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Dietary inclusion of non-conventional palm kernel meal enhances growth,

digestive enzyme activities and carcass characteristics of juvenile rohu (Labeo
rohita)

Article in Aquaculture Reports · October 2020

DOI: 10.1016/j.aqrep.2020.100502

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 Aquaculture Reports 18 (2020) 100502

Contents lists available at ScienceDirect

Aquaculture Reports
journal homepage: www.elsevier.com/locate/aqrep

Dietary inclusion of non-conventional palm kernel meal enhances growth,

digestive enzyme activities and carcass characteristics of juvenile rohu
(Labeo rohita)
S. Sangavi a, Paramita Banerjee Sawant a, *, Muralidhar P. Ande b, Karthireddy Syamala b, N.
K. Chadha a
a
Division of Aquaculture, ICAR- Central Institute of Fisheries Education, Versova, Mumbai, 400061, Maharashtra, India
b
Division of Aquaculture, ICAR- Central Institute of Fisheries Education, Kakinada Centre, Kakinada, 533001, Andhara Pradesh, India

A R T I C L E I N F O A B S T R A C T

Keywords: A 60-day feeding trial was performed to test the nutritional value and utilization possibility of palm kernel meal
Enzyme activities (PKM) as a feed ingredient for juvenile Labeo rohita. Five iso-nitrogenous diets were prepared with various in­
Growth performance clusions of PKM which replaced sunflower oil cake and de-oiled rice bran namely, control (without PKM), T1 (50
Palm kernel meal
g/kg PKM), T2 (100 g/kg PKM), T3 (150 g/kg PKM) and T4 (200 g/kg PKM). The experiment was conducted in
Plant feed ingredient
350 L fibre reinforced plastic tanks in triplicate and each tank stocked with twenty-five juvenile rohu (7.2 ± 0.01
Rohu
g) were fed twice daily at 5% of body weight with the experimental diet. The growth performance values showed
a higher overall linear trend in T2 and it is significantly different from control as well as T1 groups. Final results
showed highest average body weight, specific growth rate, protein efficiency ratio, and apparent net protein
utilization in a dose-dependent manner (p < 0.05). Significantly higher amylase, protease, and lipase activities
were recorded in T2 treatment (p = 0.003, p = 0.001 and p = 0.002, respectively). Additionally, dietary PKM
significantly lowered the aspartate amino transferase, alkaline amino transferase and alkaline phosphatase
enzyme activities in a dose-dependent manner (p < 0.05). Significantly higher lactate dehydrogenase, malate
dehydrogenase, superoxide dismutase and catalase activities in the liver tissues were recorded in T4 (p = 0.004,
p = 0.01 and p = 0.02 and p = 0.001, respectively). Based on the polynomial regression analysis, the PKM
inclusion at 26.17–100.11 g/kg can be effectively used in the diet of juvenile L. rohita as a non-conventional
growth-promoting feed ingredient without any harmful effects on its growth performance and physiological
activities.

1. Introduction among the feed industry (El-Sayed, 1999) to reduce the feed cost. PKM
(Palm Kernal Meal) is an agricultural by-product of the oil palm (Elaeis
The global fish production in the year of 2016 had reached 170.9 guineensis Jacq.) industry and is considered as an agro-industrial waste
million tonnes, of which 79.1 million tonnes fish comes from aquacul­ (Ng and Chong, 2002). This meal is produced from the oil palm fruit
ture, and this sector is growing at an average annual growth rate of 6.6 kernels, after the extraction of palm kernel oil. The global production of
% since 1995 (SOFIA, 2018). In the future, this sector is going to play a PKM is steadily increasing due to immense growth in oil palm industry
vital role in providing protein-rich food (fish) to the protein starving with 7 million metric tonnes (Kim et al., 2016). PKM is considered a
world. However, the intensified production methods, coupled with well-established feed for ruminants and contains valuable dietary
excessive use of fish meal in feed, are threatening the aquaculture as well sources of protein, amino acids, energy, and fiber. At lower incorpora­
as the aqua-feed industry. Thus, urged the researchers to use conven­ tion levels, it has proven to be a successful feed ingredient in poultry and
tional plant sources as a feed ingredient which was on the other side swine diets (Ng, 2003). At present, agro-industry by-products are gain­
increased the feed cost. Therefore, recently, the trend on formulating ing importance due to their nutritional composition, lower price, and
aqua-feed with non-conventional feedstuffs is getting momentum readily usable after reprocess. Besides, they are not fully utilized in

* Corresponding author.
E-mail address: [email protected] (P.B. Sawant).

https://doi.org/10.1016/j.aqrep.2020.100502
Received 13 May 2020; Received in revised form 21 September 2020; Accepted 23 September 2020
Available online 14 October 2020
2352-5134/© 2020 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
S. Sangavi et al. Aquaculture Reports 18 (2020) 100502

aqua-feed preparation, due to lack of information on the method of respectively, replacing sunflower oil cake and de-oiled rice bran to
production and commercialization and the presence of anti-nutritional balance the nutritional composition of the diet. Other ingredients such
factors and their detoxification methods. On the other side, there are as soybean meal, groundnut oil cake, wheat flour, corn flour were
several researchers have attempted to incorporate PKM as a feed included at appropriate levels in all the diets (Table 1). Carboxymethyl
ingredient in the diets of Oreochromis niloticus (Omoregie and Ogbe­ cellulose (CMC) was used as binder and these ingredients were mixed in
mudia, 1993), Labeo senegalensis (Omoregie, 2001), Red hybrid tilapia predetermined proportions with water to make a dough which was then
(Ng et al., 2002; Ng and Chong, 2002), hybrid C. macrocephalus × steam cooked for 20 min in a pressure cooker at 15 psi. After cooling, oil
C. gariepinus (Ng and Chen, 2002), Red tilapia (Iluyemi et al., 2010), Nile and vitamin-mineral mixture and butylated hydroxyl toluene (BHT)
tilapia juveniles (Carvalho et al., 2012), Clarius gariepinus (Udo et al., were added equally in all the diets. Subsequently, the glutinous dough
2012), sex reversed Nile tilapia (Thongprajukaew et al., 2015) and mixture was subjected to a hand pelletizer (die of 2 mm diameter) to
O. niloticus (Adjanke et al., 2016). However, the level of PKM incorpo­ prepare pellets of the required size. Finally, the pellets were dried by air,
ration in the fish diet varies among species. In India, carp culture followed by oven drying at 60 ◦ C for 48 h, and then stored at 4 ◦ C until
dominated by rohu (Labeo rohita) and catla (Catla catla), forms the further use in feeding.
strength of the freshwater aquaculture practice (Laxmappa, 2015).
Among Indian major carps, Rohu (Labeo rohita) is the highly preferred 2.2. Experimental setup and rearing
species, and it is also commonly cultured in other Asian countries,
especially in Indian sub-continent (Khan et al., 2004). With the above The study followed a completely randomized design, and the
background pointing towards the efficacy of PKM in fish diets, the experiment was conducted in 15 FRP tanks (350 L capacity) where each
present study has been conducted to illustrate the possibility of inclusion treatment were triplicated. A total of twenty-five fish (initial average
of PKM in the diet of juvenile L. rohita. weight 7.2 ± 0.01 g) were randomly stocked in each distinct experi­
mental tank (containing 300 L of water) and fed twice in a day (08:00
2. Materials and methods and 17:00 h) upto satiation level, during the experimental trial period of
60 days. The tanks were siphoned in alternate days for removal of fecal
2.1. Diet formulation and preparation matter to avoid contamination of water.
Water quality parameters such as temperature, dissolved oxygen and
After reviewing the inclusion levels of PKM used in previous studies pH were monitored daily, whereas total hardness, total alkalinity,
(Omoregie and Ogbemudia, 1993; Omoregie, 2001; Thongprajukaew ammonia-N and nitrite-N have been monitored at an interval of three
et al., 2015; Adjanke et al., 2016), five iso-nitrogenous (300 g/kg crude days. The water temperature of all the experimental tanks was checked
protein) experimental diets were formulated, and the proximate by using a water thermometer (MERCK, Germany). The pH of water was
composition of experimental diets have been given in Table 1. Control checked daily by using a pH probe (HI 11310, HANNA Instruments,
diet is devoid of PKM, whereas the treatment groups contained 50 g/kg Singapore). Dissolved oxygen, total hardness, and total alkalinity were
(T1), 100 g/kg (T2), 150 g/kg (T3) and 200 g/kg (T4) of PKM measured as per the standard methods of American Public Health

Table 1
Feed formulation and proximate composition of experimental diets (% dry weight basis: Mean ± S.E).
Treatment
Ingredients (g/100 g)
C T1 T2 T3 T4 p-value

Soyabean meal1 30 30 30 30 30 –
Palm kernel meal2a 0 5 10 15 20 –
Groundnut oil cake1 15 15 15 15 15 –
Sunflower oil cake1b 20 20 15 15 10 –
De-oiled rice bran1c 15 10 10 5 5 –
Wheat flour1 5 5 5 5 5 –
Corn flour1 5 5 5 5 5 –
Vitamin-mineral mix3 2 2 2 2 2 –
Choline chloride 0.3 0.3 0.3 0.3 0.3 –
(Himedia, India)
Carboxymethyl cellulose (Himedia, India) 1.675 1.675 1.675 1.675 1.675 –
Butylated hydroxyl toluene (Himedia, India) 0.025 0.025 0.025 0.025 0.025 –
Vegetable (Sunflower) Oil (ml/100 g)1 6 6 6 6 6 –
Moisture (%) 10.23 ± 0.04b 10.71 ± 0.34ab 11.02 ± 0.06a 10.99 ± 0.02a 10.79 ± 0.10a 0.023
Crude protein (%) 30.09 ± 0.05a 30.08 ± 0.01a 30.13 ± 0.04a 30.10 ± 0.04a 30.05 ± 0.04a 0.712
Crude fat (%) 8.02 ± 0.04d 8.69 ± 0.01b 8.60 ± 0.01c 8.88 ± 0.01a 8.87 ± 0.08a 0.001
Ash (%) 9.87 ± 0.05a 9.73 ± 0.03ab 9.61 ± 0.01bc 9.47 ± 0.04c 9.23 ± 0.07d 0.001
Crude fibre (%) 10.54 ± 0.06c 11.56 ± 0.35b 11.92 ± 0.51ab 12.39 ± 0.24ab 12.58 ± 0.06a 0.001
Nitrogen free extract (%) 41.46 ± 0.08a 39.92 ± 0.36b 39.72 ± 0.53b 39.14 ± 0.17b 38.25 ± 0.04b 0.001
Digestible energy (Kcal/100 g) 358.47 ± 0.47a 358.31 ± 1.52a 356.88 ± 2.01a 356.49 ± 0.79a 356.11 ± 0.25a 0.001

C- Control without PKM, T1− 50 g/kg PKM, T2− 100 g/kg PKM, T3− 150 g/kg PKM and T4− 200 g/kg PKM.
Data expressed as Mean ± SE; Mean values in the same row with different superscript differ significantly (p<0.05). One way ANOVA was used following Duncan
multiple range test in SPSS− 22.0.
2a
Palm kernel meal: Crude protein- 17.93 %; Crude fat- 2.6 %; Ash- 4.56 %; Crude fibre- 23.83 %.
1b
Sunflower oil cake: Crude protein- 34.01 %; Crude fat- 14.79 %; Ash- 6.6 %; Crude fibre- 13.22 %.
1c
De-oiled rice bran: Crude protein- 15.03 %; Crude fat- 1.5 %; Ash- 6.54 %; Crude fibre- 9.23 %.
1 Purchased from local dealers, Andhra Pradesh, India.
2 Ruchi Soya Industries Limited, Andhra Pradesh, India.
3 Composition of vitamin-mineral mix (PREEMIX PLUS, Himedia, India) (quantity per 2.5 kg).
Vitamin A, 55 00 000 IU; Vitamin D3, 11 00 000 IU; Vitamin B2, 2000 mg; Vitamin E, 750 mg; Vitamin K, 1000 mg; Vitamin B6, 1000 mg; Vitamin B12, 6 mcg; Calcium
Pantothenate, 2500 mg; Nicotinamide, 10 g; Choline Chloride, 150 g; Mn, 27 000 mg; I, 1000 mg; Fe,7500 mg; Zn, 5000 mg; Cu, 2000 mg; Co, 450 L- lysine, 10 g; DL-
Methionine, 10 g; Selenium, 125 mg; Vitamin C, 2500 mg.

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S. Sangavi et al. Aquaculture Reports 18 (2020) 100502

1
Association (2005). Ammonia-N and nitrite-N concentrations were protein− min− 1.
determined using ammonia-nitrite Test Kit (Spectroquant
NOVA-MERCK, Germany). Besides the standard method, the dissolved 2.7. Antioxidant enzyme analysis
oxygen concentration was checked using DO probe (HI 764080, HANNA
Instruments, Singapore) on daily basis. Superoxide Dismutase (SOD) activity in liver tissue of rohu was
estimated by the methods of Misra and Fridovich (1972) based on the
2.3. Growth performance analysis oxidation of epinephrine-adrenochrome transition by the enzyme. The
change in absorbance at 480 nm was measured in UV spectrophotometer
Sampling was done fortnightly by taking twenty-five fish from each and the activity was expressed as the amount of protein required to
tank (n = 75/treatment), and the individual fish length and weight were inhibit 50 % autooxidation of epinephrine. Catalase was assayed by the
recorded. The total length (tip of the snout to tip of the caudal fin) and method of Takahara et al. (1960) and expressed as nanomole of H2O2
the total weight of the fish were measured using a meter scale and digital decomposed min− 1 mg protein− 1.
electronic weighing balance, respectively. The calculated growth pa­
rameters such as follows: 2.8. Analysis of proximate composition
Specific Growth Rate (SGR, %/day) = [(ln Final weight- ln Initial
weight)/ number of days] × 100 Pre-weighed feed samples as well as fish carcass were dried in a hot
Feed Conversion Ratio (FCR) = Feed given (dry weight)/ Weight air oven at 105 ± 5 ◦ C for 18− 24 hours to measure the moisture content.
gain (wet weight) Then the dried samples were homogenized and used for the estimation
Protein Efficiency Ratio (PER) = Body weight gain (wet weight)/ of crude protein, lipid, and ash contents by Kjeldhal, Soxhlet, and
protein intake gravimetric method using muffle furnace, respectively (AOAC, 1995).
Apparent Net Protein Utilization (ANPU) = Final carcass protein-
Initial carcass protein (wet weight)/ Total protein fed 2.9. Statistical analysis
Survival (%) = (Total number of fish harvested/ Total number of fish
stocked) × 100. Data on growth and physio-metabolic parameters were analyzed
with the General Linear Model (GLM) one-way analysis of variance
2.4. Sample preparation for enzyme analysis (ANOVA) procedure using SPSS for Windows statistical package pro­
gram, version 22 (SPSS Inc., USA, IL). The statistical significance for all
Three fish were sacrificed from each tank at the end of the experi­ data was determined at p < 0.05, and mean values between different
ment, and their tissues (liver and muscle) were removed aseptically and experimental treatments were compared using Duncan’s Multiple Range
weighed. The collected tissues were homogenized with 0.25 M chilled Tests (DMRT). Polynomial contrasts were used to test both linear and
sucrose solution in a glass tube using teflon coated mechanical tissue quadratic effects of dietary inclusion of PKM on the observed response
homogenizer (MICCRA D-9, Germany). The tube was continuously kept variables. The optimum PKM inclusion was determined using poly­
in ice-cold condition to avoid heating. The homogenate was centrifuged nomial regression analysis (Yossa and Verdegem, 2015).
for 10 min at 5000 rpm in a refrigerated centrifuge. Then, the super­
natant was collected and used for further enzymatic analysis. 3. Results

2.5. Digestive enzyme analysis 3.1. Water quality parameters

Amylase activity of intestine samples was estimated by dinitro sali­ Water quality parameters such as temperature (26.6–28.8 ◦ C), dis­
cylic acid (DNS) method (Rick and Stegbauer, 1974) and the absorbance solved oxygen (5.3–7.4 mg L− 1), pH (7.4–8.4), hardness (132–152 mg
was measured at 540 nm. One unit of amylase activity was expressed as L− 1), total alkalinity (75–85 mg L− 1), ammonia (0.25 to 0.5 mg L− 1) and
moles of maltose released from starch per min at 37 ◦ C. The protease nitrite (0.5–1.0 mg L− 1) were recorded within the optimal range for the
activity was estimated by the casein digestion method (Drapeau, 1976). healthy growth of rohu fingerlings.
The activity was determined by tyrosine standard curve and amount of
enzyme needed to release soluble acid fragments equivalent to Δ0.001 3.2. Growth performance of juvenile L. rohita
A280 per minute at 37 ◦ C and pH 7.8. Lipase activity was determined by
the titrimetric method of Cherry and Crandall (1932) based on the In general, PKM inclusion increased growth performance indices
measurement of fatty acids released by the enzymatic hydrolysis of tri­ such as final average weight, feed intake, SGR, FCR, PER and ANPU
glycerides present in a stabilized emulsion of olive oil. values of juvenile rohu than those of the the control fish (p < 0.05, Fig. 1,
Table 2 2 ) during the 60 days experimental period. It was observed that
2.6. Metabolic enzymes analysis dietary inclusion of PKM on growth performance indices showed an
overall significant effect (p < 0.05), and followed both linear and
Aspartate Amino Transferase (AST) and Alkaline Amino Transferase quadratic trend.
(ALT) activity of liver tissues were assayed according to the method Final average weight and feed intake showed the highest amount in
described by Wooten (1964). AST and ALT activities were based on the 100 g/kg treatment (p < 0.05). Fish fed by 100 g/kg PKM attained the
detection of glutamate and pyruvate, which was released during the highest specific growth rate (p < 0.05). PKM inclusion in the diet
reversible transamination reaction and the activity was expressed as improved FCR compared to control diet (without PKM) (p < 0.05). The
nanomoles of oxaloacetate and pyruvate formed mg protein− 1 min− 1 at lowest amount of FCR was recorded in 50 and 100 g/kg treatments while
37 ◦ C, respectively. The procedure employed for Alkaline Phosphatase the highest amount recorded in 150 and 200 g/kg treatments (p < 0.05).
(ALP) was described by Anon (1963) and expressed as moles of PER and ANPU values were significantly differ amoung treatments, with
para-nitrophenol released mg protein− 1 min− 1 at 37 ◦ C. highest recorded level in 100 g/kg respectively (p < 0.05). The survival
Lactate dehydrogenase (LDH) activity was assayed by the method of of fish did not differ significantly among treatments (p > 0.05).
Wróblewski and Ladue (1955). Malate dehydrogenase (MDH) activity The relationship between the growth performance indices and di­
was assayed by the method of Ochoa (1955). The absorbance was etary PKM levels were expressed by the polynomial regression equations
recorded at 340 nm at 30-sec interval for 3 min, and enzymatic activity (quadratic), where final average weight: y = -0.0002x2 + 0.0275x +
of LDH and MDH were expressed as micromoles of NAD released mg 16.644, R2 = 0.6931, optimal dose = 68.94 g/kg (Fig. 2A); SGR: y = -2E-

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S. Sangavi et al. Aquaculture Reports 18 (2020) 100502

Fig. 1. Average body weight (g) of juvenile rohu (Labeo rohita) fed with experimental diets containing different inclusion levels of palm kernel meal.

Table 2
Average body weight and growth parameters of juvenile Labeo rohita observed during 60 days experimental period.
Treatments p-value
Parameters PSEa R2
C T1 T2 T3 T4 Overall Linear Quadratic

Initial average weight (g) 7.23a 7.24a 7.25a 7.26a 7.25a 0.009 0.820 0.251 0.938 –
Final average weight (g) 16.52c 17.51b 18.44a 15.49d 15.20e 0.326 <0.001 <0.001 <0.001 0.6931
Feed intake 30.01c 31.74b 33.86a 28.62d 28.22e 0.558 <0.001 <0.001 <0.001 –
% SGR/day 1.38c 1.47b 1.55a 1.26d 1.23e 0.033 <0.001 <0.001 <0.001 0.7118
FCR 3.23b 3.09c 3.02c 3.47a 3.55a 0.057 <0.001 <0.001 <0.001 0.7905
PER 1.03b 1.07a 1.09a 0.95c 0.93c 0.017 <0.001 <0.001 <0.001 0.5791
ANPU 62.73b 66.91b 72.74a 56.27c 53.97c 1.955 <0.001 0.001 <0.001 0.7125
Survival (%) 98.66a 98.66a 98.66a 98.00a 97.66a 0.361 0.891 0.374 0.703 –

C- Control without PKM, T1− 50 g/kg PKM, T2− 100 g/kg PKM, T3− 150 g/kg PKM and T4− 200 g/kg PKM.
SGR, Specific Growth Rate, FCR, Feed Conversion Ratio, PER, Protein Efficiency Ratio, ANPU, Apparent Net Protein Utilization.
Data expressed as Mean (n=25, r=3); Mean values in the same row with different superscript differ significantly (p<0.05). One way ANOVA was used following
Duncan multiple range test in SPSS− 22.0. Estimated Marginal Means. aPooled Standard Error of the mean.

05x2 + 0.0025x + 1.3929, R2 = 0.7118, optimal dose = 65.04 g/kg (quadratic), where amylase: y = -5E-05x2 + 0.009x + 2.7443, R2 =
(Fig. 2B); FCR: y = 3E-05x2 - 0.0034x + 3.2051, R2 = 0.7905, optimal 0.6458, optimal dose = 100.11 g/kg (Fig. 3A); protease: y = -5E-05x2 +
dose = 56.83 g/kg (Fig. 2C); PER: y = -6E-06x2 + 0.0007x + 1.0414, R2 0.0026x + 4.4049, R2 = 0.8622, optimal dose = 26.17 g/kg (Fig. 3B);
= 0.5791, optimal dose = 58.50 g/kg (Fig. 2D), and ANPU: y = -0.001x2 and lipase: y = -0.0003x2 + 0.0289x + 18.633, R2 = 0.7138, optimal
+ 0.1452x + 63.119, R2 = 0.7125, optimal dose = 72.67 g/kg (Fig. 2E). dose = 48.27 g/kg (Fig. 3C).

3.3. Proximate composition of the carcass 3.5. Metabolic enzymes

The estimated proximate composition of the experimental fish are The AST and ALT values were significantly higher (p < 0.05) in 100
given in Table 3. There is an overall significant effect in crude protein g/kg treatment than control and lower values recorded in T4 group
and the variance was found to follow both the linear and quadratic (Table 4). The ALT and ALP values followed no linear and quadratic
trends. Higher crude protein level was recorded in fish fed by 100 g/kg trends among the treatments. The relationship between the AST, ALT
PKM (p < 0.05) and lower protein content in 200 g/kg treatment. and ALP enzymes activities and dietary PKM levels were expressed by
Carcass fat content did not show any significant (p > 0.05) differences the polynomial regression equations (quadratic), where AST: y = -1E-
among treatments. The ash content was highest in the control and 04x2 + 0.0165x + 2.6666, R2 = 0.5783, optimal dose = 82.57 g/kg
showed a decreasing trend with an increase in PKM inclusion diets. The (Fig. 4A); ALT: y = -0.0006x2 + 0.0791x + 15.401, R2 = 0.9871, optimal
carcass carbohydrate content showed the maximum value with increase dose = 66.04 g/kg (Fig. 4B); and ALP: y = -0.0003x2 + 0.0446x +
in PKM level (200 g/kg) which is significantly varied from T2 (100 g/kg 10.079, R2 = 0.6887, optimal dose = 74.50 g/kg (Fig. 4C).
PKM) and was recorded the lowest value among other PKM fed groups (p There was a significant variation (p < 0.05) noticed in the muscle
< 0.05). The highest moisture contents were recorded in the T4 and T3, and showed linear effects on LDH and MDH values.The maximum
respectively; showing significant differences from other treatments. amount of LDH and MDH were recorded in T4 (200 g/kg PKM) treat­
ment, whereas the control group registered the lowest value.
3.4. Digestive enzymes
3.6. Antioxidant enzymes
The digestive enzymes (amylase, protease and lipase) activities were
significantly increased in T2 group fed with diet containing 100 g/kg The SOD and catalase activities showed an overall significance (p <
PKM than the control group (p = 0.003, p = 0.001 and p = 0.002, 0.05) and linear effects, but no quadratic trend was observed in the fish
respectively), however, significantly lower values were recorded in the fed PKM diets (Table 4).The treatment T3 and T4 were exhibited
treatment of 200 g/kg PKM (Table 4). significantly (p < 0.05) higher SOD and catalase activities than control,
The relationship between the digestive enzyme activities and dietary 50 and 100 g/kg PKM treatments. However, the SOD and catalase ac­
PKM levels were expressed by the polynomial regression equations tivities of control, T1, and T2 groups did not vary significantly (p >

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S. Sangavi et al. Aquaculture Reports 18 (2020) 100502

Fig. 2. Significant quadratic relationships and polynomial regressions analysis (P < 0.05) between final average weight (A) (p < 0.001), specific growth rate (B) (p <
0.001), feed conversion ratio (C) (p < 0.001), protein efficiency ratio (D) (p < 0.001), and apparent net protein utilization (E) (p < 0.001) of Labeo rohita fed with
various inclusion levels of palm kernel meal diets.Values are expressed as mean from triplicate groups (n = 3).

Table 3
Proximate composition of the carcass (% wet weight basis) of experimental fish (Labeo rohita fingerlings) samples at the end of feeding trial (60 days).
Treatments p-value
Parameters PSEa
C T1 T2 T3 T4 Overall Linear Quadratic

Moisture (%) 75.86ab 75.17b 75.3b 76.57a 76.74a 0.214 0.029 0.017 0.053
Crude protein (%) 17.1c 18.09b 18.89a 16.21d 16.07d 0.289 <0.001 <0.001 <0.001
Crude fat (%) 1.39a 1.37a 1.15a 1.29a 1.25a 0.064 0.844 0.515 0.610
Ash (%) 2.82a 2.49ab 2.35ab 2.19b 2.14b 0.091 0.090 0.010 0.402
Total carbohydrate 2.81ab 2.87ab 2.28b 3.72a 3.78a 0.198 0.044 0.026 0.136

C- Control without PKM, T1− 50 g/kg PKM, T2− 100 g/kg PKM, T3− 150 g/kg PKM and T4− 200 g/kg PKM.
Estimated Marginal Means. a Pooled Standard Error of the mean. Data expressed as Mean; Mean values in the same row with different superscript differ significantly
(p<0.05). One way ANOVA was used following Duncan multiple range test in SPSS− 22.0.

0.05). protein, energy and fiber were well-established in the animal feeding
(Agunbiade et al., 1999). The utilization of PKM in the animal diets can
4. Discussion be evaluated by sensorial analysis and it is an important index for the
determination of meat quality (Ochang et al., 2007; Zamani et al.,
Among the non-conventional feed ingredients, PKM are abundant in 2017). The study on sensorial characteristics (appearance, flavor, smell
tropical areas of the world (Agunbiade et al., 1999; Kim et al., 2013; and juiciness) of the meat conducted by Ribeiro et al. (2011) in lamb, Ao
Rhule, 1996; Sharmila et al., 2014). Kim et al., 2016 reported that global et al. (2011) in pig and Zamani et al. (2017) in broiler chicken indicated
PKM production is steadily increasing in these areas with 7 million the higher acceptability of PKM in the diets. Hence from the above
metric tonnes per annum.The potential use of PKM as a source of dietary findings, it has been proven that PKM could be successfully incorporated

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S. Sangavi et al. Aquaculture Reports 18 (2020) 100502

Table 4
Digestive, metabolic and stress enzymatic activities of juvenile Labeo rohita fed with different inclusions of palm kernel meal diets.
Treatments p-value
Parameters PSEa R2
C T1 T2 T3 T4 Overall Linear Quadratic

Amylase (U/mg protein/min) 2.72bc 3.04ab 3.37a 2.67c 2.61c 0.087 0.003 0.115 0.001 0.6458
Protease (U/mg protein/min) 4.37a 4.39a 4.47a 3.37b 3.15b 0.167 0.001 <0.001 0.035 0.8622
Lipase (U/mg protein/min) 19.48ab 16.58bc 21.13a 14.27cd 11.27d 1.062 0.002 0.001 0.036 0.7138
AST (U/mg protein/min) 2.59c 3.24b 3.85a 2.33c 2.36c 0.172 0.001 0.043 0.001 0.5783
ALT (U/mg protein/min) 15.67ab 17.06ab 17.79a 13.29bc 11.66c 0.758 0.020 0.010 0.028 0.9871
ALP (U/mg protein/min) 10.11ab 12.06a 9.72ab 6.51b 6.09b 0.863 0.116 0.025 0.379 0.6887
LDH (U/mg protein/min) 0.02b 0.04b 0.04b 0.22a 0.30a 0.035 0.004 <0.001 0.120 –
MDH (U/mg protein/min) 0.08c 0.108bc 0.109bc 0.21ab 0.24a 0.021 0.015 0.001 0.326 –
SOD (Units/mg protein) 10.11b 10.64b 10.68b 13.11a 13.12a 0.430 0.020 0.002 0.604 –
Catalase (Units/mg protein) 47.72c 49.16c 50.63c 59.43b 65.82a 1.982 <0.001 <0.001 0.030 –

C- Control without PKM, T1− 50 g/kg PKM, T2− 100 g/kg PKM, T3− 150 g/kg PKM and T4− 200 g/kg PKM.
Estimated Marginal Means. a Pooled Standard Error of the mean. Data expressed as Mean (n=25, r=3); Mean values in the same row with different superscript differ
significantly (p<0.05). One way ANOVA was used following Duncan multiple range test in SPSS− 22.0.

Fig. 3. Significant quadratic relationships and polynomial regressions analysis (P < 0.05) between amylase (A) (p = 0.001), protease (B) (p = 0.035), and lipase (C)
(p = 0.036) activities of Labeo rohita fed with various levels of palm kernel meal inclusion diets. Values are expressed as mean from triplicate groups (n = 3).

as a feed ingredient in animal diets (Ng, 2003). In this context, the Kamali-Sanzighi et al. (2019) in common carp fed with 10 % of PKM
utilization of the PKM inclusion in the diets for juvenile rohu (L. rohita) diets. In addition, the obtained quadratic polynomial regression results
were evaluated based on growth performance, carcass composition and revealed that growth performance of L. rohita were increased at
enzymatic activities. 56.83–72.67 g/kg PKM. However, higher level of PKM inclusion (200
g/kg) in the fish diets negatively affected the growth performance of the
experimental fish. Similar growth trend were reported in L. senegalensis
4.1. Fish growth performance and carcasscomposition (Omoregie, 2001), nile tilapia (Omoregie and Ogbemudia, 1993) and
red hybrid tilapia (Ng and Chong, 2002) when fed with PKM incorpo­
In the present study, higher growth parameters of juvenile L. rohita rated diet and in rohu (Shamna et al., 2016) fed with Jatropha protein
were recorded at 100 g/kg PKM (ANOVA result) inclusion in fish fed concentrate.
diets; thus indicating the potential use of PKM as a non-conventional, The PKM contains considerable amount of non-starch poly­
cost-effective feed ingredient in the fish diets. Similarly, studies on saccharides i.e., an unavailable lignocellulosic constituent (lignin, cel­
date palm seed meal (DSM) inclusion reported to improve the growth lulose and hemicellulose) that makes the feed unpalatable as previously
rate in common carp (Ahmed et al., 2017; Kamali-Sanzighi et al., 2019; stated by Jauncey and Ross (1982) and Thongprajukaew et al. (2015).
Mohammadi et al., 2018), African catfish ((Sotolu et al., 2013) and nile FCR and FER are used to determine the growth performance and feed
tilapia (Assem et al., 2014; Dawood et al., 2020a, b). There were sig­ utilization capacity of the cultured fish (Amin et al., 2005). In this study,
nificant variations detected in growth rate of juvenile rohu between the values of FCR were within the range as reported in earlier studies in
control and PKM inlusion diet groups as similarly stated by Omoregie rohu fed with aquatic weed (Ray and Das, 1992), salseed meal
(2001) in Labeo senegalensis, Adjanke et al. (2016) in nile tilapia and

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S. Sangavi et al. Aquaculture Reports 18 (2020) 100502

Fig. 4. Significant quadratic relationships and polynomial regressions analysis (P < 0.05) between (A) aspartate amino transferase (AST) (p = 0.001), (B) alkaline
amino transferase (ALT) (p = 0.028), and (C) alkaline phosphatase (ALP) (p = 0.379) activities of Labeo rohita fed with experimental diets containing various in­
clusion levels of palm kernel meal. Values are expressed as mean from triplicate groups (n = 3).

(Mukhopadhyay and Ray, 1996), sesame seed meal (Mukhopadhyay and the experimental groups and it could be due to adaptive nature of her­
Ray, 1999a,b), copra meal (Mukhopadhyay and Ray, 1999a,b), duck­ bivorous fish (rohu) to utilize plant ingredients in the feed, thus in­
weed leaf meal (Bairagi et al., 2002), Leucaena leaf meal (Bairagi et al., creases the lipogenic activity (Akinleye et al., 2010; Kaushik et al., 2004;
2004), green pea seed meal (Ramachandran et al., 2005) and Jatropha Kumar et al., 2011a,b; Shamna et al., 2016; Skonberg et al., 1997) in the
protein concentrate (Shamna et al., 2014) diets. The fish reared in T3 cultured fish. The ash content was inversely proportional to PKM in­
and T4 groups (150 and 200 g/kg PKM) respectively, exhibited lower clusion levels, indicating that there could be an insufficient supply of
PER and ANPU values; similarly, common carp (Kumar et al., 2011a,b) dietary mineral as reported by Kumar et al., 2011a,b; Nagel et al., 2012;
and rohu (Bairagi et al., 2002; Maity and Patra, 2008; Ramachandran Slawski et al., 2013 and Shamna et al., 2016 and its absorption by the
et al., 2005; Shamnaet al., 2014; Xavier et al., 2012) fed with fishes.
plant-based non-conventional feed ingredient displayed lower PER
values. The higher amount of PKM inclusion in the diet increases the
non-starch polysaccharides (anti-nutritional factor) in the feed, which 4.2. Digestive enzymes
limits the utilization of nutrients present in the diet. Roslan et al. (2017)
reported that the extrusion process of PKM enhanced its nutritive value Amylase activity was improved in rohu fed 100 g/ kg PKM diet,
and reduced the highly indigestible polysaccharides content. In agree­ which positively indicates the degree of starch gelatinization (Kumar
ment with the present observation, Nalawade and Bhilave (2011) re­ et al., 2006; Mohapatra et al., 2002; Thongprajukaew et al., 2015) of the
ported that unavailable lignocellulosic constituents in the feed could be diet. Similarly, fermented DSM effectively improved the digestive
negatively affecting the activity of protease enzyme, since these values enzyme activities and helped to improve the digestion process without
were measured to determine the protein utilization capacity of fish. decreasing the feed intake (Hong et al., 2004; Dawood et al., 2020a, b).
Final results signifying survival in the experimental groups were com­ Besides, higher incorporation of PKM in the diet negatively affected the
plementary with early investigations by Iluyemi et al. (2010), who re­ enzymatic activity, thus lowers digestion of dietary carbohydrate in fish
ported that the survival of red tilapia fingerlings were not significantly as noticed in earlier studies with Chuni (commercially available low-cost
affected due to toxins released from the experimental feeds. cattle fodder) in the diet for rohu fingerlings (Saha and Ray, 1998). In
The carcass is always influenced by the fish feed composition and agreement with the present observation, Cheng et al. (2010); Murashita
also by percentage and quantity of feed intake (Gawlicka et al., 2002; et al. (2015) and Kumar et al. (2018a) reported that plant-based diets
Hung et al., 1987; Javaherdoust et al., 2020). In the present study, lower have high fibre content which results in lower amylase activity.
crude protein in the carcass was observed in fish fed with 200 g/kg PKM Thongprajukaew et al. (2015) and Xavier et al. (2012) observed inverse
diets, which is attributed to the presence of indigestible fibre (non-starch results in sex-reversed nile tilapia that the ability to digest carbohydrate
polysaccharides) in the PKM as similarly reported by Ng and Chen in soaked PKM and unsoaked diets, respectively. Thus, it signifies that
(2002) in hybrid catfish and Adjanke et al. (2016) in nile tilapia fed PKM the type and the amount of feed ingredient in the diets of L. rohita
diets and thereby limiting protease activity (Francis and Becker, 2001; determine the activity of digestive enzymes (Sethuramalingam and
Kumar et al., 2010; Shamna et al., 2016) and nutrient utilization. The Haniffa, 2002); and it also depends on the nitrogen-free extract in diets
lipid contents of the present study showed no significant variations in all and age of fish (Patra et al., 2002).
A similar trend was recorded in protease and lipase enzymatic

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S. Sangavi et al. Aquaculture Reports 18 (2020) 100502

activities, and the lowest values were recorded in 200 g/kg PKM diet. study, Sitja-Bobadilla et al. (2005) in Gilthead sea bream and Olsvik
Iluyemi et al. (2010) reported that it might be due to the presence of et al. (2011) in Atlantic salmon stated that plant-based diets could
anti-nutritional factors present in the plant-based feed ingredient. trigger oxidative stresses in fish. Similar to our observations, SOD and
Earlier findings were similarly complimentary with lower protein di­ catalase activities were triggered in grass carp (Zheng et al., 2012),
gestibility in rohu (Maity and Patra, 2008; Saha and Ray, 2011; Xavier tilapia (Deng et al., 2015) and rohu (Shamna et al., 2016) due to the
et al., 2012), common carp (Kumar et al., 2011a,b; Sivani et al., 2013) presence of toxic components and anti-nutritional factors in the diets
and rainbow trout (Kumar et al., 2011a,b) fed with non-conventional containing cotton seed meal, rubber seed meal, and Jatropha protein
plant-based meals such as water hyacinth, Azolla leaf, PKM, Jatropha concentrate, respectively.
kernel meal, etc. Hence, this may be the reason for the adverse growth It is vital to state that this study is a preliminary investigation on the
rate, which causes higher FCR in the T4 (200 g/kg PKM) treatment. possibility of utilizing PKM as an alternative non-conventional feed
Lipase activity were higher in fish fed 100 g/ kg PKM diet group, ingredient in the diet of L. rohita and the results obtained are testimony
possibly due to improved utilization of lipids (Thongprajukaew et al., for possible enhancement in growth, digestive and metabolic enzyme
2015), this can be correlated with increased digestion and absorption of activities as well as carcass characteristics of rohu using PKM.
lipids in intestine due to bile acid secretion (Javaherdoust et al., 2020;
Ketels, 1994). Similarly, Kumar et al. (2011a,b) and Sivani et al. (2013) 5. Conclusion
noticed a decrease in enzyme activities in O. mykiss and C. carpio due to
heat-stable anti-nutrient (phytate) present in detoxified Jatropha kernel Based on the results obtained from the present study, it can be
meal diets. concluded that inclusion of PKM in the diet of juvenile rohu at an
optimised level (ranging from 26.17–100.11 g/kg) is possible without
4.3. Metabolic enzymes negotiating the growth performance, carcass characteristics, digestive
and metabolic enzyme activities of the fish. Nevertheless, a long-term
In this study, lower ALT and ALP (implying growth and proper feeding trial is recommended in various ecosystems with analysis of
functioning of fish) values were observed in the diets containing higher anti-nutritional factors in PKM and its microstructure before its incor­
inclusion of PKM (200 g/kg) could be due to liver cell damage (Racicot poration in aquafeed; so as to endorse PKM to be a more practical and
et al., 1975; Agarwal et al., 1984) by the action of non-starch poly­ cost-effective feed ingredient, profitable for carp culture and farmers.
saccharides containing maximum amount of indigestible fibre in the
diet. Similar results of damaged liver cells and organ disruption were CRediT authorship contribution statement
noticed by Hemre et al. (2005) and Sanden et al. (2006) on soybean meal
diets fed to Atlantic salmon; Kumar et al. (2010) in common carp and S. Sangavi: Methodology, Investigation, Resources, Formal analysis,
Kumar et al. (2011a),b on feeding detoxified Jatropha curcas kernel meal Writing - original draft. Paramita Banerjee Sawant: Conceptualization,
to rainbow trout fingerlings. In the current study, liver AST and ALT Resources, Supervision, Validation, Visualization, Writing - review &
activities were observed to be higher in 100 g/kg PKM fed diets. Simi­ editing. Muralidhar P. Ande: Supervision, Writing - review & editing.
larly, Hassaan et al. (2015) and Hassaan et al. (2017) observed that the Karthireddy Syamala: Conceptualization, Methodology, Writing - re­
enzymatic activities of AST and ALT were increased in nile tilapia fed view & editing, Supervision. N.K. Chadha: Resources, Writing - review
diet containing fermented soybean meal. Also, the AST and ALT activ­ & editing, Supervision.
ities were significantly higher in rohu fed with Jatropha protein
concentrate than in those non-fermented protein concentrate (Shamna
et al., 2014). Declaration of Competing Interest
During deficit of oxygen or glucose supply to the cell/ tissue,
decreased activity of the carbohydrate metabolic enzymes such as LDH I am herewith declaring that there is no conflict of interest in pub­
and MDH is observed, indicating the reduced activity of Krebs cycle and lishing the manuscript. This manuscript, or its contents in some other
resulting in the leakage of enzymes or impairment of mitochondrial form, has not been published previously by any of the authors and is not
organization (Murray et al., 2000). Generally, LDH and MDH activity under consideration for publication in another journal. The authors
increases during stress (Vijayaraghavan and Rao, 1986) viz, starvation, declare that they have no known competing financial interests or per­
confinement, etc. Therefore in this experiment, higher LDH and MDH sonal relationships that could have appeared to influence the work re­
activities recorded in the higher PKM inclusion diets (200 g/kg) indi­ ported in this paper. All the co-authors have agreed for submission of
cated that the energy demand of the fish increased concurrently, as these this manuscript to your esteemed journal “Aquaculture Reports”. I also
fish did not accept the feed (200 g/kg PKM) effectively due to unpal­ declare that the manuscript is prepared strictly according to the Journal
atable nature and further it can be correlated with the lower growth format as provided in the instruction to authors.
performance. Kumar et al. (2012) conducted the study in Channa
punctatus found that LDH activities reduced when there was exposure to Acknowledgments
the toxic substances. Similar results were demostrated by Das et al.
(2006); Shamna et al. (2014) and Asimi and Sahu (2015) in rohu This study was funded by ICAR-Central Institute of Fisheries Edu­
wherein, higher incorporation of plant-based ingredients and Jatropha cation, Mumbai, India. The authors are thankful to the Director and
protein concentrate resulted in reduced LDH and MDH activities. Vice-chancellor, ICAR-Central Institute of Fisheries Education, Mumbai,
India, for the necessary support and encouragement with this study.
4.4. Antioxidant enzymes
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