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Research Article
 

Performance of Commercial Poultry Offal Meal as Fishmeal Replacement in the Diet of Juvenile Malaysian Mahseer, Tor tambroides



Saufinas Ismail, Mohd Salleh Kamarudin and Ehsan Ramezani-Fard
 
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ABSTRACT

Mahseer is one of the most expensive freshwater fish in Malaysia and has a good potential for freshwater aquaculture industry. This study was conducted to evaluate the suitability of Poultry Offal Meal (POM) as Fish Meal (FM) replacement in the diet of Malaysian mahseer (Tor tambroides). The POM:FM ratios tested were 0:100, 25:75, 50:50, 75:25 and 100:0. One hundred and fifty mahseer fingerlings (3.0±0.05 g) were equally and randomly stocked into 15 65 L aquaria. The diets were randomly assigned to the aquaria in triplicates groups. The feeding trial was conducted for 96 days. No significant differences (p>0.05) were observed among the survival rate of fish while it was above 90% in all the treatments. Weight gain and specific growth rate significantly increased when 50-100% of dietary fishmeal was substituted with POM. Whole body composition of Malaysian mahseer was not significantly influenced by the experimental diets. This study showed that fishmeal in the diet of mahseer can be replaced by POM up to 100% ratio without any adverse effect on survival, growth performance and body composition.

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Saufinas Ismail, Mohd Salleh Kamarudin and Ehsan Ramezani-Fard, 2013. Performance of Commercial Poultry Offal Meal as Fishmeal Replacement in the Diet of Juvenile Malaysian Mahseer, Tor tambroides. Asian Journal of Animal and Veterinary Advances, 8: 284-292.

DOI: 10.3923/ajava.2013.284.292

URL: https://scialert.net/abstract/?doi=ajava.2013.284.292
 
Received: July 02, 2012; Accepted: July 27, 2012; Published: February 11, 2013



INTRODUCTION

Mahseers (Tor spp.) are an important group of big scale riverine cyprinids occurring in mountainous rivers and lakes of most trans-Himalayan countries (Ramezani-Fard et al., 2011a). Its name may be derived from Hindi (mahasir: maha-great and sir-head), Sanskrit (maha-salka: large-scaled) or Indo-Persian (mahisher: mahi-fish and sher-tiger) (Thomas, 1897). In India, mahseer is known as the king of Indian freshwater systems (Nandeesha et al., 1993). In Malaysia, mahseer is one of the most expensive freshwater fish and has a good potential for freshwater aquaculture industry (Ramezani-Fard et al., 2011b; Misieng et al., 2011). There are three species of mahseer in Malaysia: Tor tambroides, T. douronensis and T. tambra (Ingram et al., 2005; Nguyen et al., 2006). Tor tambroides (Malaysian mahseer) has also a high demand in recreational and ornamental fish industry due to its character and attractive coloration (Ng, 2004). The distribution and abundance of this species have declined over the recent years due to significant degradation of their natural habitats caused by deforestation, overfishing and agricultural development (Ismail et al., 2011).

Ng et al. (2008) found that Malaysian mahseer fingerling needs about 45-50% dietary protein while Misieng et al. (2011) reported a lower optimum dietary protein requirement of 40%. Fishmeal and shrimp meal has long been used as a major protein source in aqua-feeds because of their high nutritional value (Siraj et al., 1988; Hlophe and Moyo, 2011). Fish meal is of good quality protein and has an attractive odour which increases the palatability of fish diet (Adeniji, 2008). However, the availability of this feedstuff in future can no longer be assured because the ocean stocks for some species have been reduced (Hlophe et al., 2011). Demand for fishmeal is still so high and is not commensurate with its production. The higher biological value of fishmeal compared to the other protein sources makes it more expensive than the others (Omole et al., 2008). The high fishmeal price leads to the increase of feed cost (Hu et al., 2008; Millamena, 2002). Therefore, finding an alternative protein source which can fully or partially replace fishmeal is now becoming increasingly important especially for fish such as mahseer that require high dietary protein (Ng et al., 2008). Cruz-Suarez et al. (2007) reported that 50 to 65% replacement of fishmeal will reduce feed cost by 10 to 14% which in turn reduces the aquaculture production cost.

Several authors have studied the performance of Poultry Offal Meal (POM) in various fish species and observed that POM as a cheaper and good protein source can be comparable to fishmeal (Shapawi et al., 2007; Emre et al., 2003). POM in some countries is defined as a meal which is produced from viscera, heads and blood while in US it is defined as a meal containing all by-products of poultry including feathers (Dale et al., 1993). POM has slightly higher in crude protein and fat compared to fishmeal (Omole et al., 2008).

To date, there is no published information on the feasibility of using POM in mahseer diet as a fishmeal replacement. This study was conducted to determine the effects of replacement of dietary fishmeal with POM on the growth, survival and body composition of Malaysian mahseer and to determine the optimal replacement ratio of POM in the diet of this fish.

MATERIALS AND METHODS

Diet preparation: Five isonitrogenous and isocaloric diets were formulated in order to substitute different ratio of fishmeal (0 -control-, 25, 50, 75 and 100%) with POM (Table 1).

Table 1: The composition of test diets (% as fed basis)
Image for - Performance of Commercial Poultry Offal Meal as Fishmeal Replacement in the Diet of Juvenile Malaysian Mahseer, Tor tambroides
NFE: Nitrogen-free extract

The formulation was performed using the winfeed 2.8 for Windows (Winfeed Limited, Cambridge, UK). All diets contained 35% crude protein and 17.5 kJ g-1 gross energy (Misieng et al., 2011). The diets were pelletized using a single screw extruder (Brabender KE19, die size 3 mm Ø). The barrel temperatures were set at 60-100-120°C and the temperature at the die head was 160°C. The feeding, shaft and four-bladed cutter speeds were set at 50, 150 and 310 rpm, respectively. The extruded pellets were stored in sealed plastic bags at 4°C until use.

Feeding trial: The feeding trial was conducted at the Aquaculture Experimental Station, Universiti Putra Malaysia. Tor tambroides fry were procured from a local fish supplier and acclimatised in a 1 ton PE tank for 7 days. During the acclimation period, fish were fed diet 1 (Table 1). One hundred and fifty fingerlings (3.0±0.5 g) were equally and randomly assigned to 15 glass aquaria with capacity of 65 L. Continuous filtration and aeration kept dissolved oxygen level in each aquarium above 5.5 mg L-1. Water temperature, pH, dissolved oxygen and ammonia nitrogen were monitored twice per week. Water temperature was found between 23 and 3°C while pH ranged between 6.5 and 8.8. The toxic ammonia (NH3+) was below 0.01 mg L-1. The experiment was conducted for 14 weeks from May to August 2011 and fish were fed twice per day (09:00 and 18:00 h) at 3% b.wt. Fish were sampled and weighed every two weeks and the quantity of feed was adjusted accordingly. Aquaria water was partially changed (70%) during each sampling. Dead fish were collected and sent to Universiti Putra Malaysia Veterinary Hospital in order to diagnose causes of death. At the end of the experiment, Weight Gain (WG), Specific Growth Rate (SGR), Feed Conversion Ratio (FCR) and Protein Efficiency Ratio (PER) were calculated using following formulae. The fish were then sacrificed and stored at -45°C for further whole body proximate analysis:

Image for - Performance of Commercial Poultry Offal Meal as Fishmeal Replacement in the Diet of Juvenile Malaysian Mahseer, Tor tambroides

Chemical analysis: The proximate analyses of the diets and fish were carried out according to AOAC methods (AOAC, 1997). The proximate analyses were done in triplicates. Whole fish samples were prepared through freeze-drying and grinding. Moisture content was estimated by drying samples in an oven at 105°C for 24 h to constant weight. The crude protein (nitrogenx6.25) was determined by the Kjeldahl method while crude lipid was estimated by ether extraction using a Soxhlet system. The crude fibre was determined using acid/base digestion followed by burning the samples to ash in a muffle furnace at 600°C for 12 h. The gross energy of diets and fish was determined by direct combustion in an adiabatic bomb calorimeter.

Statistical analysis: All data were subjected to one-way Analysis of Variance (ANOVA) using SPSS 17 for Windows (SPSS INC., Chicago, IL, USA) and the difference was considered significant at p<0.05. Duncan’s Multiple Range Test was used to test mean differences. All percentage data were arcsine transformed prior to statistical analyses.

RESULTS

The survival rate of T. tambroides was generally high (90-100%) and no significant differences (p>0.05) among treatments were observed (Table 2). Few fish on diet 1 and diet 3 died because they were accidently trapped and killed by the filter. Few fish on diet 2 also died in the last two weeks due to non-infectious problems. However, a non-pathogenic or opportunistic group of bacteria (Klebsiella sp.) in fish were isolated from them.

The highest percentage of weight gain was observed in fish fed diets 3, 4 and 5 and there were no significant differences (p>0.05) between fish fed these diets (Table 2). However, weight gain in fish fed diets 1 and 2 were significantly lower (p<0.05) than those fed the other diets. Unlike the weight growth pattern, a rapid length growth was observed among all treatments in the first two weeks. However, the rate of length growth was slowly decreased after this period. Final total length in fish fed diets 3, 4 and 5 were significantly higher (p<0.05) than those fed diet 1 and 2. The highest total length gain was observed in fish fed diet 4 (31.60±2.63%) while it was not significantly different (p>0.05) with those fed diets 3 and 5.

The specific growth rate was generally low and showed a similar pattern as the weight gain. Fish on diet 4 showed the highest SGR while it was not significantly different (p>0.05) with those fed diets 3 and 5 and was significantly higher than fish fed diets 1 and 2 (p<0.05). Feed Conversion Ratios (FCR) of the experimental diets are shown in Table 2. The lowest and the best FCR (3.27±0.20) was achieved when fish fed diet 4 while it was not significantly different with fish fed diets 3 and 5. The FCR in fish fed diets 1 and 2 were significantly higher (p<0.05). The best Protein Efficient Ratio (PER) was also observed in fish fed diets 3, 4 and 5.

Table 3 shows the whole body composition of Malaysian mahseer juveniles fed different diets. Protein (39.37-45.65% DM) and crude fat (42.61-47.94% DM) were the main components of whole body of the fish. No significant differences (p>0.05) were observed among the whole body composition of fish fed different diets.

Table 2: Survival rate, growth performance and feed efficiency of Malaysian mahseer fed diets containing different percentage of POM as fishmeal replacement
Image for - Performance of Commercial Poultry Offal Meal as Fishmeal Replacement in the Diet of Juvenile Malaysian Mahseer, Tor tambroides
Values within the same row having the same superscript are not significantly different at p>0.05, SGR: Specific growth rate, FCR: Feed conversion ratio, PER: Protein efficiency ratio

Table 3: Whole body proximate composition of juvenile Tor tambroides before and after feeding the experimental diets
Image for - Performance of Commercial Poultry Offal Meal as Fishmeal Replacement in the Diet of Juvenile Malaysian Mahseer, Tor tambroides
Values within the same row having the same superscript are not significantly different at p>0.05, NFE: Nitrogen free extract

DISCUSSION

Malaysian mahseer is a slow-growing species which takes a longer time to reach to marketable size compared to other carp species (Ingram et al., 2005; Ng et al., 2008). The specific growth rate of T. tambroides in this study (0.29-0.52% day-1) was similar to those reported by Ramezani-Fard et al. (2012), Kamarudin et al. (2011) and Misieng et al. (2011). However, this rate was lower than the other Tor species. Indian mahseer T. putitora grows at 1.5-1.8% day-1 (Rahman et al., 2005).

A longer culture period definitely increases the production cost through the feed, labour and maintenance costs. In addition, Malaysian mahseer requires high dietary protein Ng et al. (2008) and Misieng et al. (2011) which in turn correlates with a higher feed price due to the use of more fishmeal as the main protein source in the feed. Fishmeal supply is very limited, so its price inflates as the demand goes up every year (Shapawi et al., 2007). To reduce the fishmeal dependency and feed price, fishmeal needs to be partially or fully replaced by other alternative protein sources. Alternative protein sources such as POM or poultry by product meal, soybean meal, animal protein mixture and bone and meat meal have been studied by several researchers (Yang et al., 2004; Hernandez et al., 2007; Wang et al., 2008; Adewolu et al., 2010). However, most of these alternatives can be considered as a partial substitute for fishmeal. POM is a protein source mainly used in pet foods because of its palatability, high quality protein and essential fatty acids, vitamins and minerals (Cruz-Suarez et al., 2007). A high quality POM contains about 70% crude protein and relatively low ash content (Nengas et al., 1999; Davis and Arnold, 2000) and it is suggested that this feed stuff can be partially or fully substituted for fishmeal (Ogale, 2002). Shapawi et al. (2007) expressed that POM has a high potential to be integrated in the diet of carnivorous fish species such as groupers. In agreement with our findings, Takagi et al. (2000) also suggested that POM can be used in fish diet without any significant depression in fish performance. It should be considered that 50% replacement of dietary fishmeal with POM will lead to a cost reduction of about 10-14% per ton of feed (Cruz-Suarez et al., 2007).

The FCR values of 3.27 to 5.79 have been recorded in this study. Misieng et al. (2011) observed better FCR values of 2.19 to 3.02 for T. tambroides while Ramezani-Fard et al. (2012) and Kamarudin et al. (2011) reported FCR values of 1.4-2.0. The range of FCR in well-prepared fish diets is generally between 1.2 and 1.5 (De Silva and Perera, 1985). However, the FCR trend in the present study was in agreement with the earlier research in which FCR in the diets of some fish such as gibel carp (Yang et al., 2006) and humpback grouper (Shapawi et al., 2007) decreases with increasing inclusion of POM. The PER found in this study (0.08-0.14) was slightly higher than that was reported for Malaysian mahseer by Misieng et al. (2011) [0.06-0.11]. High PER suggested that fish were able to digest the diets containing POM and to absorb their nutrients efficiently.

The study showed that fishmeal can be fully replaced by POM in the Malaysian mahseer diet without any adverse effect on its growth performance and feed utilization. Yang et al. (2006) reported that high quality poultry by Product meal (PBM) can fully replace fishmeal in the diet of gibel carp. However they recommended an optimal fishmeal replacement of only 66.5%. In contrast, Emre et al. (2003) and Zabihi et al. (2011) reported a reduction in the growth of mirror carp, Cyprinus carpio fingerlings with the increase of dietary PBM level. This is due to the limited amino acids and the low digestibility of feather connective tissue and skin content in PBM. However, POM used in this study did not contain any feather materials.

Earlier works indicated that only 50% of fishmeal can be replaced by poultry by product meal in the diets of rainbow trout (Steffens, 1994), Clarias gariepinus (Adewolu et al., 2010) and prawns (Yang et al., 2004) without affecting their growth. Usman et al. (2007) also reported that poultry offal silage meal can only replace up to 37% of fishmeal in the diet of tiger grouper, Epinephelus fuscoguttatus without any adverse effects on fish productivity.

This study showed that the body composition of T. tambroides was not affected by the replacement of fishmeal with POM. Similar findings regarding the effects of diets on the body composition of Malaysian mahseer have been reported. Misieng et al. (2011) noted that an increase in the dietary protein level of T. tambroides does not affect its body protein, fat and NFE but increases its body ash content. Ramezani-Fard et al. (2012) also reported that the body composition of T. tambroides does not change when fish are fed with diets containing low or high omega-3 and low or high saturated fatty acids. However, Kamarudin et al. (2011) found that dietary lipid sources affect the body fat content of T. tambroides. The increase of whole body fat content has been observed in rainbow trout (Steffens, 1994) and mirror carp (Emre et al., 2003) when they are fed with POM diets. However, the negative trend occurs in mirror carp (Emre et al., 2003; Zabihi et al., 2011). In the other hand, no differences in whole body moisture and fat are found in gibel carp (Yang et al., 2006) and humpback grouper (Shapawi et al., 2007) when POM is included in their diets. However, the whole body protein and energy content in gibel carp fed POM diets are slightly higher than those fed fishmeal diet (Yang et al., 2006). Omole et al. (2008) reported that fat content of POM is higher than fat content of some local fishmeal.

CONCLUSION

In the present study, it is concluded that poultry offal meal could fully replace fishmeal in the diet of Malaysian mahseer (Tor tambroides) fingerlings without affecting the survival rate, growth performance and whole body proximate composition.

ACKNOWLEDGMENTS

The authors would like to thank Dinding Soya and Multifeeds Sdn Bhd (Malaysia) for the supply of poultry offal meal. This project was funded by the Malaysian Government through E-Science grant no. 05-01-04-SF0209.

REFERENCES

1:  Adeniji, A.A., 2008. Effects of feeding three protein sources with or without fishmeal supplementation on the performance of growing grasscutters. Asian J. Anim. Vet. Adv., 3: 98-103.
CrossRef  |  Direct Link  |  

2:  Adewolu, M.A., N.B. Ikenweiwe and S.M. Mulero, 2010. Evaluation of an animal protein mixture as a replacement for fishmeal in practical diets for fingerlings of Clarias gariepinus (Burchell, 1822). Isr. J. Aquacult. Bamidgeh, 62: 237-244.
Direct Link  |  

3:  AOAC., 1997. Official methods of analysis of the Association of Analytical Chemists. 16th Edn., Association of Official Analytical Chemist, Washington, DC., USA

4:  Cruz-Suarez, L.E., M. Nieto-Lopez, C. Guajardo-Barbosa, M. Tapia-Salazar, U. Scholz and D. Ricque-Marie, 2007. Replacement of fishmeal with poultry by-product meal in practical diets for Litopenaeus vannamei and digestibility of the tested ingredients and diets. Aquaculture, 272: 466-476.
CrossRef  |  

5:  Dale, N., B. Fancher, M. Zumbado and A. Villacres, 1993. Metabolizable energy content of poultry offal meal. J. Appl. Poult. Res., 2: 40-42.
Direct Link  |  

6:  Davis, D.A. and C.R. Arnold, 2000. Replacement of fishmeal in practical diets for the pacific white shrimp, Litopenaeus vannamei. Aquaculture, 185: 291-298.

7:  De Silva, S.S. and M.K. Perera, 1985. Effects of dietary protein level on growth, food conversion and protein use in young Tilapia nilotica at four salinities. Trans. Am. Fish. Soc., 114: 584-589.
CrossRef  |  Direct Link  |  

8:  Emre, Y., H. Sevgili and I. Diler, 2003. Replacing fish meal with poultry by-product meal in practical diets for mirror carp (Cyprinus carpio) fingerlings. Turk. J. Fish. Aquatic., 3: 81-85.

9:  Hernandez, M.D., F.J. Martinez, M. Jover and B.G. Garcia, 2007. Effects of partial replacement of fishmeal by soybean meal in sharpsnout seabream (Diplodus puntazzo) diet. Aquaculture, 263: 159-167.
CrossRef  |  

10:  Hlophe, S.N. and N.A.G. Moyo, 2011. The effect of different plant diets on the growth performance, gastric evacuation rate and carcass composition of Tilapia rendalli. Asian J. Anim. Vet. Adv., 6: 1001-1009.
CrossRef  |  

11:  Hlophe, S.N., N.A.G. Moyo and J.R. Sara, 2011. Use of kikuyu grass as a fishmeal substitute in practical diets for Tilapia rendalli. Asian J. Anim. Vet. Adv., 6: 1076-1083.
CrossRef  |  

12:  Hu, M., Y. Wang, Q. Wang, M. Zhao and B. Xiong et al., 2008. Replacement of fishmeal by rendered animal protein ingredients with lysine and methionine supplementation to practical diets for gibel carp, Carassius auratus gibelio. Aquaculture, 275: 260-265.
Direct Link  |  

13:  Ingram, B., S. Sungan, G. Gooley, S.Y. Sim, D. Tinggi and S.S. De Silva, 2005. Induced spawning, larval development and rearing of two indigenous Malaysian mahseer, Tor tambroides and T. douronensis. Aquacult. Res., 36: 983-995.
CrossRef  |  Direct Link  |  

14:  Ismail, M.F.S., S.S. Siraj, S.K. Daud and S.A. Harmin, 2011. Association of annual hormonal profile with gonad maturity of mahseer (Tor tambroides) in captivity. Gen. Comp. Endocrinol., 170: 125-130.
CrossRef  |  

15:  Kamarudin, M.S., E. Ramezani-Fard, C.R. Saad and S.A. Harmin, 2011. Effects of dietary fish oil replacement by various vegetable oils on growth performance, body composition and fatty acid profile of juvenile Malaysian mahseer, Tor Tambroides. Aquacult. Nutr.
CrossRef  |  

16:  Millamena, O.M., 2002. Replacement of fishmeal by animal by-product meals in a practical diet for grow-out culture of grouper Epinephelus coioides. Aquaculture, 204: 75-84.
CrossRef  |  

17:  Misieng, J.D., M.S. Kamarudin and M. Musa, 2011. Optimum dietary protein requirement of Malaysian mahseer (Tor tambroides) fingerling. Pak. J. Biol. Sci., 14: 232-235.
CrossRef  |  Direct Link  |  

18:  Nandeesha, M.C., G. Bhadraswamy, J.G. Patil, T.J. Varghese, K. Sarma and P. Keshavananth, 1993. Preliminary results on induced spawning of pond-raised mahseer, Tor khudree. J. Aquac. Trop., 8: 55-60.

19:  Nengas, I., M.N. Alexis and S.J. Davies, 1999. High inclusion levels of poultry meals and related by-products in diets for gilthead seabream Sparus aurata L. Aquaculture, 179: 13-23.
CrossRef  |  

20:  Ng, C.K., 2004. Kings of the Rivers: Mahseer in Malaysia and the Region. Inter Sea Fishery, USA., ISBN: 9789834170400, Pages: 170

21:  Ng, W.K., N. Abdullah and S.S. de Silva, 2008. The dietary protein requirement of the Malaysian mahseer, Tor tambroides (Bleeker) and the lack of protein-sparing action by dietary lipid. Aquaculture, 284: 201-206.
CrossRef  |  

22:  Nguyen, T.T.T., B. Ingram, S. Sungan, G. Gooley, S.Y. Sim, D. Tinggi and S.S. de Silva, 2006. Mitochondrial DNA diversity of broodstock of two indigenous mahseer species, Tor tambroides and T. douronensis (Cyprinidae) cultured in Sarawak, Malaysia. Aquaculture, 253: 259-269.
CrossRef  |  Direct Link  |  

23:  Ogale, S.N., 2002. Mahseer Breeding and Conservation and Possibilities of Commercial Culture. In: The India Experience, Petr, T. and D.B. Swar (Eds.). Tata Power Company Ltd., Lonavla, pp: 193-212

24:  Omole, A.J., O.T. Iji, B.A. Makanjuola and J.B. Fapohunda, 2008. Nutritional value of chicken offal as replacement for local fish meal in growing snails. J. Cell Anim. Biol., 2: 96-99.
Direct Link  |  

25:  Rahman, M.A., M.A. Mazid, M.R. Rahman, M.N. Khan, M.A. Hossain and M.G. Hussain, 2005. Effect of stocking density on survival and growth of critically endangered mahseer, Tor putitora (Hamilton), in nursery ponds Aquaculture, 249: 275-284.
CrossRef  |  Direct Link  |  

26:  Ramezani-Fard, E., M.S. Kamarudin, C.R. Saad and S.A. Harmin, 2011. Changes over time in muscle fatty acid composition of Malaysian mahseer, Tor Tambroides, fed different dietary lipid percentage. Afr. J. Biotechnol., 10: 18256-18265.
Direct Link  |  

27:  Ramezani-Fard, E., M.S. Kamarudin, S.A. Harmin, C.R. Saad, M.K. Abd Satar and S.K. Daud, 2011. Ontogenic development of the mouth and digestive tract in larval Malaysian mahseer, Tor tambroides Bleeker. J. Applied Ichthyol., 27: 920-927.
CrossRef  |  

28:  Ramezani-Fard, E., M.S. Kamarudin, S.A. Harmin and C.R. Saad, 2012. Dietary saturated and omega-3 fatty acids affect growth and fatty acid profiles of Malaysian mahseer. Eur. J. Lipid Sci. Tech., 114: 185-193.
CrossRef  |  

29:  Siraj, S.S., Z. Kamaruddin, M.K.A. Satar and M.S. Kamarudin, 1988. Effects of feeding frequency on growth, food conversion and survival of red tilapia (Oreochromis mossambicus/O. niloticus) hybrid fry. Proceedings of the 2nd International Symposium on Tilapia in Aquaculture, March 16-20, 1987, Bangkok, Thailand, pp: 383-386

30:  Takagi, S.T., H. Hosokawa, S. Shimeno and M. Ukawa, 2000. Utilization of poultry by-product meal in a diet for red sea bream Pagrus major. Nippon Suisan Gakkaishii, 66: 428-438.
Direct Link  |  

31:  Thomas, H.S., 1897. The Rod in India: Being Hints how to Obtain Sport, With Remarks on the Natural History of Fish and their Culture and Illustrations of Fish and Tackle. 3rd Edn., W. Thacker, UK., Pages: 435

32:  Usman, R., N.N. Palinggi and T. Ahmad, 2007. Utilisation of local feed ingredients in tiger grouper grow out moist diets. Aquacult. Asia Mag., 12: 33-36.
Direct Link  |  

33:  Wang, Y., K. Li, H. Han, Z.X. Zheng and D.P. Bureau, 2008. Potential of using a blend of rendered animal protein ingredients to replace fishmeal in practical diets for malabar grouper (Epinephelus malabricus). Aquaculture, 281: 113-117.
CrossRef  |  

34:  Yang, Y., S. Xie, Y. Cui, X. Zhu, W. Lei and Y. Yang, 2006. Partial and total replacement of fishmeal with poultry by-product meal in diets for gibel carp, Carassius auratus gibelio Bloch. Aquacult. Res., 37: 40-48.
CrossRef  |  

35:  Yang, Y., S. Xie, W. Lei, X. Zhu and Y. Yang, 2004. Effect of replacement of fishmeal by meat and bone meal and poultry by-product meal in diets on the growth and immune response of Macrobrachium nipponense. Fish Shellfish Immun., 17: 105-114.
CrossRef  |  PubMed  |  

36:  Zabihi, A., M. Faramarzi, M. Lashkarbolouki, S. Kiaalvandi and F. Iranshahi, 2011. Effect of chicken slaughter wastes on growth and feeding parameters and body composition of common carp (Cyprinus carpio). J. Res. Biol., 2: 122-128.

37:  Steffens, W., 1994. Replacing fish meal with poultry by-product meal in diets for rainbow trout, Oncorhynchus mykiss. Aquaculture, 124: 27-34.
CrossRef  |  

38:  Shapawi, R., W.K. Ng and S. Mustafa, 2007. Replacement of fish meal with poultry by-product meal in feeds formulated for the polka-dot grouper, Cromileptes altivelis. Aquaculture, 273: 118-126.
CrossRef  |  

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