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Chapter 6 BIOCHEMICAL CHARACTERIZATION AND PIGMENT PROFILE OF EUGLENA AND ITS USE AS FEED IN SOME INDIGENOUS FISHES OF CACHAR DISTRICT (ASSAM)

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Page 1: BIOCHEMICAL CHARACTERIZATION AND PIGMENT PROFILE OF …shodhganga.inflibnet.ac.in/bitstream/10603/21978/11/11_chapter 6.p… · The pigments are characteristic of certain algal groups

Chapter 6

BIOCHEMICAL CHARACTERIZATIONAND PIGMENT PROFILE OF EUGLENAAND ITS USE AS FEED IN SOMEINDIGENOUS FISHES OF CACHARDISTRICT (ASSAM)

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BIOCHEMICAL CHARACTERIZATION AND PIGMENT PROFILE OF

EUGLENA AND ITS USE AS FEED IN SOME INDIGENOUS FISHES OF

CACHAR DISTRICT (ASSAM)

6.1 Introduction

The pigments are characteristic of certain algal groups. Four different kinds of pigments that are

usually found in algae are chlorophyll, carotenes, xanthophylls and phycobilins but in Euglena is

devoid of phycobilins pigments. Of the other three kinds, chlorophyll a, chlorophyll b, carotene,

-carotene, zeaxanthin, flovoxanthin, flavicin are common pigment in Euglena.

Chlorophyll and carotenes are fat soluble molecules and are extracted from thylakoid membranes

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with the help of organic solvents such as acetone, methanol, etc. but phycobilins and peridinin

are water soluble that can be extracted from algal tissues after the organic solvent extraction of

chlorophyll from those tissues. In some cases, red colouration in the water occurs due to the

increase in presence of characteristic xanthophyll pigment called astaxanthin or euglenorhodone

or hematochrome. Cunningham and Schiff (1986a) found that Euglena contains xanthophyll

pigments diadinoxanthin and diatoxanthin but lutein, fucoxanthin and violaxanthin are not

present. Casper-Lindley and Bjorkman (1998) observed at high light intensities Euglena lacked

xanthophylls pigment. The definition of photosynthetic pigments that cause light energy to turn

into chemical energy in all photosynthetic organisms was first determined by Stokes (1864).

Sorby (1873) classified blue chlorophyll as chlorophyll a, green chlorophyll as chlorophyll b and

orange-yellow as xanthophyll according to the pigment colors. Chlorophyll is a key biochemical

component in the molecular apparatus that is responsible for photosynthesis. Chlorophyll is a

metal-chelate, or a central magnesium ion is bonded to a larger organic molecule called a

porphyrin. The porphyrin molecule is composed tetrapyrrole units joined vinylic groups. The

magnesium ion is the centre of electron transfer during photosynthesis (Fig. 6.1). The content of

chlorophyll a relating to the pigment level is almost the same in all algal groups but chlorophyll

b and c changes(Donkin, 1976; Martin et al., 1991; and Grung et al., 1992). Carotenoids are

naturally occurring fat soluble pigments that are responsible for the different colours of algae

(Ben-Amotz and Fishler, 1998). Carotenoids are usually yellow to red and present in green,

yellow, leafy vegetables and in yellow fruits. They are aliphatic hydrocarbons consisting of

polyisoprene backbone. Pigmentation in Euglenophyta is found to be due to the presence of

carotenoids such as carotene, zeaxanthin, neoxanthin and diadinoxanthin (Goodwin, 1976; Kirk

and Tilney-Bassett, 1978). Rosowski and Parker (1982) found the presence of zeaxanthin, lutein,

violaxanthin and neoxanthin in euglenophyceae. Earlier it was found that secondary carotenoids

such as ketocarotenoids of xanthophylls were associated with chlorophyceae (e.g., green algae),

but then it had been encountered in euglenophyceae. The role of carotene pigments in algae is

not exactly known but it is suggested that they function as a passive light protecting filter and

have the role of accessory pigments transferring energy and oxygen (Lichtenthaller, 1987; Yong

and Lee, 1991 and Bidigare et al., 1993). In Euglena, carotenoids are found to play a major role

in protecting chloroplasts against photosensitized oxidation (Bamji and Krinsky, 1965). Vechetel

et al., (1992) determined that carotene pigments are the most important photosynthetic pigments

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and it prevents chlorophyll and thylakoloid membrane from the damage due to photo-oxidation.

Carotenoids contain a conjugated double bond system of the polyene type (C-C=C-C=C). Energy

absorbed by carotenoids are transferred to chlorophyll a for photosynthesis.

Fig. 6.1: Molecular structure of chlorophyll

Various studies have indicated that carotenoids may prevent or inhibit certain types of cancer,

arthrosclerosis, age-related muscular degeneration and other diseases. At sufficiently high

concentrations, carotenoids can protect lipids from peroxidative damage (Burton, 1984).

Carotenoids have antiproliferative effect on various cancer cell lines; lycopene has been shown

- Carotene has been

shown to inhibit the expression of antiapoptotic protein Bcl-2 in cancer cells, thus reducing the

growth of cancer cells (Karas, 2000). Paramylum is the characteristic carbohydrate reserve of the

Euglenophyta (Braas and Stone, 1968) which is similar to starch. It accumulates when Euglena

are grown on an organotrophic medium in the dark and is consumed either in the dark when cells

receive or at the end of the exponential growth phase (Freyssinet et al., 1972) or when cells are

transferred to the light (Dwyer and Smillie, 1970; Dwyer and Smillie, 1971; Freyssinet 1972;

Schwartzbach et al.,1975). The chloroplasts found in Euglena contain chlorophyll which aid in

the synthesis of carbohydrates is stored as starch granules and paramylon. In Euglena paramylon

is made in the pyrenoids. The eugenoids have chlorophylls a and b and they store their

photosynthate in an unusual form called paramylon starch, a B-1, 3 polymer of glucose. The

paramylon is stored in rod like bodies throughout the cytoplasm. These are called paramylon

bodies and are often visible as colorless or white rigid rods (Calvayrac, 1981). Protein or amino

acids are the by-products of an algal process for the production of other fine chemicals, or with

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appropriate genetic enhancement, microalgae could produce desirable amino acids in sufficiently

high concentrations (Borowitzka, 1988). The high protein content of various algae species is one

of the main reasons to consider them as an unconventional source of protein (Soletto et al.,

2005). Euglena is an organism with a number of interesting characteristics. It has three, rather

than two membranes surrounding its chloroplasts (Gibbs, 1978) which have implications for the

targeting of nuclear-encoded chloroplast proteins. It is a popular flagellated laboratory

microorganism found in freshwater environments (Buetow et al., 1982). It represents one of the

simplest and earliest derived eukaryotic cells. The production of variety of extracellular

substances plays an important role in growth, physiology and ecosystems of algae. Extracellular

products which are liberated from Euglena contain lot of nitrogenous substances.

Producer Product group Application

Euglena ( - carotene) Carotenoids Pigments, cosmetics,

Pro-vitamins

Euglena gracilis Vitamin C and vitamin E Nutrition

-tocopherol, ascorbic acid)

Algal blooms are often disastrous in aquatic bodies and particularly in fish ponds due to the

addition of fertilizers it causes eutrophication and alter the quality of water which results into

fish mortality (Padmavathi, 2007). Most of the works deals with the physico-chemical

parameters operating in a particular water body while some workers have discussed about the

distribution of unicellular and colonial organisms. In 2000, Hosmani and Vasanth work on the

biochemical aspects of water pollution in two lakes of Mysore city. Rahman et al., (2007)

studied on Euglena bloom and its impact on fish growth. They correlated the water quality in the

bloomed ponds with fish growth and found that bloom had a negative effect on fish growth.

Though they did not analyze the gut contents of the fishes inhabiting the same ponds. Most

researches on fish growth are based on impact of water quality on fish growth (Vas, 2006;

Sugunan et al., 2006)

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So far biochemical aspects of algae have received less attention in natural habitats of freshwater

ecosystems (Gatenby et al., 2003). The present chapter embodies the results of investigation on

the biochemical potential and pigment profile of Euglena tuba. Also included in this chapter

some informations on intake of Euglena tuba by the indigenous fishes to explore its innate

potential as fish feed.

6.2 Methodology

For the biochemical characterization and pigment profile analysis, all the 16 ponds were

selected and algal samples were collected bimonthly from July-2009 to May- 2010. Euglena

intake information was obtained by analyzing the guts of some indigenous fish variety.

Informations pertaining to the fish kill was obtained by interaction with the local people through

a structured questionnaire. The detail methodology pertaining to the work described in this

chapter has already been discussed in Chapter 3.

6.3 Results and Discussion

6.3.1 Pigment profile of Euglena tuba

Pigment concentration and biochemical properties are largely dependent upon the type of algae.

Euglena that grows at different light intensities show remarkable changes in their chemical

composition, pigment content and photosynthetic activity (Guschina and Harwood, 2005).

Chlorophyll a, b and carotenoids are fat soluble pigment. Table 6.1 shows characteristics of

different photosynthetic pigments. In general, carotenoid was found highest in almost all the

ponds (Fig.6.2 - 6.17) except Madhuraghat, Dudhpatil, Udarband, Barjalenga and Sonai.

Chlorophyll b was always lower than other pigments. In Arkatipur, Chlorophyll a (7.18µg/ml)

and b (0.85µg/ml) were highest in March. Both chlorophyll and carotenoids were low in July.

The chlorophyll a is an index of water quality and phytoplankton biomass (James and Head,

1972; Papista et al., 2002; Desortova, 1981; Canfield et al., 1985; Voros and Padisak, 1991).

Carotenoid gradually increased from the month of July then decreased with a fall in May. While

chlorophyll a was found to be more or less stable. During March and May, in Baskandi

carotenoid showed heavy fluctuation with its lowest concentration in January (2.5µg/ml) when

chlorophyll b was highest (0.9µg/ml). In Karikandi, carotenoid was found to increase initially

from the month of July to November with a sudden fall in January then gradually increased

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towards May. A decrease in chlorophyll a concentration from 6.0µg/ml to 3.5µg/ml was noticed

in the month of May. In Machpara, chlorophyll a and carotenoid shown a similar trend from July

to May while chlorophyll b has a fall from November to May. Carotenoid concentration fell

down to its lowest point in March (2.3µg/ml) then again increased in May (8.6 µg/ml) in

Kashipur while chlorophyll a did not differ much in its concentration. In Bagpur, lowest

carotenoid was observed in July (2.5 µg/ml) when both chlorophyll a and b were highest (9.3

µg/ml and 0.5 µg/ml). Chlorophyll b was greatly fluctuating in Madhuramukh pond with its

highest value (0.5µg/ml) in May when carotenoid was lowest (3.3µg/ml). In Madhuragha,t

chlorophyll a was higher than the carotenoid from the month of November. Increase in

chlorophyll a (9.5 µg/ml) is followed by decrease in carotenoid in March (2.0µg/ml).

Chlorophyll b gradually increased from September (0.1 µg/ml) to March (0.3µg/ml) then fell

down in May (0.1µg/ml). Increases in chlorophyll a concentration in the water and pH is related

to Euglena density whereas oxygen concentration changes are related to the changes in the

density of euglenophytes (Pereira et al., 2001). Chlorophyll b had its peak in January in

Dudhpatil. In this pond chlorophyll a was always higher than the carotenoid. The high level of

antioxidant property in Euglena species is contributed by the fact that it contains carotenoid

pigment. Carotenoid pigment is a potent radical scavenger and singlet oxygen quencher

(Gouveia, 2008). Carotenoids are known to posses antioxidative properties (Di Mascio et al.,

1991, Kobayashi et al., 1997, Fang et al., 2002). The antioxidant activity of carotenoids arises

primarily as a consequence of the ability of the conjugated double-bonded structure with

delocalize electrons (Mortensen, 2001). This is primarily responsible for the excellent ability of

-carotene to physically quench singlet oxygen without degradation and for the chemical

-carotene with free radicals such as the peroxyl, hydroxyl and superoxide radicals.

In Durgabari, carotenoid was lowest in September (1.21µg/ml) and highest in May (10.87µg/ml)

when chlorophyll a and b reached it’s lowest. Euglenophytes (Euglena) made up more

chlorophyll a than diatoms, chlorophytes and especially cyanobacteria (Reynolds, 1984, Pereira

et al., 2001). Carotenoid was found to be more or less stable from July (2.11µg/ml) to November

(2.05µg/ml) then decrease then increased again in Udarband. In Silcoorie, chlorophyll b was

found to be lowest in September (0.09µg/ml) while highest in March (0.45µg/ml) which

decrearses again in May (0.32µg/ml). Generally, higher chlorophyll a concentration translate

into higher individual cell counts and biomass of phytoplankton, though not always, as not all

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algal cells produce equal amounts of chlorophyll a (Felip and Catalan, 2000). In Dargakona,

highest chlorophyll a (11.97µg/ml) and b (0.67µg/ml) was followed by lowest carotenoid

(0.99µg/ml) in March. The pigment chlorophyll a, b and carotenoid were found to be fluctuating

from July to May in Irangmara pond. Chlorophyll a (9.54µg/ml) and b (0.32µg/ml) were highest

in Jaunary when carotenoid (3.12µg/ml) was lowest in Barjalenga. In Sonai, chlorophyll a

increased gradually from the month of July than decreased in May. Cunningham and Schiff

(1986) mentioned that the amount of chlorophyll b was relatively lesser than chlorophyll a.

6.3.2. Biochemical characterization of Euglena tuba

In general Carbohydrate concentration was found to be more than the protein content of the

species. Euglena gracilis is reported to have high protein content Chae et al. (2006). Algal cell

mainly made up of proteins, carbohydrates, fats and nucleic acids in varying proportions but their

percentages can vary with the type of algae, some types of algae are made up of up to 40% fatty

acids based on their overall mass. It is this fatty acid that can be extracted and used as biofuel

(Gross, 2009). Fig.(6.18 -6.33) show variation of carbohydrate and protein concentrations in

each pond ecosystem. In Arkatipur Carbohydrate was higher in all the months except March

when protein (102.94µg/ml) was higher than the carbohydrate(97.23µg/ml) concentration. In

Baskandi, Karikandi, Machpara, Kashipur, Bagpur, Madhuramukh, Madhuraghat, Dudhpatil,

Udharband, Silcoorie, Irangmara and Sonai carbohydrate concentration was always higher than

the protein value. While in other ponds such as Durgabari, Dargakona and Barjalenga

fluctuations in carbohydrate and protein concentrations were observed in between the months.

Pigment concentrations most essentially the chlorophyll a concentration of a species which is a

measure of biomass is associated with all other biochemical parameters. Statistical analysis of

the pigments and biochemical properties of Euglena tuba (Table 6.2) showed a significant

negative correlation (p a and Carotenoid pigment. Higher Chlorophyll

a pigment was associated with higher carbohydrate and protein value (p

Euglena tuba was found to be rich in macro and micronutrient concentrations (Table 6.3-6.4).

Among three major macronutrients nitrogen showed high value (2.0%) followed by phosphorus

(0.32%) and least value was observed in potassium (0.3%). For micronutrients high value was

found in manganese (1178 mg/kg) which was much more as compared with other nutrient

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followed by iron (89.6 mg/kg). Zinc concentration was recorded as 75.9 mg/kg and least value

was found for copper (3.5 mg/kg).

6.3.3 Euglena intake by indigenous fishes

Euglena tuba is a dominant unicellular alga in the fishery ponds of Cachar district. Euglena sp.

are known to reduce significantly other groups of algae (Hosmani, 1988). In our study dissolved

oxygen content never reached below 5 mg/l (Chapter- 4) level providing a favorable

environment for the fish survival. Blooms are known to deplete oxygen level in the aquatic body

causing huge fish mortality but in our study Euglena tuba blooms were not found to be harmful

for the fish growth rather they found to provide ample amount of oxygen to the environment by

the process of photosynthesis. This finding also derive support from earlier work by Brunson et

al. (1994). The district has not yet been reported to have any fish kill event due to such bloom.

Though more than 75% of freshwater fishes feed on plankton in their different stages of life

cycle (Jafri et al., 1999) and despite rich availability of the Euglena tuba in fishery ponds

application of the alga as fish feed is uncertain. Lu et al. (2004) also reported that larval tilapia

Oreochromis niloticus ingested significantly less Euglena gracilis but the ingestion was higher

than the Chlorella vulgaris. Fishes include (Plate 6.1) Darkina (Esomus danricus), Jati puti (

Puntius sophore), Chepta puti ( Puntius conchonius), Puta (Puntius sarana),

Japani(Cyprinus carpio), Goroi(Chana punctatus), Moka (Amblypharyngodon mola), Ghoria

(Labeo goria), Rohu (Labeo rohita), Puti(Puntius ticto) and Chandhowa (Chanda nama ). The

gut contents of the fishes from the heavily bloomed ponds were analyzed (Plate 6.2) and a very

low number of Euglena could be encountered in these 11 indigenous fish varieties. However Das

et al. (2009) mentioned that intake of Euglena viridis powder in Rohu increases its immunity and

makes Labeo rohita more resistant to Aeromonas hydrophila. Despite the huge abundance of

Euglena tuba in the studied pond ecosystems, food choice of the fishes might be another factor

for reducing the intake of the particular alga in their diet. Irrespective of the food selection and

consumption of the fishes Euglena tuba was found to have rich carbohydrate and protein content

which might have a potential to increase the food value of the same. High nutritive value of

Euglena tuba opens a new area where a future prospect occurs in formulation of the fish feed by

blending Euglena tuba powder according to the fish food habit that may increase the food

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selection and consumption rate of the fishes which would help in high and healthier growth rate

of the fishes on commercial basis.

6.4 Conclusion

In general, for all the ponds carotenoid concentration was higher than the chlorophyll a and

chlorophyll b pigments except Madhuraghat, Dudhpatil, Udharband, Barjalenga and Sonai with

prominent bimonthly pigment fluctuations. Carotenoid pigment was rich and found to be

dominant over the chlorophyll a and b pigments and was found to have significant negative

correlation (p with chlorophyll a. Higher algal biomass in terms of chlorophyll a was

associated with higher carbohydrate and protein value (p Higher concentrations of macro

and micronutrients in the species may have attributed to higher amount of proteins and

carbohydrate metabolism. Thus Euglena tuba with its well balanced nutrients may pave a new

way towards the fish food formulations which would ultimately increase the commercial output

of the fishery ponds.

Table 6.1: Characteristics of photosynthetic pigments

Pigment Color Soluble in

Chlorophyll a Bluish green Fat soluble

Chlorophyll b Yellowish green Fat soluble

Carotene Orange Fat soluble

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Table 6.2: Correlation between pigments and biochemical properties of Euglena tuba.

Table 6.3: Macro-nutrient content in Euglena tuba

Nutrient Percentage (%)

Total Nitrogen (N) 2.07

Total Phosphorus (P) 0.317

Total Potassium (K) 0.30

Table 6.4: Micronutrient concentration of Euglena tuba

Trace metal Concentration (mg/kg)

Iron (Fe) 89.6

Manganese (Mn) 1178.4

Zinc (Zn) 75.9

Cupper (Cu) 3.5

Correlations

1 .384** -.494** .771** .726**.000 .000 .000 .000

96 96 96 96 96.384** 1 .071 .162 .184.000 .493 .115 .072

96 96 96 96 96-.494** .071 1 -.525** -.458**.000 .493 .000 .000

96 96 96 96 96.771** .162 -.525** 1 .633**.000 .115 .000 .000

96 96 96 96 96.726** .184 -.458** .633** 1.000 .072 .000 .000

96 96 96 96 96

Pearson CorrelationSig. (2-tailed)NPearson CorrelationSig. (2-tailed)NPearson CorrelationSig. (2-tailed)NPearson CorrelationSig. (2-tailed)NPearson CorrelationSig. (2-tailed)N

Chlorophylla

Chlorophyllb

Carotenoid

Protein

Carbohydrate

Chlorophylla Chlorophyllb Carotenoid Protein Carbohydrate

Correlation is significant at the 0.01 level (2-tailed).**.

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Fig. 6.2: Variation of photosynthetic pigments of Euglena tuba in Arkatipur pond

Fig. 6.3: Variation of photosynthetic pigments of Euglena tuba in Baskandi pond

Fig. 6.4: Variation of photosynthetic pigments of Euglena tuba in Karikandi pond

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Fig. 6.5: Variation of photosynthetic pigments of Euglena tuba in Machpara pond

Fig. 6.6: Variation of photosynthetic pigments of Euglena tuba in Kashipur pond

Fig. 6.7: Variation of photosynthetic pigments of Euglena tuba in Bagpur pond

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Fig. 6.8: Variation of photosynthetic pigments of Euglena tuba in Madhuramukh pond

Fig. 6.9: Variation of photosynthetic pigments of Euglena tuba in Madhuraghat pond

Fig. 6.10: Variation of photosynthetic pigments of Euglena tuba in Dudhpatil pond

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Fig. 6.11: Variation of photosynthetic pigments of Euglena tuba in Durgabari pond

Fig. 6.12: Variation of photosynthetic pigments of Euglena tuba in Udarband pond

Fig. 6.13: Variation of photosynthetic pigments of Euglena tuba in Silcoorie pond

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Fig. 6.14: Variation of photosynthetic pigments of Euglena tuba in Dargakona pond

Fig. 6.15: Variation of photosynthetic pigments of Euglena tuba in Irangmara pond

Fig. 6.16: Variation of photosynthetic pigments of Euglena tuba in Barjalenga pond

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Fig. 6.17: Variation of photosynthetic pigments of Euglena tuba in Sonai pond

Fig. 6.18: Variation of biochemical parameters in Arkatipur pond

Fig. 6.19: Variation of biochemical parameters in Baskandi pond

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Fig. 6.20: Variation of biochemical parameters in Karikandi pond

Fig. 6.21: Variation of biochemical parameters in Machpara pond

Fig. 6.22: Variation of biochemical parameters in Kashipur pond

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Fig. 6.23: Variation of biochemical parameters in Bagpur pond

Fig. 6.24: Variation of biochemical parameters in Madhuramukh pond

Fig. 6.25: Variation of biochemical parameters in Madhuraghat pond

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Fig. 6.26: Variation of biochemical parameters in Dudhpatil pond

Fig. 6.27: Variation of biochemical parameters in Durgabari pond

Fig.6.28: Variation of biochemical parameters in Udarband pond

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Fig.6.29: Variation of biochemical parameters in Silcoorie pond

Fig.6.30: Variation of biochemical parameters in Dargakona pond

Fig. 6.31: Variation of biochemical parameters in Irangmara pond

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Fig.6.32: Variation of biochemical parameters in Barjalenga pond

Fig. 6.33: Variation of biochemical parameters in Sonai pond

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Plate 6.1: Some of the indigenous fish varieties (whose gut analysed) from different ponds

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Plate 6.2: Optical micrographs of Euglena tuba obtained from guts of fishes