Azolla meal as an alternative protein source in the diet of Etroplus suratensis

doi:10.21203/rs.3.rs-2889247/v1

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Azolla meal as an alternative protein source in the diet of Etroplus suratensis

https://doi.org/10.21203/rs.3.rs-2889247/v1

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An experiment of 60-days duration was conducted to evaluate the effect of plant protein source by replacing fish meal protein with Azolla meal protein on growth performance, feed utilisation, survival, enzymatic activity and cost-effective feed for Etroplus suratensis fingerling. The mean initial average weight of fish 5.48±0.015g was stocked in plastic troughs (60 L) at a stocking rate of 10 fishes per trough. Three diets were formulated by inclusion of AZM protein by replacing fish meal (FM) protein at 0 (control diet), 7.5, 15, and 22.5 level. Each diet was fed to three replicate group fish at the rate of 5% of the total fish biomass, daily for a period of 60 days. Etroplus suratensis fed with AZM 15% diet attained highest weight gain, specific growth rate, and average daily growth, protein efficiency ratio (p<0.05) and elevation in digestive enzyme activity. Fish fed with AZM 22.5% diet showed the best feed conversion ratio, Feed efficiency ratio, highest survival rate and cost-effective diet, there is no significant difference (p>0.05) observed. According to the finding of current study, Azolla meal can be candidate feed ingredient to replace fish meal without compromising growth performance.

Etroplus suratensis

growth

Azolla meal

enzymatic activity

cost-effective diet

Pearl spot Etroplus suratensis, also known as green chromide, is widely found in brackish water to freshwater and ecosystems in India and Sri Lanka (Rishi and Singh, 1982). Species having omnivorous feeding habit, easily adapted from brackish water to freshwater, tolerate high environmental stress, easy adapt to existing farming technology and having high demand as a food source and as ornamental fish. Global fish food consumption was increased at a rate of 3.1% per year from 1961 to 2018 on a per capita 20.5 kg. Aquaculture accounted 46% of the total production and 52% of fish for human consumption (FAO 2020). India has enormous potential for aquaculture activities. However, aquaculture industry facing some problems like outbreak of disease, feed cost fluctuations, and high investment because of the fish meal cost. Aquafeed industry is mainly depending on fish meal due to its major source of protein, amino acid profile, high nutrient digestibility, in feed formulation (Magouz et al., 2020). Nowadays, fish meal supply has been decreased in market due to the reduction of natural fishery resources. So, it important to replace the fish meal with incorporation of non-conventional aquatic plant protein sources that should reduce the cost of feed, in this regard, Azolla microphylla meal could be an alternative ingredient due to its higher productivity and nutritive value, which encompasses 13–30% of crude protein (dry weight basis), rich on essential amino acids, vitamins and minerals. These nutrients improve the digestive system, immune functions and high metabolic rates which increase the growth performance (Gangadhar et al., 2017; Dawood and Koshio, 2019; Volkmann et al., 2008; Panigrahi et al., 2014). It has also potential source of nitrogen (Biotech, 2004). Hence, based on the foregoing highlights the present study has designed to study the influence of cost-effective Azolla meal on growth and survival of Etroplus suratensis.

2.1. Experimental animals and design for feeding trial

Etroplus suratensis fingerlings were collected from Pulicat Lake, Thiruvallur district, Tamil Nadu. After collection, the fingerlings were transferred to the experimental site, treated with KMnO4 and conditioned for one week and fed with commercial feed. Average temperature recorded during the acclimation periods was 27.32 ± 0.075°C.

A 60-day feeding trial was carried out in plastic troughs (60 l capacity) at Pulicat Research Field Facility (PRFF), Pulicat an off-campus facility of Dr. M.G.R Fisheries College and Research Institute, Ponneri Tamil Nadu. With three replications, four dietary treatments were used: 0% (AZM0), 7.5% (AZM7.5), 15% (AZM15), and 22% of azolla inclusion (AZM22.5). Totally 120 numbers of pearl spot (5.48 ± 0.01 g) were equally distributed into twelve experimental troughs. The Etroplus suratensis fingerling fed at a rate of 5% of total average body weight of fish per day at 10:00 and 17:00 hrs. The excess feed was siphoned out after 2 hrs. feeding. Every fortnight, amount of feed adjusted accordingly to fish biomass.

2.2. Preparation of experimental diet

Dry Azolla meal was collected from the Erode, Tamil Nadu by using indiamart.com website. Other ingredients collected from the Directorate of Incubation and Vocational Training in Aquaculture Muttukadu, Tamil Nadu. Feed ingredients ground and sieved through 80 µ mesh. The control diet (0% AZM) was formulated without addition of Azolla meal and three treatment diets were formulated with inclusion of Azolla meal to replaced Fish meal at 7.5%, 15%, and 22.5% and designated as diet AZM7.5, AZM15 and AZM22.5. The ingredient composition of experimental diets is given in Table 1. The feed ingredient has been prepared by mixing and then extruded in the extruder through 2 mm die, after extruded feed has been dried in room temperature and then stored in air-tight packets.

Table 1

Ingredient composition of formulated feed
Ingredients	Percentage of inclusion
	Control (C)	AZM7.5%	AZM15%	AZM22.5%
Fish meal	15	10	5	0
Azolla meal	0	7.5	15	22.5
Corn gulten meal	12	13.5	15	17.5
Soybean meal	22	22	22	22
Corn flour	27	23	19	14
Cassava	3	3	3	3
Wheat	18	18	18	18
Pam oil	2	2	2	2
Vitamin Mineral premix	1	1	1	1
Total	100	100	100	100

2.3. Water quality parameter analysis

The water quality parameters such as temperature, pH, dissolved oxygen (DO), alkalinity, total hardness, nitrite, nitrate and ammonia were tested by standard methods of APHA (2005) on initial day and subsequently on the 6th day of the experimental period.

Fish Sampling and Growth Parameters

The fish growth parameter viz., weight gain, specific growth rate, food conversion ratio and food efficiency ratio were analysed following standard formula as described below:

$$\text{A}\text{v}\text{a}\text{r}\text{a}\text{g}\text{e} \text{d}\text{a}\text{i}\text{l}\text{y} \text{g}\text{r}\text{o}\text{w}\text{t}\text{h} \left(\text{A}\text{D}\text{G}\right) \left(\text{g}\right)=\frac{\text{F}\text{i}\text{n}\text{a}\text{l} \text{w}\text{e}\text{i}\text{g}\text{h}\text{t} – \text{i}\text{n}\text{i}\text{t}\text{i}\text{a}\text{l} \text{w}\text{e}\text{i}\text{g}\text{h}\text{t}}{\text{D}\text{a}\text{y}\text{s} \text{o}\text{f} \text{c}\text{u}\text{l}\text{t}\text{u}\text{r}\text{e} }$$

$$\text{M}\text{e}\text{a}\text{n} \text{w}\text{e}\text{i}\text{g}\text{h}\text{t} \text{g}\text{a}\text{i}\text{n} \left(\text{M}\text{W}\text{G}\right) \left(\text{g}\right)=\text{F}\text{i}\text{n}\text{a}\text{l} \text{b}\text{o}\text{d}\text{y} \text{w}\text{e}\text{i}\text{g}\text{h}\text{t}-\text{I}\text{n}\text{i}\text{t}\text{i}\text{a}\text{l} \text{b}\text{o}\text{d}\text{y} \text{w}\text{e}\text{i}\text{g}\text{h}\text{t}$$

$$\text{S}\text{p}\text{e}\text{c}\text{i}\text{f}\text{i}\text{c} \text{g}\text{r}\text{o}\text{w}\text{t}\text{h} \text{r}\text{a}\text{t}\text{e} \left(\text{S}\text{P}\text{G}\right) \left(\text{%}\right)=\frac{\text{L}\text{n} \text{F}\text{i}\text{n}\text{a}\text{l} \text{w}\text{e}\text{i}\text{g}\text{h}\text{t} – \text{L}\text{n} \text{I}\text{n}\text{i}\text{t}\text{i}\text{a}\text{l}}{\text{N}\text{o} . \text{o}\text{f} \text{d}\text{a}\text{y}\text{s}}\times 100$$

$$\text{F}\text{e}\text{e}\text{d} \text{C}\text{o}\text{n}\text{v}\text{e}\text{r}\text{s}\text{i}\text{o}\text{n} \text{R}\text{a}\text{t}\text{i}\text{o} \left(\text{F}\text{C}\text{R}\right)=\frac{\text{T}\text{o}\text{t}\text{a}\text{l} \text{f}\text{e}\text{e}\text{d} \text{g}\text{i}\text{v}\text{e}\text{n}}{ \text{w}\text{e}\text{i}\text{g}\text{h}\text{t} \text{g}\text{a}\text{i}\text{n} \text{o}\text{f} \text{f}\text{i}\text{s}\text{h} \left(\text{B}\text{i}\text{o}\text{m}\text{a}\text{s}\text{s}\right)}$$

$$\text{F}\text{e}\text{e}\text{d} \text{E}\text{f}\text{f}\text{i}\text{c}\text{i}\text{e}\text{n}\text{c}\text{y} \text{R}\text{a}\text{t}\text{i}\text{o} \left(\text{F}\text{E}\text{R}\right) =\frac{\text{B}\text{o}\text{d}\text{y} \text{w}\text{e}\text{i}\text{g}\text{h}\text{t} \text{g}\text{a}\text{i}\text{n} \left(\text{W}\text{e}\text{t} \text{w}\text{e}\text{i}\text{g}\text{h}\text{t}\right)}{\text{T}\text{o}\text{t}\text{a}\text{l} \text{f}\text{e}\text{e}\text{d} \text{g}\text{i}\text{v}\text{e}\text{n} \left(\text{D}\text{r}\text{y} \text{w}\text{e}\text{i}\text{g}\text{h}\text{t}\right)}$$

$$\text{P}\text{r}\text{o}\text{t}\text{r}\text{i}\text{n} \text{E}\text{f}\text{f}\text{i}\text{c}\text{i}\text{e}\text{n}\text{c}\text{y} \text{R}\text{a}\text{t}\text{i}\text{o} \left(\text{P}\text{E}\text{R}\right) =\frac{\text{W}\text{e}\text{t} \text{w}\text{e}\text{i}\text{g}\text{h}\text{t} \text{g}\text{a}\text{i}\text{n}}{\text{D}\text{r}\text{y} \text{w}\text{e}\text{i}\text{g}\text{h}\text{t} \text{o}\text{f} \text{p}\text{r}\text{o}\text{t}\text{e}\text{i}\text{n} \text{f}\text{e}\text{d}}$$

$$\text{S}\text{u}\text{r}\text{v}\text{i}\text{v}\text{a}\text{l} \text{R}\text{a}\text{t}\text{e} \left(\text{S}\text{R}\right)\left(\text{%}\right) =\frac{\text{N}\text{o}. \text{o}\text{f} \text{a}\text{n}\text{i}\text{m}\text{a}\text{l} \text{s}\text{u}\text{r}\text{v}\text{i}\text{v}\text{e}\text{d} \text{a}\text{t} \text{t}\text{h}\text{e} \text{e}\text{n}\text{d} \text{o}\text{f} \text{e}\text{x}\text{p}\text{r}\text{i}\text{m}\text{e}\text{n}\text{t}}{\text{N}\text{o}. \text{o}\text{f} \text{a}\text{n}\text{i}\text{m}\text{a}\text{l} \text{s}\text{t}\text{o}\text{c}\text{k}\text{e}\text{d} \text{a}\text{t} \text{t}\text{h}\text{e} \text{s}\text{t}\text{a}\text{r}\text{t} \text{o}\text{f} \text{e}\text{x}\text{p}\text{r}\text{i}\text{m}\text{e}\text{n}\text{t} } \times 100$$

2.4. Digestive Enzymes analysis

The lipase enzyme activity of intestinal tissue was assessed by the method of Cherry and Crandell (1932). Protease assay was done following the method of Kunitz (1947), which was adopted and described by Sumathi and Pattabiraman (1975) and amylase were estimated by Somogyi – Nelson method using 3, 5-dinitrosalicyclic acid (DNSA) (Bernfeld, 1955).

2.5. Statistical data analysis

One way analysis of variance (ANOVA) was used to determine differences between treatment means which were considered significant at (p < 0.05). Post-hoc analysis was done when significant differences were found between treatment means, using Duncan test used for significant difference. Analyses were performed using SPSS software version 16.0 for windows (SPSS Inc., Chicago, USA).

3.1. Water quality

Over the period of 60 days feeding trials, there is no significant difference (p > 0.05) was observed in the water quality parameters recorded Table 2, between the experimental treatments.

Table 2

Water quality parameters (Mean ± SE) recorded during the experimental period
Parameters	Control	AZM 7.5	AZM 15	AZM 22.5	P value
Temp (ºC)	27.42 ± 0.075 ^a	27.46 ± 0.008 ^a	27.42 ± 0.055 ^a	27.42 ± 0.064 ^a	0.934
DO	5.13 ± 0.60 ^a	5.33 ± 0.17 ^a	5.23 ± 0.03 ^a	5.23 ± 0.14 ^a	0.717
pH	7.76 ± 0.08 ^a	7.73 ± 0.14 ^a	7.7 ± 0.15 ^a	7.6 ± 0.05 ^a	0.775
Alkalinity	153 ± 1.20 ^a	152 ± 2.02 ^a	159 ± 3.21 ^a	150 ± 5.36 ^a	0.360
Hardness	184 ± 12.99 ^a	166 ± 5.84 ^a	171 ± 3.17 ^a	187 ± 4.93 ^a	0.250
Ammonia	0.07 ± 0.005 ^a	0.073 ± 0.003 ^a	0.06 ± 0.005 ^ab	0.05 ± 0.000 ^b	0.022
Nitrate	0.3 ± 0.115 ^a	0.06 ± 0.003 ^b	0.05 ± 0.003 ^b	0.07 ± 0.008 ^b	0.047
Nitrite	0.02 ± 0.010 ^a	0.02 ± 0.005 ^a	0.01 ± 0.005 ^a	0.02 ± 0.003 ^a	0.522
Values with different superscripts showed significant (P < 0.05) difference

3.2. Proximate composition of experimental diets

Proximate composition of the candidate ingredients and the experimental diets are shown in Tables 3 and 4.

Table 3

Proximate composition (%) of azolla meal and experimental diets
Ingredients	Fish meal	Azolla meal	Corn gluten meal	Soybean meal	Corn flour	Cassava	Wheat
Moisture	12.61	9.00	3.19	5.39	6.75	-	14.00
Protein	58.56	25.00	60.71	48.70	7.87	9.00	12.00
Crude Fiber	< 1	10.12	< 1	5.30	1.40	-	2.70
Total ash	19.04	10.50	1.55	7.46	1.69	-	2.30
Total fat	7.60	3.70	3.00	1.52	4.30	-	3.70

Table 4

Proximate composition feed
Ingredients	Control (C)	AZM7.5%	AZM15%	AZM22.5%
Moisture	8.10	6.70	6.20	5.30
Protein	30.26	30.09	30.33	30.00
Crude Fiber	6.00	8.00	10.00	12.00
Total ash	16.80	14.40	16.00	11.20
Total fat	3.30	3.50	3.00	0.50

3.3. Growth performance of Etroplus suratensis fed with azolla meal incorporated diets

The highest mean weight gain (MWG) of the fingerlings was observed in AZM15% incorporation (5.706 ± 0.008 g) followed by AZM7.5% (5.336 ± 0.006 g), AZM22.5% (4.91 ± 0.011 g) and control diet (2.740 ± 0.017 g). Specific growth rate (SGR) was found to be higher in AZM15% (1.188 ± 0.003) incorporated diet fed fish compared to AZM7.5% (1.132 ± 0.000), AZM22.5% (1.065 ± 0.003) and control diet (0.675 ± 0.004) fed fish. The maximum average daily growth (ADG) rate was observed in the fingerlings fed with AZM15% incorporates diet (0.095 ± 0.000 g) followed by AZM7.5% (0.088 ± 0.000 g), AZM22.5% (0.081 ± 0.000 g) and control (0.045 ± 0.000 g). The best feed conversion ratio (FCR) and feed efficiency ratio (FER) were observed in AZM22.5% incorporation (2.100 ± 0.160 and 0.481 ± 0.034) compared to 15% incorporation (2.161 ± 0.088 and 0.464 ± 0.018) and 7.5% incorporation (2.310 ± 0.089 and 0.434 ± 0.017). The FCR and FER value of control diet fed fish were 2.838 ± 0.135 and 0.354 ± 0.017, respectively. Survival rate (SR) was found to be lower (73.33 ± 3.33%) in control diet fed fish whereas highest SR (93.33 ± 6.66%) was noticed in 22.5% of azolla meal incorporated diet fed fish. MWG, SGR, ADG, PER of fingerlings were significantly differed (p < 0.05), at the same time, FCR, FER and SR of fish did not show the significant difference (p > 0.05) among all the AZM based experimental diets (Table 5)

Table 5

Growth performance and feed utilization of *Etroplus suratensis* fed experimental diets
Treatment	MIW	MFW	MWG (g)	SGR (%)	ADG (g)	FCR	FER	PER	SR (%)
0AZM	5.48 ± 0.015^a	8.22 ± 0.011^d	2.740 ± 0.017^d	0.675 ± 0.004^d	0.045 ± 0.000^d	2.838 ± 0.135^a	0.354 ± 0.017^b	0.090 ± 0.000^d	73.33 ± 3.33^b
7.5AZM	5.48 ± 0.008^a	10.82 ± 0.014^b	5.336 ± 0.006^b	1.132 ± 0.000^b	0.088 ± 0.000^b	2.310 ± 0.089^b	0.434 ± 0.017^a	0.174 ± 0.000^b	83.33 ± 3.33^ab
15AZM	5.48 ± 0.018^a	11.19 ± 0.020^a	5.706 ± 0.008^a	1.188 ± 0.003^a	0.095 ± 0.000^a	2.161 ± 0.088^b	0.464 ± 0.018^a	0.187 ± 0.000^a	86.66 ± 3.33^ab
22.5AZM	5.48 ± 0.014^a	10.39 ± 0.014^c	4.910 ± 0.011^c	1.065 ± 0.003^c	0.081 ± 0.000^c	2.100 ± 0.160^b	0.481 ± 0.034^a	0.162 ± 0.000^c	93.33 ± 6.66^a
P Value	0.991	0.000	0.000	0.000	0.000	0.10	0.019	0.000	0.067
Values with different superscripts differ significantly (p < 0.05) except feed conversion ratio, feed efficiency ratio and survival rate.

3.4. Enzymatic analysis

The enzymatic analysis of Etroplus suratensis fed with Azolla meal incorporated diets are given in Table 6, and Fig. 1. The higher amylase activity was observed in the fish fed with 15% inclusion of AZM diet. Significant difference (p < 0.05) observed between control and treatment. Higher protease activity (0.80 ± 0.87) was observed in the fed fish with 15% AZM incorporated diet fed fish compared to 7.5, 22.5% and control diet fed fish. Significant difference (p < 0.05) observed between AZM and control diet fed fish, however, there was no significant difference (p > 0.05) observed within the AZM treatment. Lipase activity was found to be significantly (p < 0.05) higher in 15% AZM inclusion diet fed fish compared to 7.5, 22.5% and control. At the same time, 7.5 and 22.5% incorporated diet fed fish showed the significant difference (p < 0.05) than control.

Table 6

Enzymatic activity analysis
Factors		Amylase (U mg -1 protein)	Protease (U mg -1 protein)	Lipase (U mg -1 protein)
Control		5.660 ± 0.559 ^b	0.513 ± 0.045 ^b	2.843 ± 0.111 ^g
Azolla	7.5	13.066 ± 0.426^a	0.782 ± 0.008 ^a	8.801 ± 0.064 ^a
	15	13.953 ± 0.342 ^a	0.806 ± 0.087 ^a	9.360 ± 0.097 ^b
	22.5	12.910 ± 0.811 ^a	0.714 ± 0.005 ^a	8.621 ± 0.065 ^b
P Value		0.000	0.011	0.000
Values with different superscripts showed significant (P < 0.05) difference

In the present study investigating that fish meal protein can be replaced with Azolla meal protein in diets of Etroplus suratensis fingerlings at 7.5, 15, and 22.5% inclusion levels without compromising growth performances and feed efficiencies. In this study Azolla fed Etroplus suratensis fingerling showed significantly higher (p < 0.05) mean weight gain, SGR, ADG, PER, SR than the control diet fed fishes, similar reports were observed by Joseph et al. (1994) in Etroplus suratensis. The highest mean weight gain of 5.706 ± 0.008 g was observed in the fingerling fed with 15% Azolla incorporated diet. The mean weight gain observed in the control fish was only 2.740 ± 0.017 g. The finding of the present study agreed with the results of Magouz et al. (2020) who reported that inclusion level upto 20% Azolla improved growth performance of Oreochromis niloticus. In the present study highest Azolla incorporation in the feed was 22.5% and the fishes showed lower growth performance than the other concentrations, which reveals that increasing more than 20% may not yield fruitful result. This was also confirmed by Joseph et al. (1994) who observed lower growth performance and food conversion with increasing Azolla incorporation in the diet of Etroplus suratensis. Similar results were observed in Oreochromis niloticus by Ebrahim et al. (2007). The reason for the poor performance of higher concentration may probably be due to the lowering protein digestibility of this fern, as mentioned by Leonard et al. (1998) in Oreochromis aureus. Also, the poor performance of Tilapia zillii fish fed high levels of Azolla meal on diets might be contributed with the deficiency of some essential amino acids especially methionine, lysine and histidine, as well as the high neutral detergent fiber of Azolla as reported by Buckingham et al. (1978) and Cole and Van Lunen (1994). In the present study, 15% incorporation of Azolla meal fed fish showed highest amylase, protease and lipase enzyme activity. Between dietary treatment and control there is significant difference (p < 0.05) observed except lipase enzyme activity. Growth performance of the fishes were associated with the digestibility of nutrient and feed efficiency. The present study was supported by Sithara and Kamalaveni (2008) who’s reported that higher levels of Azolla inclusion in the diet of Oreochromis niloticus affect digestive enzyme activity. Similar results were also observed by Hong et al. (2004) in the diet of Oreochromis niloticus. Based on the growth performance of the experimental trials, the Azolla meal at 22.5% incorporation showed cost effective feed for Etroplus suratensis as compared to other diets. Similar kind of result reported by El-Sayed (1992) reported that replacing fish meal by substitution of Azolla meal at 25% showed cost effective for Oreochromis niloticus. Similarly, Fiogbe et al., 2004 reported that Azolla meal at 20% incorporation showed cost effective for Oreochromis niloticus. Ebrahim et al. (2007) reported that incorporation of Azolla meal decreased the feed cost in Oreochromis niloticus.

The present study concludes that incorporation of azolla upto 15% in diet of E. suratensis fingerlings gives higher weight gain, specific growth rate, average daily growth, protein efficiency ratio and digestive enzyme activities. Azolla inclusion in feed preparation results in cutting on feed cost.

Dear editor / Reviewer

Please note that the manuscript does not need an ethical approval, you are therefore kindly requested to consider the manuscript.

Authors contributions

Sumit Gaidhane- performed experiment and drafted the article, prepared figures and tables.

Dr.B.Ahilan- designed the experiment and reviewed the manuscript.

P.Chidambaram- reviewed the manuscript.

N. Jayakumar– analysed and data interpreted the data.

Funding

Tamil Nadu Dr.J.Jayalalithaa Fisheries University- Dr. M.G.R Fisheries College and Research Institute provided the funds and all the necessary facilities to carry out this study.

Availability of Data and materials

The data used to support the finding are all included in the article.

Acknowledgements

The authors wish to extend their gratitude to Dr. M.G.R Fisheries College and Research Institute, ponneri (Dr. M.G.R FC and RI) off campus pulicat research field facility, Pazhverkadu, research centre. Tamil Nadu Dr. Jayalalithaa Fisheries University (TNJFU) for provision of space, equipment, supply of feed ingredients and preparation of experimental feed for this study.

Competing of interest

The author declare no competing interests.

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Azolla meal as an alternative protein source in the diet of Etroplus suratensis

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Abstract

Figures

1.0. Introduction

2.0. Materials and Methods

2.1. Experimental animals and design for feeding trial

2.2. Preparation of experimental diet

Fish Sampling and Growth Parameters

2.4. Digestive Enzymes analysis

2.5. Statistical data analysis

3.0. Results

3.1. Water quality

3.2. Proximate composition of experimental diets

3.4. Enzymatic analysis

4.0. Discussion

5.0. Conclusion

Declarations

References

Additional Declarations

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