stadler, J. on physiological performance and digestibility of Nile tilapia
Mollion, M.C. Verdus, Y. Karamanos, H. Morvan, and D. fingerlings, 137149. 1st Scientific Conference of the Egyptian
Christiaen, 171181. Barking: Elsevier Applied Science. Aquaculture Society. Sinai: Sharm El-Sheikh.
Braun, L. 1988. Spirulina: Food for the future. Aquatopics, 9th ed. El-Sayed, A.F.M. 1998. Total replacement of fish meal with animal
Baltimore: National Agricultural Library. protein sources in Nile tilapia, Oreochromis niloticus (L.) feeds.
Broun, W. 1980. Note on the survival of algal resting cells during Aquaculture Research 29: 275280.
long-term maintenance in darkness and minimum lake bottom Estevez, J.M., M. Ciancia, and A.S. Cerezo. 2004. System of galactans
temperature. Comparison of Anabaena 5: 677680. of the red seaweed Kappaphycus alvarezii with emphasis on its
Brown, M.R. 1991. The amino acid and sugar composition of 16 minor constituents. Carbohydrate Research 339: 25752592.
species of microalgae used in mariculture. Journal of Experi- Estevez, J.M., M. Ciancia, and A.S. Cerezo. 2008. The system of
mental Marine Biology and Ecology 145: 7999. sulfated galactans from the red seaweed Gymnogongrus torulo-
Brown, M.R. 2002. Nutritional value of microalgae for aquculture. In: sus (Phyllophoraceae, Rhodophyta). Location and structural
Avances en Nutricion Acucola VI. eds. L. E Cruz-Suarez, D analysis. Carbohydrate Polymers 73: 594605.
Ricque-Marie, M Tapia-Salazar, M G Gaxiola-Cortes, N Simoes. Fisher, A.W., and J.S. Burlew. 1953. Nutritional value of microscopic
Memorias del VI Simposium Internacional de Nutricion Acu- algae. In Algal culture from laboratory to Pilot plant, 600th ed,
cola. 3 al 6 de Septiembre del Cancun, Quintana Roo, Mexico. ed. J.W. Burlew, 303. Washington: Carnegie institute.
Brown, M.R., S.W. Jeffrey, J.K. Volkman, and G.A. Dunstan. 1997. Flaibani, A., Y. Olsen, and T.J. Painter. 1989. Polysaccharides in
Nutritional properties of microalgae for mariculture. Aquacul- desert reclamation: Composition of exocellular proteoglycan
ture 151: 315331. complexes produced by filamentous blue-green and unicellular
Brown, M.R., M. Mular, I. Miller, C. Trenerry, and C. Farmer. 1999. green edaphic algae. Carbohydrate Research 190: 235248.
The vitamin content of microalgae used in aquaculture. Journal Floreto, E.A.T., S. Teshima, and S. Koshio. 1996. The effects of
of Applied Phycology 11: 247255. seaweed diets on the lipid and fatty acids of the Japanese disc
Brown, M.R., and C.A. Farmer. 1994. Riboflavin content of six abalone Haliotis discus hannai. Fisheries Science 62: 582588.
species of microalgae used in mariculture. Journal of Applied Fowler, L.G. 1991. Poultry by product meal as a dietary protein
Phycology 6: 6165. source in fall chinook salmon diets. Aquaculture 99: 309321.
Bureau, D.P., A.M. Harris, D.J. Bevan, L.A. Simmons, P.A. Azevedo, Fryer, G., and T.D. Iles. 1972. The cichlid fishes of the Great Lakes of
and C.Y. Cho. 2000. Use of feather meals and meat and bone Africa: Their biology and evolution, 641. Edinburgh: Oliver & Boyd.
meals from different origins as protein sources for rainbow trout Garca-Gonzalez, M.J., J.C. Moreno, F.J. Manzano, M.G. Florencio,
(Oncorhynchus mykiss) diets. Aquaculture 181: 281291. and Guerrero. 2005. Production of Dunaliella salina biomass
Capper, B.S., J.F. Wood, and A.J. Jackson. 1982. The feeding value rich in 9-cis-b-carotene and lutein in a closed tubular photobi-
for carp of two types of mustard seed cake from Nepal. oreactor. Journal of Biotechnology 115: 8190.
Aquaculture 29: 373377. Getachew, T. 1987. A study of an herbivorous fish, Oreochromis
Chakraborty, S., and S.C. Santra. 2008. Biochemical composition of niloticus L., diet and its quality in two Ethiopian Rift Valley
eight benthic algae collected from Sunderban. Indian Journal of lakes, Awasa and Zwai. Journal of Fish Biology 30: 439449.
Marine Sciences 37(3): 329332. Gladue, R.M., and J.E. Maxey. 1994. Microalgal feeds for aquacul-
Choi, K.J., V. Nakhost, J. Krukonis, and M. Karel. 1987. Supercritical ture. Journal of Applied Phycology 6: 131141.
fluid extraction and characterization of lipids from algae Gouveia, L., and J. Empis. 2003. Relative stabilities of microalgal
Scenedesmus obliquus. Food Biotechnology 1(2): 263281. carotenoids in microalgal extracts, biomass and fish feed: Effect
Chu, Fu-Lin E., J.L. Dupuy, and K.L. Webb. 1982. Polysaccharide of storage conditions. Innovative Food Science & Emerging
composition of five algal species used as food for larvae of the Technologies 4: 227233.
American oyster, Crassostrea virginica. Aquaculture 29(34): Guroy, B.K., A.A. Tekinay, S. Cirik, D, Guroy, and F, Sanver. 2007.
241252. Effects of Ulva rigida or Cystoseira barbata meals as a feed
Collyer, D.M., and G.E. Fogg. 1955. Studies on fat accumulation by additive on growth performance, feed utilization, and body
algae. Journal of Experimental Botany 6: 256. composition in Nile tilapia, Oreochromis niloticus. Turkish
Cook, B.B. 1960. The nutritive value of waste grown algae. Presented Journal of Veterinary and Animal Sciences 31: 9197.
at the 88th annual Meeting of American Public Health Associ- Hasan, M.R., and P.M. Das. 1993. A Preliminary study on the use of
ation Inc. San Fransisco. poultry offal meal as dietary protein source for the fingerlings of
Coutteau, P., and P. Sorgeloos. 1992. The requirement for live algae Indian major carp, Laboe rohita (Hamilton). In Fish nutrition
and their replacement by artificial diets in the hatchery and practise, ed. S.J. Kaushik, and P. Luquet, 793801. Paris: Institut
nursery rearing of bivalve molluscs: An international survey. National de la Recheche Agronomique.
Journal of Shellfish Research 11(2): 467476. Hasan, M.R., M.S. Haq, R.M. Das, and G. Mowlah. 1997. Evaluation
De Philippis, R., A. Ena, R. Paperi, C. Sili, and M. Vincenzini. 2000. of poultry feather meal as a dietary protein source for Indian
Assessment of the potential of Nostoc strains from Pasteur major carp, Labeo rohita Fry. Aquaculture 151: 4754.

123
Proc Zool Soc

Hasan, M.R., A.K. Azad, A.M. Omar Farooque, A.M. Akand, and exopolymer biosynthesis in Anabaena cylindrica 10C. Phyto-
P.M. Das. 1991. Evaluation of some oilseed cakes as dietary chemistry 42: 655659.
protein sources for the fry of Indian major carp, Labeo rohita Lewis, R.A. 1956. Extracellular polysaccharides of green algae.
(Hamilton). In Fish nutrition research in Asia, 5th ed, ed. S.S. Canadian Journal of Microbiology 2: 665672.
De Silva, 107117. Manila: Asian Fisheries Society. Lim, L.C. 1991. An overview of live feeds productions systems in
Hasan, M.R., P.K. Roy, and A.M. Akand. 1994. Evaluation of Singapore. In Rotifer and microalgae culture systems, ed. B.J.
leucaena leaf meal as dietary protein source for Indian major Harvey, 203221. Redmund: Argent Laboratories.
carp, Labeo rohita fingerling. In Fish nutrition research in Asia, Metting, F.B. 1996. Biodiversity and application of microalgae.
6th ed, ed. S.S. De Silva, 6976. Manila: Asian Fisheries Journal of Industrial Microbiology 17: 477489.
Society. Millner, H.W. 1948. The fatty acids of Chlorella. Journal of
Hasan, M.R., P.K. Roy, N. Shaheen, and G. Mowlah. 1988. Biochemistry 176: 813817.
Evaluation of leucaena leaf meal as dietary protein source for Moriarty, C.M., and D.J.W. Moriarty. 1973. Quantitative estirnation
the fingerling of Indian major carp, Cirrhinus mrigala (Hamil- of the daily ingestion rate of phytoplankton by Tilapia nilotica
ton) Bangladesh. Journal of Aquaculture 10: 6982. and Haplochromis nigripinnis in Lake George, Uganda. Journal
Hejazi, M.A., and R.H. Wijffels. 2004. Milking of microalgae. Trends of Zoology, London 171: 1523.
in Biotechnology 22: 189194. Mukherjee, S., D. Parial, N. Khatoon, A. Chaudhuri, S. Sen Roy, S.
Henson, R. 1990. Spirulina improves Japanese fish feeds. Aquacul- Homechaudhuri, and R. Pal. 2011. Effect of formulated algae
ture Magazine 6: 3843. based diet on growth performance of Labeo rohita Hamilton.
Higgs, D.A., J.R. Markert, D.W. Macquarrie, J.R. McBride, B.S. Journal of Algal Biomass Utilisation 2(4): 19.
Dosanjh, C Nichols and G. Hoskins. 1979. Development of Mustafa, G.M., and H. Nakagawa. 1995. A review: Dietary benefits of
practical dry diets for coho salmon, Oncorhynchus kisutch, using algae as an additive in fish feed. Israeli Journal of Aquaculture-
poultry by-product meal, feather meal, soybean meal, and Bamidgeh 47: 155162.
rapeseed meal as major protein sources. Proceedings of the Mustafa, M.G., T. Umino, and H. Nakagawa. 1994. The effect of
World Symposium on Finfish Nutrition and Fishfeed Technol- spirulina feeding on muscle protein deposition in red seabream,
ogy, Hamburg, 2023, 1978. Vol.II. Berlin. pp 191218. Pagrus major. Journal of Applied Icthyology 10: 141145.
Hindak, F., and S. Probil. 1968. Chemical composition, protein Nichols, B.W. 1970. Comparative lipid biochemistry of photosyn-
digestibility and heat of combustion of filamentous green algae. thetic organisms. In Phytochemical phylogeny, ed. J.B. Harbone,
Plant Biology 10: 234. 105118. London: Academic Press New York.
Hossain, M.A., and K. Jauncey. 1989. Nutritional evaluation of some Olvera-Novoa, M.A., L.J. Daminguez-Cen, L. Olivera-Castillo, and
Bangladeshi oil seed meals as partial substitutes for fish meal in A. Carlos and Martinez-palacios. 1998. Effect of the use of the
the diets of common carp, Cyprinus carpio L. Aquaculture and micro algae Spirulina maxima as fish meal replacement in diets
Fisheries Management 20: 255268. for tilapia, Oreachromis mossambicus (Peters) fry. Aquaculture
Hossain, Z., H. Kurihara, and K. Takahashi. 2003. Biochemical Research 29: 709715.
composition and lipid compositional properties of the brown Paoletti, C., M. Vincentini, F. Bocci, and R. Materassi. 1980.
alga Sargassum horneri. Pakistan Journal of Biological Sciences Compositizione biochemical generaledellebiomasse di Spiruli-
6: 14971500. naplatensis e Spirulina maxima. In Prospettive della coltura di
Jackson, A.J., B.S. Capper, and A.J. Matty. 1982. Evaluation of some Spirulina Italia, vol. 111, ed. R. Materassi. Firenze: Firenze-
plant proteins in complete diets for the tilapia Sarotherodon Accademia dei Georgofili.
mossambicus. Aquaculture 27: 97109. Parson, T.R., K. Stephens, and J.D.H. Strickland. 1961. On the chemical
Jaleel, S.A., and C.J. Soeder. 1978. Current trends in microalgal composition of eleven species of marine phytoplanktpons. Journal
cultures as protein source in West Germany. Indian Food Packer of the Fisheries Research Board of Canada 18: 1001.
27: 45. Patnaik, S., T.M. Samocha, D.A. Davis, R.A. Bullis, and C.L.
Jaya, T.V., M.L. Scarino, and M.A. Spaodoni. 1980. Caratteristiche Browdy. 2006. The use of algal meals as highly unsaturated fatty
nutrizional in vivo di Spirulina maxima. In Prospective della- acid sources in practical diets designed for Litopenaeus vanna-
coltura di Spirulina in Italia, ed. I.R. Materassi, 195. Florence: mei. Aquaculture Nutrition 12: 395401.
Firenze-Academia dei Georgofili. Percival, E.E., and J.R. Turvey. 1974. Polysaccharides of algae. In
Kates, M., and B.E. Volcani. 1966. Lipid components of Diatoms. CRC, handbook of microbiology, condensed edition, 532nd ed,
Biochimica et Biophysica Acta 116: 264. ed. A.L. Laskin, and H.A. Lechevalier. Cleveland: CRC Press
Kenyon, C.N. 1972. The fatty acid compositions of unicellular strains Inc.
of blue green algae. Journal of Bacteriology 109: 827832. Priestly, G. 1976. Algal proteins. In Food from wastes, 144th ed, ed.
Khatoon, N., P. Chattopadhyay, A. Mukhopadhyay, M. Mukhopad- G.G. Birch, K.J. Parker, and J.T. Worgan. London: Applied
hyay, and R. Pal. 2009. Algal diet in prawn aquaculture. Fishing Science.
Chimes 28(10/11): 4447. Pulz, O., and W. Gross. 2004. Valuable products from biotechnology
Khatoon N, A. Chaudhuri, S. Sen Roy, N. Kundu, S. Mukherjee, D. of microalgae. Applied Microbiology and Biotechnology 65(6):
Mazumdar, S. Homechaudhuri and R. Pal. 2010. Algae as feed 635648.
supplement in fish nutrition. Journal of Botanical Society of Ramus, J.S. 1972. The production of extracellular polysaccharides by
Bengal 64(2): 8593. the unicellular red alga Porphyridium eurugineum. Journal of
Khatoon, N., P. Sengupta, S. Homechaudhuri, and R. Pal. 2010. Phycology 8: 97111.
Evaluation of algae based feed in Gold fish (Carassius auratus) Regunathan, C., and S.G. Wesley. 2006. Pigment deficiency correc-
nutrition. Proceedings of Zoological Society 63(2): 109114. tion in shrimp broodstock using Spirulina as a carotenoid source.
Kumar, V., B.R. Pillai, P.K. Sahoo, J. Mohanty, and S. Mohanty. Aquaculture Nutrition 12(6): 425432.
2009. Effect of dietary astaxanthin on growth and immune Renaud, S.M., D.L. Parry, and L.V. Thinh. 1994. Microalgae for use
response of giant freshwater prawn Macrobrachium rosenbergii in tropical aquaculture I: Gross chemical composition and fatty
(De Man). Asian Fisheries Science 22: 6169. acid composition of twelve species of microalgae from the
Lama, L., B. Nicolaus, V. Calandrelli, M.C. Manca, I. Romano, and Northern Territory, Australia. Journal of Applied Phycology 6:
A. Gambacorta. 1996. Effect of growth conditions on endo- and 337345.

123
Proc Zool Soc

Ricketts, T.R. 1966. On the chemical composition of some unicellular Tseng, C.T., and Y. Zhao. 1994. Extraction, purification and
algae. Phytochemistry 5: 67. identification of polysaccharides of Spirulina (Arthrospira)plat-
Sasikumar, K. 2000. Studies on biochemical composition and heavy ensis (Cyanophyceae). Algological Studies 75: 303312.
metal accumulation in seaweeds in the Vellar and Uppanar Venkataraman, L.V., and E.W. Becker. 1985. Biotechnology and
estuaries, southeast coast of India. M. Phil Thesis, Annamalai utilization of algaeThe Indian experience. Mysore: Central
University, India. Food Technological Research Institute. 257.
Schneider, J.C., and P. Roessler. 1994. Radiolabeling studies of lipids Venkataraman, L.V., T. Somasekaran, and E.W. Becker. 1994.
and fatty acids in Nannochloropsis (Eustigmatophyceae), an Replacement value of blue-green alga Spirulina platensis for
oleaginousmarine alga. Journal of Phycology 30: 594598. fishmeal and a vitamin mineral premix for broiler chicks. British
Seguineau, C., A. Laschi-Loquerie, J. Moal, and J.F. Samain. 1996. Poultry Science 35: 373381.
Vitamin requirements in great scallop larvae. Aquaculture Villegas, C.T., O. Millamena, and F. Escritor. 1990. Food Value of
International 4: 315324. (Brachionus plicatilis) fed three selected algal species as live
Sen Roy, S., A. Chaudhuri, S. Mukherjee, S. Homechaudhuri, and R. food for milkfish (Chanos chanos) Forsskai, fry production.
Pal. 2011. Composite algal supplementation in nutrition of Aquaculture and Fisheries Management 21: 213219.
Oreochromis mossambicus. Journal of Algal Biomass Utilisation Viskari, P.J., and C.L. Colyer. 2003. Rapid extraction of phycobili-
2(1): 1020. proteins from cultured cyanobacteria samples. Analytical Bio-
Sen Roy, S., N. Barman, and R. Pal. 2009. Stess Induced changes in chemistry 319: 263271.
total lipid and fatty acid composition of Navicula minima Grun. Volkman, J.K., S.W. Jeffrey, P.D. Nichols, G.I. Rodgers, and C.D.
Journal of Botanical Society of Bengal 63(1): 4751. Garland. 1989. Fatty acid and lipid composition of ten species of
Stickney, R.R., R.W. Hardy, K. Koch, R. Harrold, D. Seawright, and microalgae used in mariculture. Journal of Experimental Marine
K.C. Massee. 1996. The effects of substituting selected oilseed Biology and Ecology 128: 219240.
protein concentrates for fish meal in rainbowtrout Oncorhynchus Vonshak, A. 1997. Spirulina platensis (Arthrospira). In Physiology,
mykiss diets. Journal of World Aquaculture Society 27: 5763. cell biology and biotechnology, ed. A. Vonshak. Basingstoke:
Steffens, W. 1994. Replacing fish meal with poultry by-product meal Taylor and Francis.
in diets for rainbow trout, Oncorhynchus mykiss. Aquaculture Webb, K. L., F E Chu. 1983. Phytoplankton as a food source for
124: 2734. bivalve larvae. In Proceedings of the Second International
Tacon, A.G.J., K. Jauncey, A. Falaye, M. Pantha, I. Macgowan, and Conference on Aquaculture Nutrition: Biochemical and Physi-
E.A. Safford. 1984. The use of meat and bone meal, hydrolysed ological Approaches to Shellfish Nutrition. eds.G. D. Pruder, C.
feather meal and soybean meal in practical fry and fingerling J. Langdon and D. E. Conklin 272291. Louisiana State
diets for Oreochromis niloticus. In Proceedings of First Inter- University, Baton Rouge, LA.
national Symposium on Tilapia in Aquaculture, ed. L. Fishelson, Wee, K.L., and S.S. Wang. 1987. Nutritive value of Leucaena leaf
and Z. Yaron, 356365. Israel: TelAviv University Press. meal in pelleted feed for Nile tilapia. Aquaculture 62: 97108.
Thompson, G.A. 1996. Lipids and membrane function in green algae. Yilmaz, M., A. Gumas, S. Yilmaz, and N. Polat. 2003. Aged based
Biochimica et Biophysica Acta 1302: 1745. food preferences of common carp (Cyprinus carpio L., 1758)
Todd Lorenz, R., and G.R. Cysewski. 2000. Commercial potential for inhabiting fish lakes in the Bafra District of Samsun Province
Haematococcus microalgae as a natural source of astaxanthin. (Lakes Tath and Gici). Turkish Journal of Veterinary and Animal
Trends in Biotechnology 18: 160167. Sciences 4: 971978.
Tornabene, T.G., G. Holzer, S. Lien, and N. Burris. 1983. Lipid Yongmanitchai, W., and O.P. Ward. 1991. Growth and omega-3 fatty
composition of the nitrogen starved green alga Neochloris acid production by Phaeodactylum tricornutum under different
oleoabundans. Enzyme and Microbial Technology 5(6): culture conditions. Applied and Environmental Microbiology 57:
435440. 419425.
Trewevas, E. 1983. Tilapiine Fishes of the Genera Sarotherodon, Zeinhom, M. M. 2004. Nutritional and physiological studies on fish.
Oreochromis and Danakilia. British Museum of Natural History, Ph. D. thesis. Faculty of Agriculture, Zagazig University. Egypt.
(878)583. Ithica: Comstock Publishing Associates. Zibetti, R.G.M., M.D. Noseda, A.S. Cerezo, and M.E. Duarte. 2005.
Trubachev, N.I., I.I. Gitelzon, G.S. Kalacheva, V.A. Barashkov, V.N. The system of galactans from Cryptonemia crenulata (Halymen-
Belyanin, and R.I. Andreeva. 1976. Biochemical composition of iaceae, Halymeniales) and the structure of two major fractions.
several blue green algae and Chlorella. Prikladnaia Biohimiia i Kinetic studies on the alkaline cyclization of theunusual diad G2S
Mikrobiologiia 12: 196202. fi D(L)6S. Carbohydrate Research 340: 711722.

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