Research Article

Biological Performance in Black Fin Seabream, Acanthopagrus berda (Forsskal, 1775) by Using Two Different Protein-Based Diets in Seawater Earthen Ponds

Sajid Ali1, Ghulam Abbas1, Shahnaz Rashid1, Asma Fatima1*, Abdul Malik1, Dilawer Ali1, Muneer Hussain Bijoro1, Ushra Batool Hashmi1, Rumaisa Abdul Rahim1, Shahid Hussain2, Kashif Ali3, Jabbar Memon4 and Javeria Khourshid1

1Centre of Excellence in Marine Biology, University of Karachi, Karachi-75270, Pakistan; 2Department of Fisheries, Gilgit-Baltistan, Pakistan; 3Department of Food Engineering, University of Debrecen, Egyetem, Hungary; 4Directorate of Fisheries Sindh, Livestock and Fisheries Department, Govt. of Sindh, Pakistan.

Received | March 13, 2023; Accepted | April 26, 2023; Published | August 03, 2023

*Correspondence | Asma Fatima, Centre of Excellence in Marine Biology, University of Karachi, Karachi-75270, Pakistan; Email: [email protected]

Citation | Ali, S., G. Abbas, S. Rashid, A. Fatima, A. Malik, D. Ali, M.H. Bijoro, U.B. Hashmi, R.A. Rahim, S. Hussain, K. Ali, J. Memon and J. Khourshid. 2023. Biological Performance in Black Fin Seabream, Acanthopagrus berda (Forsskal, 1775) by Using Two Different Protein-Based Diets in Seawater Earthen Ponds. Sarhad Journal of Agriculture, 39(3): 632-640.

DOI | https://dx.doi.org/10.17582/journal.sja/2023/39.3.632.640

Keywords | Acanthopagrus berda, Fishmeal, Soybean and seawater ponds, Hapa, Growth and meat quality

Copyright: 2023 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Introduction

Black fin seabream (Acanthopagrus berda) is the commercial fish worldwide (FAO, 2012; Abbas et al., 2015; Mourente and Bell, 2006; Rahim et al., 2015). The demand of black fin is increasing due to its good taste and meat quality (Sing et al., 2014; Zhang et al., 2014). The potential culture production for sea bream is now possible in Pakistan because of rapid and high growth rate, resistance to extreme environmental circumstances and large size in a short span (Sa et al., 2006; Rigos et al., 2011; Sarwat, 2014; Rahim et al., 2015). It is noteworthy that sustainable aquaculture depends on the nutritionally balanced feed and the crucial element of fish feed is the protein which is highly important for the growth, digestion, and immunity development (Alvarez-Gonzalez et al., 2001; Hecht et al., 2003; Ai et al., 2004; Ngandzali et al., 2011; El-­Dahhar et al., 2013). Feed is an important component in aquaculture but feeding frequency and feeding rate are also important according to species specific nature of fish (El-Dahhar et al., 2013; Abbas et al., 2011, 2015). As a result, an appropriate feeding level is critical for successful aquaculture, which will save costs and avoid water damage (Abbas and Siddiqui, 2009).

Fishmeal is one of the vital source of protein in aquaculture and most of the fishmeal is obtained from wild fish stock but this source is not environmentally friendly which further leads to overexploitation and stock depletion (Booman et al., 2018). Therefore, the findings of appropriate animal protein substitute are necessary in aquaculture diet. According to fish experts the plant meal can be used as an alternate source of fishmeal and can be replaced by partially or completely. In this context, the soybean meal is considered as the best and cheap protein source in aqua-feed (Krogdahl et al., 2000; Romarheim et al., 2013; FAO, 2016; Voorhees et al., 2019).

Therefore, the purpose of this research is to analyze the substitution of fishmeal by soybean meal and its effects on the biological performance of commercially important black fin seabream species (A. berda) reared in seawater ponds.

Materials and Methods

Experimental site, fish collection and diet

Current study was conducted in seawater earthen ponds at Garho, Thatta Sindh (Latitude: 24°18’7.68”, Longitude: 67°36’19.3”). The dietary efficacy of black-fin seabream (Acanthopagrus berda) was monitored in four nylon meshed hapa (3.7×9.5×9.5 feet) for 60 days. Juveniles (35.75±3.2g) were collected with the help of a cast net from Sakro Creek near Thatta, Sindh, and transported to Garho fish ponds. The total acclimatization period was 2 weeks prior to the experiment. After acclimatization, juveniles (n=15) were distributed into each treatment hapa (T1 and T2) and with two replicates. Two iso-nitrogenous diets were prepared. In Diet-1 soybean meal was included as the main protein source and Diet-2 consist of fishmeal. Compound floating pelleted feed was given at 3% wet body weight twice a day, morning 09:00 am and evening 16:00 pm. Length (cm) and weight (g) of fish were measured fortnightly and the quantity of daily ration was readjusted according to body weight. Experimental diet ingredients for blackfin seabream were labeled in Table 1.

 

Table 1: Feed ingredients composition and chemical analysis (%) of the experimental diets supplied to juveniles of blackfin seabream in seawater ponds.

Ingredients (%)	Diet-1 T1= Soybean meal (%)	Diet-2 T2= Fishmeal (%)
Soybean meal	20	0
Fishmeal	0	20
Mustured oil cake	20	20
Maize Gluten	16	16
Rice bran	21	21
Wheat bran	10	10
Topica	6	6
Vitamin/ mineral premix	2	2
Fish oil	5	5
Total (%)	100 (%)	100 (%)
Chemical analysis (%)
Moisture	9.4	9.1
Crude protein	39.9	39.8
Crude lipid	4.2	4.6
Crude fiber	9.1	8.9
Ash	11	12.2

 

Sample and data analysis

After 2 weeks of trial, we were collected juveniles from each treatment and replicate hapa with the help of scoop net and the total length (cm) and weight (g) were recorded with the help of digital weight balance machine and immediately released back into their respective hapas. Growth indices (Abbas et al., 2011; Daudpota et al., 2016) were used to calculate the overall growth performance of fish.

Following formulas were used for the calculation and analysis of data:

Weight gain = body wt. final – body wt. initial

Average daily wt. gain = fresh body wt. gain/ duration

WG % if initial weight = final weight – initial weight/ initial weight ×100

FCR = diet given/ weight gain (WG)

SGR = Ln final weight – Ln initial weight ⁄ time duration × 100

K = Final weight ⁄ final length × 100

Water quality assessment

Water quality parameter like temperature, salinity, ammonia, pH and dissolved oxygen were monitored on a daily basis. Temperature was measured by using GH Zeal Ltd-London England digital thermometer, ammonia and dissolve oxygen (DO) were examined by Merck KGaA, 64271, Germany portable test kit, pH was measured by EzDO 6011 Taiwan pH meter and salinity was measured by refractometer (Atago, S/Mill-E, 0.100‰, Japan).

Biochemical assessment

Three fish juveniles were randomly selected, anesthetize and kept at –20˚C for whole body proximate investigation. The moisture, protein, lipid, and ash were calculated according to AOAC (2000). To analyze moisture content, samples were dried into an oven (105°C for 12 hours), crude protein was measured using Kjeldahl method (N × 6.25), and lipid content was analyzed by using the petroleum-ether extraction method, whereas, ash was determined by using muffle furnace (550°C for 18 hours).

Statistical assessment

Data of length weight and other parameters were statistically analyzed by using different statistical methods recommended by Rahim et al. (2015). Data was presented as mean values with standard deviation. The probability level was establish as P<0.05 (Steel et al., 1997).

Results and Discussion

Fish growth

The initial mean weight of black fin juveniles was 36.2±2.2 and 36.44±2.9g and the final mean weight was recorded about 76.6±2.6 and 80.2±1.7gin Treatment 1 and 2, respectively. The maximum weight gain was observed in juveniles (T2, 44.6±0.42g) fed D-2 fishmeal based diet than D-1 soybean meal (T1, 41.6±0.49g), but it is found a slight difference (p<0.05) between treatments and considered that soybean meal can be completely replaced by fishmeal. No significant difference (p>0.05) was found in feed conversion ratio and specific growth ratio of T1 and T2 (1.47±0.02, 1.56±0.02% and 1.25±0.01, 1.31±0.02%, respectively). No adverse effects of feed was noticed throughout the study and found high survival ratio (100%) with nil mortality. Although, Figure 1 shows the relative growth of black fin seabream juveniles (A. berda) reared in two different treatments for 60 days. In Treatment 2, juveniles showed a higher growth fed fishmeal based diet as compared to Treatment 1. Figure 2 described the regression analysis between length-weight of juveniles and showed no significant difference (P > 0.05) among treatments (R2= 0.95).

 

Physiochemical parameters

Water quality parameters were assessed throughout the study and found in optimal range. The mean value of temperature (°C) was recorded in T1 (31.35 ± 0.77°C) and in T2 (31.55 ± 0.77°C), salinity recorded in T1 (34.15 ± 0.07‰) and T2 (34.25 ± 0.07‰). Dissolved oxygen (DO, ml/L) in T1= 7.15 ± 0.07 and in T2= 7.2 ± 0.14ml/L, while, pH (7.9 ± 0.28 and 8 ± 0.28) and ammonia (0.025 ± 0.02 and 0.02 ± 0.01mg/L) in T1 and T2, respectively (Table 3). In aquaculture, the optimal value of physicochemical parameters is indispensable for all the aquatic animals specifically to perform their biological processes in the water.

 

Meat quality

Table 2 reveals proximate composition of fish. There was no significant (p>0.05) difference in meat quality between fish fed on two different diets for 60 days.

 

Table 2: Growth parameters of Acanthopagrus berda reared earthen ponds in hapa for the duration of 60 days.

Parameters	(T1) Soybean meal	(T2) Fishmeal
Initial weight (g)	36.2±2.2	36.44±2.9
Initial length (cm)	13.34±0.11	13.38±0.08
Final weight (g)	76.6±2.6	80.2±1.7
Final length (cm)	15.24±0.10	15.36±0.1
Weight gain	41.6±0.49	44.6±0.42
Specific growth rate	1.25±0.01	1.31±0.02
WG, % of initial weight	111.60±0.14	120.1±0.04
Feed conversion ratio	1.56±0.02	1.47±0.02
Condition factor	2.26±0.01	2.34±0.02
Survival rate	100±0.0	100±0.0
Proximate composition (%)
Moisture	70.61±1.3	71.50±1.5
Protein	40.35±0.3	41.72±0.6a
Lipid	7.6±0.3	8.2±0.2a
Ash	2.5±0.5	2.8±0.3

*Values are presented as Mean±S.D

 

Table 3: Water quality parameter (temperature, salinity, pH, ammonia and dissolved oxygen) of the ponds for the duration of 60 days.

Parameters	Treatment-1	Treatment-2
Salinity (‰)	34.15±0.07	34.25±0.07
Temperature(°C)	31.35±0.77	31.55±0.77
Dissolved Oxygen(ml/L)	7.15±0.07	7.2±0.14
Ammonia(mg/L)	0.025±0.02	0.02±0.01
pH	7.9±0.28	8±0.28

*Values are presented as Mean±S.D

 

Balance nutrition in aquaculture is the important necessity to grow and flourish of any aquatic species in captivity. Numerous experiments were conducted to assess the nutritional requirements of demersal fish in aquaculture and protein is the main component of the fish diet (Catacutan et al., 2001; Abbas and Siddiqui, 2003; Mourente and Bell, 2006). Fishmeal (animal protein source) have been widely use in aqua diet to fulfil the protein demand globally but overharvesting and less capture fishery production ultimately affect the production and availability of fishmeal. Researchers are constantly finding new available resources of feed stuff which can replace fishmeal in aqua-diet. Another disadvantage of using fishmeal is that a costly product and it has many health hazard effects of accumulated heavy metals which can be transferred by food chain. In comparison of fishmeal with plant meal (i.e., soybean meal), it is environmentally safe, cost effective, easily available and having high production worldwide. Plant protein have now been widely used in aquaculture as a substitute to animal protein (fishmeal) which is obtained from small pelagic fishes (Nordrum et al., 2000; Li and Robinson, 2015; Voorhees et al., 2019). Uses of plant protein is an appropriate, cheap and profitable substitute protein source for aquaculture industries (FAO, 2016; Voorhees et al., 2019). In this study, the amount of fishmeal was completely replaced by soybean meal in the diet of seabream juveniles which was cultured in semi-intensive marine water ponds to analyze the biological performance of fish. Results showed that, WG (41.6±0.49g) obtained by soybean meal diet (T1) was slightly lower than fishmeal diet in T2 (44.6±0.42g). Such finding match with the previous studies by Kader et al. (2012b) they replaced 100% soybean meal with fishmeal in the diets of juveniles of red seabream and achieved good results. Regarding replacement of fish meals with soybean meal either partially or completely, many scientists conducted research on different fish species with variable setup such as 20 to 50% replacement of fishmeal with soybean meal in the diet of red seabream (Takagi et al., 1999, 2001), gilthead seabream (Kissil et al., 2000), turbot (Day and González, 2000) and Japanese flounder (Choi et al., 2004; Deng et al., 2006). Higher replacements ratio such as 75 to 94% of fishmeal with soybean meal have been discovered by Aragão et al. (2003) in Senegalese sole (Soleasenegalensis) and juveniles of cobia, Rachycentroncanadum (Salze et al., 2010). However, the total substitution of fishmeal with soybean proteins was attained by Liang et al. (2017) in Japanese seabass (Lateolabraxjaponicus), Voorhees et al. (2019) in rainbow trout (Oncorhynchus mykiss) and obscure puffer (Takifugu obscurus) by Ye et al. (2019).

Different fish species grow differently by feeding soybean protein and convert efficiently in body meat, that is because soybean meal is deficient in the essential amino acids like methionine and lysine which limits the growth of fish as well as digestibility and acceptability problems (Chatzifotis et al., 2008; Kader et al., 2010, 2012a). The difference in growth achieved by soybean meal diet may be due to the deficiency in essential amino acid in the diet of black fin sea bream because there was no addition of deficient amino acid takes place. On the other hand, continuous supply of EPA and DHA in the diet to regularize fish growth but complete replacement of fishmeal causes deficiency of these essential fatty acids and this is also proved by earlier studies (Kader et al., 2012a). Some studies supported partial substitution of fishmeal to plant protein in fish diet that did not affect the animal’s performance reported by (Hansen et al., 2007; Suarez et al., 2009; Salze et al., 2010; Bonaldo et al., 2011; Zhang et al., 2018). Also, there was no negative effect in physical feature or any other biological parameter other than growth was noted in our study. Similarly, skin color and texture of body was not affected by inclusion of soybean in the diet of sea bream was reported by (De Francesco et al., 2007).

FCR and SGR obtained by soybean meal in the current study was non-significant (P>0.05) among treatments. These results show that soybean meal can be substitute for fishmeal which resembles with the study of (Lin and Luo, 2011). Although, high survival rate was obtained on both diets was similar to our study results (Ye et al., 2019).

Water quality is the most important factor that contributes in the failure or success of culture and it is also influence on the physiology and health related problems of aquatic species (Piper et al., 1982). In our experiment water quality parameters were found in a suitable range.

Conclusions and Recommendations

The current study on plant protein (soybean meal) pointed out the substitution of fishmeal in aqua diet. In conclusion, fishmeal is still preferable diet in aquaculture despite high price feed than soybean meal and gave good results in terms of growth of black fin seabream juveniles (A. berda) reared in semi-intensive marine water earthen ponds. But soybean meal is the cost effective and easily available protein source can be used as a substitute to reared A. berda juveniles in captivity. However, more research is needed to use soybean meal in the diet as a partially or completely replacement of fishmeal in a long rearing period under captive environment.

Acknowledgements

We are deeply grateful to PARC for providing us financial support under Agriculture Linkage Programme (AS010-2021-24).

Novelty Statement

The current study investigates the biological performance of black-fin seabream (Acanthopagrus berda) juveniles by using two different aqua-diet in seawater earthen ponds.

Author’s Contribution

Sajid Ali: Conducted this research in seawater ponds and prepared the manuscript for publication.

Ghulam Abbas: Supervised and helped in experimental setup.

Asma Fatima: Reanalyze the data, revised and finalize the manuscript writing.

Abdul Malik:Helped data analysis, record and help during experimentation.

JabbarMemon: Provided technical assistance during experimentation.

Shahnaz Rashid: Evaluated and revised the final version of manuscript.

Dilawer Ali, Muneer Hussain Bijoro, UshraBatool Hashmi, Rumaisa Abdul Rahim, Shahid Hussain, Javeria Khourshid and Kashif Ali: Assisted in laboratory work.

Conflict of interest

The authors have declared no conflict of interest.

References

Abbas, G. and P.J.A. Siddiqui. 2003. Effect of feeding rate on growth, feed conversion and body composition of juvenile mangrove red snapper reared in seawater tanks. Pak. J. Zool. 35(2): 151-156.

Abbas, G. and P.J.A. Siddiqui. 2009. Effects of different feeding level on the growth, feed efficiency and body composition of juvenile mangrove red snapper, Lutjanus argentimaculatus (Forsskal 1775). Aquacult. Res., 40(7): 781-789. https://doi.org/10.1111/j.1365-2109.2008.02161.x

Abbas, G., B. Waryani, A. Ghaffar, A. Rahim, M. Hafeez-ur-Rehman and M. Aslam. 2015. Effect of ration size and feeding frequency on growth, feed utilization, body composition and some haematological characteristics of juvenile snapper, Lutjanus johnii (Baloch, 1792). Pak. J. Zool., 47(3): 719-73.

Abbas, G., P.J.A. Siddiqui and K. Jamil. 2011. The optimal protein requirements of juvenile mangrove red snapper, Lutjanus argentimaculatus fed isoenergetic diets. Pak. J. Zool. 44(2): 469-480.

Ai, Q., K. Mai, H. Li, C. Zhang, L. Zhang, Q. Duan and Z. Liufu. 2004. Effects of dietary protein to energy ratios on growth and body composition of juvenile Japanese seabass, Lateolabrax japonicus. Aquaculture, 230(1-4): 507-516. https://doi.org/10.1016/j.aquaculture.2003.09.040

Alvarez-González, C.A., R. Civera-Cerecedo, J.L. Ortiz-Galindo, S. Dumas, M. Moreno-Legorreta and T. Grayeb-Del Alamo. 2001. Effect of dietary protein level on growth and body composition of juvenile spotted sand bass, Paralabrax maculatofasciatus, fed practical diets. Aquaculture, 194(1-2): 151-159. https://doi.org/10.1016/S0044-8486(00)00512-3

AOAC, 2000. Official methods of analysis of association of official analytical chemists, Vol. 1. 17th edn. Association of Official Analytical Chemists, Arlington, USA, 684.

Aragão, C., L.E. Conceição, J. Dias, A.C. Marques, E. Gomes and M.T. Dinis. 2003. Soy protein concentrate as a protein source for Senegalese sole (Solea senegalensis Kaup 1858) diets: Effects on growth and amino acid metabolism of postlarvae. Aquacult. Res., 34(15): 1443-1452. https://doi.org/10.1111/j.1365-2109.2003.00971.x

Bonaldo, A., L. Parma, L. Mandrioli, R. Sirri, R. Fontanillas, A. Badiani and P.P. Gatta. 2011. Increasing dietary plant proteins affects growth performance and ammonia excretion but not digestibility and gut histology in turbot (Psetta maxima) juveniles. Aquaculture, 318(1-2): 101-108. https://doi.org/10.1016/j.aquaculture.2011.05.003

Booman, M., I. Forster, J.C. Vederas, D.B. Groman and S.R. Jones. 2018. Soybean meal-induced enteritis in Atlantic salmon (Salmo salar) and Chinook salmon (Oncorhynchus tshawytscha) but not in pink salmon (O. gorbuscha). Aquaculture, 483: 238-243. https://doi.org/10.1016/j.aquaculture.2017.10.025

Catacutan, M. R., G.E. Pagador and S. Teshima. 2001. Effect of dietary protein and lipid levels and protein to energy ratios on growth, survival and body composition of the mangrove red snapper, Lutjanus argentimaculatus (Forsskal 1775). Aquacult. Res., 32(10): 811-818. https://doi.org/10.1046/j.1365-2109.2001.00618.x

Chatzifotis, S., I. Polemitou, P. Divanach and E. Antonopoulou. 2008. Effect of dietary taurine supplementation on growth performance and bile salt activated lipase activity of common dentex, Dentex dentex, fed a fish meal/soy protein concentrate-based diet. Aquaculture, 275(1-4): 201-208. https://doi.org/10.1016/j.aquaculture.2007.12.013

Choi, S.M., X. Wang, G.J. Park, S.R. Lim, K.W. Kim, S.C. Bai and I.S. Shin. 2004. Dietary dehulled soybean meal as a replacement for fish meal in fingerling and growing olive flounder Paralichthys olivaceus (Temminck et Schlegel). Aquacult. Res., 35(4): 410-418. https://doi.org/10.1111/j.1365-2109.2004.01046.x

Daudpota, A.M., G. Abbas, I.B. Kalhoro, S.S.A. Shah, H. Kalhoro, M. Hafeez-ur-Rehman and A. Ghaffar. 2016. Effect of feeding frequency on growth performance, feed utilization and body composition of juvenile Nile tilapia, Oreochromis niloticus (L.) reared in low salinity water. Pak. J. Zool., 48(1): 171-177.

Day, O.J. and H.P. Gonzalez. 2000. Soybean protein concentrate as a protein source for turbot Scophthalmus maximus L. Aquac. Nutr., 6(4): 221-228. https://doi.org/10.1046/j.1365-2095.2000.00147.x

De Francesco, M., G. Parisi, J., Pérez‐Sanchez, P. Gomez‐Réqueni, F. Médale, S.J. Kaushik, M. Mecatti and B.M. Poli. 2007. Effect of high‐level fish meal replacement by plant proteins in gilthead sea bream (Sparus aurata) on growth and body/fillet quality traits. Aquac. Nutr., 13(5): 361-372. https://doi.org/10.1111/j.1365-2095.2007.00485.x

Deng, J., K. Mai, Q. Ai, W. Zhang, X. Wang, W. Xu and Z. Liufu. 2006. Effects of replacing fish meal with soy protein concentrate on feed intake and growth of juvenile Japanese flounder, Paralichthys olivaceus. Aquaculture, 258(1-4): 503-513. https://doi.org/10.1016/j.aquaculture.2006.04.004

El-Dahhar, A.A., F.H. El-Abed and M.E. Salama. 2013. Protein and energy maintenance and maximum growth requirement for sea bass (Decentrshus laborax) larva using different feeding rates. J. Arabian Aquacult. Soc., 8: 1-18.

FAO, 2012. The state of world fisheries and aquaculture 2012. Fisheries and Aquaculture Department, Food and Agriculture Organization of the United Nations.

FAO, 2016. The state of world fisheries and aquaculture 2016 contributing to food security and nutrition for all Food and Agriculture Organization of the United Nations, Rome.

Hansen, A.C., G. Rosenlund, Ø. Karlsen, W. Koppe and G.I. Hemre. 2007. Total replacement of fish meal with plant proteins in diets for Atlantic cod (Gadus morhua L.) I. Effects on growth and protein retention. Aquaculture, 272(1-4): 599-611. https://doi.org/10.1016/j.aquaculture.2007.08.034

Hecht, T., A. Irish and J. Sales. 2003. Effect of protein level and varying protein–lipid concentrations on growth characteristics of juvenile spotted grunter Pomadasys Commersonnii (Haemulidae). Afr. J. Mar. Sci., 25(1): 283-288. https://doi.org/10.2989/18142320309504017

Kader, M.A. and S. Koshio. 2012a. Effect of composite mixture of seafood by-products and soybean proteins in replacement of fishmeal on the performance of red sea bream, Pagrus major. Aquaculture, 368: 95-102. https://doi.org/10.1016/j.aquaculture.2012.09.014

Kader, M.A., M. Bulbul, S. Koshio, M. Ishikawa, S. Yokoyama and C.F. Komilus. 2012b. Effect of complete replacement of fishmeal by dehulled soybean meal with crude attractants supplementation in diets for red sea bream, Pagrus major. Aquaculture, 350: 109-116. https://doi.org/10.1016/j.aquaculture.2012.04.009

Kader, M.A., S. Koshio, M. Ishikawa, S. Yokoyama and M. Bulbul. 2010. Supplemental effects of some crude ingredients in improving nutritive values of low fishmeal diets for red sea bream, Pagrus major. Aquaculture, 308(3-4): 136-144. https://doi.org/10.1016/j.aquaculture.2010.07.037

Kissil, G.W., I. Lupatsch, D.A. Higgs and R.W. Hardy. 2000. Dietary substitution of soy and rapeseed protein concentrates for fish meal, and their effects on growth and nutrient utilization in gilthead seabream Sparus aurata L. Aquacult. Res., 31(7): 595-601. https://doi.org/10.1046/j.1365-2109.2000.00477.x

Krogdahl, A., A.M. Bakke-McKellep, K.H. Roed and G. Baeverfjord. 2000. Feeding Atlantic salmon Salmo salar L. soybean products: Effects on disease resistance (furunculosis), and lysozyme and IgM levels in the intestinal mucosa. Aquac. Nutr., 6(2): 77-84. https://doi.org/10.1046/j.1365-2095.2000.00129.x

Li, M.H. and E.H. Robinson. 2015. Complete feeds- Intensive systems. In D. A. Davis (Ed.) Feed and feeding practices in aquaculture. Sawston Waltham Maryland Woodhead. pp. 112–126. https://doi.org/10.1016/B978-0-08-100506-4.00004-0

Liang, X.F., L. Hu, Y.C. Dong, X.F. Wu, Y.C. Qin, Y.H. Zheng and M. Xue. 2017. Substitution of fish meal by fermented soybean meal affects the growth performance and flesh quality of Japanese seabass (Lateolabrax japonicus). Anim. Feed Sci. Technol., 229: 1-12. https://doi.org/10.1016/j.anifeedsci.2017.03.006

Lin, S. and L. Luo. 2011. Effects of different levels of soybean meal inclusion in replacement for fish meal on growth, digestive enzymes and transaminase activities in practical diets for juvenile tilapia, Oreochromis niloticus× O. aureus. Anim. Feed Sci. Technol., 168(1-2): 80-87. https://doi.org/10.1016/j.anifeedsci.2011.03.012

Mourente, G. and J.G. Bell. 2006. Partial replacement of dietary fish oil with blends of vegetable oils (rapeseed, linseed and palm oils) in diets for European sea bass (Dicentrarchus labrax L.) over a long term growth study: effects on muscle and liver fatty acid composition and effectiveness of a fish oil finishing diet. Comp. Biochem. Physiol. B, Biochem. Mol. Biol., 145(3-4): 389-399. https://doi.org/10.1016/j.cbpb.2006.08.012

Ngandzali, B.O., F. Zhou, W. Xiong, Q.J. Shao and J.Z. Xu. 2011. Effect of dietary replacement of fish meal by soybean protein concentrate on growth performance and phosphorus discharging of juvenile black sea bream, Acanthopagrus schlegelii. Aquac. Nutr., 17(5): 526-535. https://doi.org/10.1111/j.1365-2095.2010.00835.x

Nordrum, S., A.M. Bakke-McKellep, Å. Krogdahl and R.K. Buddington. 2000. Effects of soybean meal and salinity on intestinal transport of nutrients in Atlantic salmon (Salmo salar L.) and rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. B, Biochem. Mol. Biol., 125(3): 317-335. https://doi.org/10.1016/S0305-0491(99)00190-X

Piper, R.G., I.B. McElwain, L.E. Orme, J.P. McCraren, L.G. Fowler and J.R. Leonard. 1982. Fish hatchery management US department of interior fish and wildlife service. Washington, DC, 517.

Rahim, A., G. Abbas, B. Waryani, A. Ghaffar, M. Monwar, M. Hafeez-ur-Rehman and G. Dastagir. 2015. Influence of varying dietary lipid levels on growth, feed conversion and chemical composition of meat and liver of the juvenile blackfin sea bream, Acanthopagrus berda (Forsskal 1775). Pak. J. Zool., 47(5): 1467-1473.

Rigos, G., V. Zonaras, D. Nikolopoulou, M. Henry, X. Nikoloudaki and M. Alexis. 2011. The effect of diet composition (plant vs fish oil-based diets) on the availability of oxytetracycline in gilthead sea bream (Sparus aurata) at two water temperatures. Aquaculture, 311(1-4): 31-35. https://doi.org/10.1016/j.aquaculture.2010.11.018

Romarheim, O.H., T. Landsverk, L.T. Mydland, A. Skrede and M. Øverland. 2013. Cell wall fractions from Methylococcus capsulatus prevent soybean meal-induced enteritis in Atlantic salmon (Salmo salar). Aquaculture, 402: 13-18. https://doi.org/10.1016/j.aquaculture.2013.03.011

Sá, R., P. Pousão‐Ferreira and A. Oliva‐Teles. 2006. Effect of dietary protein and lipid levels on growth and feed utilization of white sea bream (Diplodus sargus) juveniles. Aquac. Nutr., 12(4): 310-321. https://doi.org/10.1111/j.1365-2095.2006.00434.x

Salze, G., E. McLean, P.R. Battle, M.H. Schwarz and S.R. Craig. 2010. Use of soy protein concentrate and novel ingredients in the total elimination of fish meal and fish oil in diets for juvenile cobia, Rachycentron canadum. Aquaculture, 298(3-4): 294-299. https://doi.org/10.1016/j.aquaculture.2009.11.003

Sarwat, J., 2014. Assessment of dietary protein and energy interactions in marine finfish culture (Doctoral dissertation, M. Phil thesis, University of Karachi, Pakistan).

Sing, K.W., M.S. Kamarudin, J.J. Wilson and M. Sofian-Azirun. 2014. Evaluation of blowfly (Chrysomya megacephala) maggot meal as an effective, sustainable replacement for fishmeal in the diet of farmed juvenile red tilapia (Oreochromis Sp.). Pak. Vet. J. 34(3): 288-292.

Steel, R.G.D., J.H. Torrie and D.A. Dickey. 1997. Principles and procedures of statistics: A biometrical approach. 3rd ed. McGraw-Hill, Boston.

Suárez, J.A., G. Gaxiola, R. Mendoza, S. Cadavid, G. Garcia, G. Alanis and G. Cuzon. 2009. Substitution of fish meal with plant protein sources and energy budget for white shrimp Litopenaeus vannamei (Boone, 1931). Aquaculture, 289(1-2): 118-123. https://doi.org/10.1016/j.aquaculture.2009.01.001

Takagi, S., H. Hosokawa, S. Shimeno, M. Maita, M. Ukawa and S.I. Ueno. 1999. Utilization of soy protein concentrate in a diet for red sea brem, Pagrus major. Aquac. Sci., 47(1): 77-87.

Takagi, S., S. Shimeno, H. Hosokawa and M. Ukawa. 2001. Effect of lysine and methionine supplementation to a soy protein concentrate diet for red sea bream Pagrus major. Fish Sci., 67(6): 1088-1096. https://doi.org/10.1046/j.1444-2906.2001.00365.x

Voorhees, J.M., M.E. Barnes, S.R. Chipps and M.L. Brown. 2019. Bioprocessed soybean meal replacement of fish meal in rainbow trout (Oncorhynchus mykiss) diets. Cogent Food Agric., 5(1): 1579482. https://doi.org/10.1080/23311932.2019.1579482

Ye, H., M. Xu, Q. Liu, Z. Sun, C. Zou, L. Chen and C. Ye. 2019. Effects of replacing fish meal with soybean meal on growth performance, feed utilization and physiological status of juvenile obscure puffer, Takifugu obscurus. Comp. Biochem. Physiol. C Toxicol. Pharmacol., 216: 75-81. https://doi.org/10.1016/j.cbpc.2018.11.006

Zhang, C., S. Rahimnejad, Y.R. Wang, K. Lu, K. Song, L. Wang and K. Mai. 2018. Substituting fish meal with soybean meal in diets for Japanese seabass (Lateolabrax japonicus): Effects on growth, digestive enzymes activity, gut histology, and expression of gut inflammatory and transporter genes. Aquaculture, 483: 173-182. https://doi.org/10.1016/j.aquaculture.2017.10.029

Zhang, L., S. Wang, W. Chen, B. Hu, S. Ullah, Q. Zhang and L. Yi. 2014. Fine structure of zebrafish (Danio rerio) spermatozoa. Pak. Vet. J., 34: 518-521.