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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
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