Effects of substitution of freshwater shrimp meal (Caridina nilotica Roux) with hydrolyzed feather meal on growth performance and apparent digestibility in Nile tilapia (Oreochromis niloticus L.) under different culture conditions

J M Munguti, H Waidbacher*, D M Liti**, M Straif* and W J Zollitsch***

Kenya Marine & Fisheries Research Institute, Sangoro Aquaculture Station, P.O Box 136 PAP-Onditi Kisumu, Kenya
* BOKU- University of Natural Resources and Applied Life Sciences Vienna, Department of Water, Atmosphere and Environment, 17 Max-Emanuel-Straße, A-1180 Vienna, Austria
** Moi University, Department of Biological Sciences, P.O Box 1125 Eldoret, Kenya
*** BOKU- University of Natural Resources and Applied Life Sciences Vienna, Department of Sustainable Agricultural Systems, Division of Livestock Sciences, Gregor Mendel-Straße 33, A-1180 Vienna, Austria
werner.zollitsch@boku.ac.at

Abstract

The effects of substituting hydrolysed feather meal (HFM) for freshwater shrimp meal (FSM;  Caridina nilotica, Roux) on growth, digestibility and survival in Nile tilapia (Oreochromis niloticus L.) were evaluated under laboratory and practical culture conditions. Fingerlings with mean ranges of 26.0-26.5 and 35.4-37.0 g were held indoor in aquaria with recirculating water, and in cages that were installed in 800 m² fertilized pond, respectively. Five isocaloric (12.3 kJ g^-1) diets, containing between 28.5 and 31.0 % of crude protein, were prepared by gradually substituting HFM for FSM at rates of 0, 25, 50, 75 and 100% and fed to fish in aquaria; tilapia in cages were fed diets at substitution levels 0, 50 and 100%. All fish were fed at 10 % of body weight day^-1 in three replicates for 84 days.

Results indicated that substitution of HFM for FSM at levels above 50% led to significant (P<0.05) growth reductions in aquaria. However, even 100% substitution rate did not significantly (P>0.05) affect growth of fish in the cages. In both experiments, survival was similar among treatments, but apparent protein digestibility decreased with increasing levels of HFM in the diet.

In conclusion, at least 50% substitution of HFM for FSM is possible in semi-intensive culture of Oreochromis niloticus, where natural food is available and where moderate growth performance levels may be accepted.

Key words: amino acids, aquaria, cage, nutrients, ponds

Introduction

Production of farmed tilapia is among the fastest expanding food sectors in the world. Nile tilapia is the most cultured freshwater species among the farmed tilapias and contributes about 71 % of the total tilapia production (FAO 2002). However, the sustenance and expansion of production is limited by the high cost of fish feeds, which comprise over 50% of the production costs (Craig and Helfrich 2002). Protein usually is the most expensive nutrient and its level and quality determine the cost of fish feeds (Tacon 1993).

Most fish feeds contain a proportion of animal protein, which is considered superior to other sources in terms of palatability and nutrient availability (Tacon 1993; Hardy and Tacon 2002). The majority of fish feeds contain fish or shrimp meal as the main sources of dietary animal protein. However, due to worldwide decline in fishery products, fish and shrimp meals are increasingly becoming scarce and expensive (Mohsen and Lovell 1990). Consequently, nutritionists and feed manufacturers have been searching for alternative dietary animal protein from non-conventional sources to replace the conventional sources and reduce feed costs (El-Sayed 1998; Abdelghany 2003; Liti et al 2005). In Kenya, Omena (Rastrineobola argentea) and Freshwater Shrimp Meal (FSM) are commonly used as animal protein sources in fish feeds. However, Rastrineobola argentea is used for human food while FSM, a by-product of the Omena (Rastrineobola argentea) fishery in Lake Victoria is increasingly becoming scarce and expensive due to frequent closures of the lake’s fishery (Munguti et al 2006). Therefore, the replacement of FSM by cheaper and available animal protein feedstuffs is likely to contribute to reduce the costs of Oreochromis niloticus feeds.

Feather meal is high in protein (Tacon et al 1984), and could be incorporated into tilapia feeds after hydrolyzation. Previous studies have indicated that hydrolyzed feather meal (HFM) could only partially substitute fish meal without growth reduction in several fish species (Falaye 1982; Steffens 1994; Bishop et al 1995; Hasan et al 1997; Mendoza et al 2001). Improvement on the utilization of feather meal has mainly been based on two approaches, the direct supplementation of limiting amino acids (Murai et al 1982; Webster et al 1991), and the application of different techniques of hydrolyzation (Moran et al 1966; Tiews et al 1979; Hughes 1990; Steffens 1994; Mendoza et al 2001). However, direct amino acid supplementation may not be economically viable given their high cost and the low prices fetched by tilapias in developing sub-Saharan African countries. Furthermore, many investigators have expressed doubts on the viability of supplementing free amino acids in diets for tilapias, since free amino acids are assimilated long before the accompanying polypeptides, and before whole proteins are broken down; therefore, they are not presented at the same time for tissue formation (Jauncey 1982). On the contrary, tilapias are reported to utilize free dissolved amino acids in natural waters (Bowen 1980). Since Oreochromis niloticus feed continuously under semi-natural conditions (Getachew 1989), it is possible that a continuous supply of amino acids from the natural food web may have a potential in improving the nutritive value of feather meal under semi-intensive culture conditions.

The current study was conducted to analyse the effects of gradual substitution of freshwater shrimp meal by hydrolyzed feather meal on growth, apparent digestibility and survival of Oreochromis niloticus under semi-intensive culture conditions. Furthermore, potential differences in the response of fish kept in aquaria and those kept in cages under semi-intensive management should be recorded.

Materials and methods 

Site and experimental facilities

The study was conducted at Sagana Fish Farm (90 km northeast of Nairobi, altitude 1230 m, latitude 0°39´S and longitude 37°12´E). Two experiments were conducted, one in laboratory aquaria, each with a dimension of 0.45 x 0.3 x 0.3 m, and the other in net cages consisting of a top and bottom frames measuring 1.2 x 0.94 m and 0.9 x 0.9 m, respectively. Each cage had a height of 0.75 m and all cages were installed in a single earthen pond measuring 20 x 40 x 1.0 m. The aquaria were connected in a thermoregulated recirculating system, comprising a settling tank for solid removal and a tickling bio-filter to remove ammonia.

Pond management and water quality

The pond was fertilized weekly at a rate of 20 kg N and 8 kg P ha^-1 with urea and diammonium phosphate, respectively. Liming was done once at 2500 kg ha^-1 with CaCO₃ at the beginning of the experiment. Water quality was assessed by measuring temperature, pH, dissolved oxygen and chlorophyll a. The parameters were measured three times a week both in the aquaria and the cages. Dissolved oxygen was measured using model 57 oxygen meter (YSI industries, Yellow springs, OH, USA), while a glass electrode-pH meter, Hi-9024 microcomputer (Hanna Instruments Ltd., Chicago, IL, USA), was used to measure pH. Chlorophyll a was determined as described in APHA (1990).

Sources and processing of feedstuffs

Fresh chicken feathers were collected from hotels around Sagana town and were sun-dried. The feathers were ground using a hammer mill and were then mixed with a solution of NaOH (5 g/l) at a ratio of 0.5 l per 1 kg of feathers. Thereafter, ground feathers were hydrolysed in an autoclave at 16 psi and about 110°C for 3 hours. The hydrolysed feather meal was sun-dried and further ground into a fine powder using a blender. A batch of freshwater shrimp was purchased from supply stores in Kisumu, and cotton seed cake from a local feed manufacturer. Wheat bran was purchased from a local wheat-processing factory. The freshwater shrimp and wheat bran were ground using a hammer mill.

Proximate analysis and diet formulation

The processed ingredients were subjected to proximate analysis before formulation of experimental diets. The analysis was carried out as described in AOAC (1990) and in triplicates. Feedstuffs were analysed for crude protein (CP), ether extracts (EE), ash, nitrogen-free extracts (NfE), and crude fibre (CF). CP was estimated from Kjeldahl nitrogen by multiplication with a factor of 6.25, while EE were quantified through the loss in weight after extraction of the sample with petroleum ether (boiling point 40-60^oC). Ash was determined by ashing dry samples in a muffle furnace at 550^oC for 4 hours. CF was determined as the ash-free residues of a digestion process in alkaline and acidic solution. NfE was determined by the difference method (dry matter-CP-EE-CF-Ash). The proximate composition of feed ingredients is shown in Table 1.

Diet formulation and preparation

Five experimental diets, each formulated to contain 30 % of CP and 12.3 kJ g^-1 digestible energy were produced by including 0, 2.25, 4.5, 6.75 and 9.4 % of HFM, together with small amounts of Carboxyl methyl cellulose as a filler material instead of FSM, thereby representing substitution rates of 0, 25, 50, 75 and 100%, respectively (Table 2).

Each ingredient was homogeneously ground to pass through a 200mm sieve. The formulations were made by mixing the necessary ingredients into a homogenate, which was moistened before passing through a modified meat mincer. The resulting expeller-like strands were sun-dried and stored at room temperature. The amino acid profiles of feed ingredients are shown in Table 3.

 Experimental animals, design and feeding

The diets were randomly allocated to groups of hand-sexed male Oreochromis niloticus fingerlings that were held in aquaria and cages. Those in aquaria were fed all the five diets in five treatments, while the caged fish were fed diets at substitution levels of 0, 50 and 100% in three treatments; both experiments had three replicates per treatment. The initial average stocking weight in aquaria and cages were 26 and 36g, respectively, at densities of 6 and 15 fish, respectively. Fish were acclimatised for two weeks prior to the start of each experiment. Feed was offered at 10% of body weight per day for 84 days. Sampling was done on a bi-weekly basis to monitor growth and adjust feeding rates. Fish were fed using the automated feeders described by Waidbacher et al (2006). The feeders were calibrated to deliver feed continuously between 8.00 and 18.00 hrs. At the end of the study, all fish from cages and aquaria were harvested, weighed and counted.

Evaluation of performance traits

Final harvest mean weight, weight gain, specific growth rate and apparent protein digestibility coefficient were measured. Specific growth rate (SGR) was calculated using the following equation:

Where W_i and W_f are the initial and final mean body weights, respectively and t is time in days from stocking to harvest.

The apparent digestibility coefficient for protein (ADC_p) was determined using acid-insoluble ash (AIA) as the indigenous inert marker. The following formula was applied:

 (adjusted from Maynard and Loosli 1962)

Where CP_f is faecal CP, CP_d is the dietary CP; AIA_d is the marker in the diet and AIA_f is the marker in the faeces. The ash content was analyzed by ashing the sample in a furnace at 550°C for 6 hours. The residue was then treated with HCl (2.5 %) and afterwards was ashed again for 2 hours, the residue representing acid-insoluble ash (AOAC 1990).

Data analysis

Statistical analysis was performed using SPSS (2006) statistical software package. Data were subjected to a one-way analysis of variance. Where appropriate, data were transformed to conform to the requirements for the test. Duncan multiple range test was applied to identify means that were significantly different from each other (Duncan 1955). The relationship between HFM inclusion level and ADC_p was evaluated by applying linear regression analysis as described by Sokal and Rohlf (1981). A type I error of 0.05 was used to define significance.

Results 

Water quality

Water quality parameters did not vary significantly (P≥0.05) among treatments, both in cages and aquaria during the experimental period. Mean value for chlorophyll a was 162.4±17.1 mg m^-3. The mean ranges for dissolved oxygen values in the cages were 3-10 mg L^-1. (mean: 6.2 mg L^-1.). Water temperature in cages ranged from 24.3 to 28.9 ^oC (mean: 27.0±0.5 ^oC) in the pond,while the water temperature was maintained between 26 and 28^oC (mean: 27.0±0.04^oC) in the aquaria. The pH values ranged from 7.8 to 8.3 (mean: 8.1±0.03) in the experimental pond and 7.0-7.5 (mean: 7.2±0.01) in the aquaria. In all cases, water quality parameters were within the values recommended for tilapia culture.

Growth performance

Data on fish growth performance for aquaria and cages are presented in Table 4 and 5, respectively.

Fish that were fed diets containing 0, 25 and 50% HFM in aquaria had similar mean weight, specific growth rate and percent weight gain and grew significantly better (P<0.05) than those fed diets in which 75 and 100% of FSM were substituted for HFM. However, there were no significant differences (P≥0.05) in growth performance between the 0, 50 and 100% HFM diet in the cages. Survival rate was high and very similar (P>0.05) among treatments both in aquaria and cages. Growth curves for Oreochromis  niloticus in aquaria and cages are presented in Figures 1 and 2, respectively.

After about two weeks from the time of stocking, fish receiving diets in which 0 to 50% of FSM had been substituted for HFM differed from the other treatments in the aquaria experiment.

Protein digestibility

Data on apparent protein digestibility (ADC_p) of fish in aquaria and cages are shown in Table 6 and Figure 3.

There were significant differences (P<0.05) in ADC_p between all treatments in the aquaria experiment. The ADC_p decreased with increasing levels of HFM both in aquaria and cages, with regression slopes of -0.26±0.02 and -0.098±0.02, respectively. In cages, only the 100 % treatment showed reduced ADC_p.

Discussion 

Data from the present study indicate that the growth of groups of Oreochromis niloticus that were fed diets containing a mixture of freshwater shrimp (FSM) and hydrolyzed feather meal (HFM) protein in cages was similar to those fed FSM as the only source of animal protein (control treatment). However, growth significantly declined when fish were fed diets containing over 4.5 % of HFM (i.e. 75-100 % FSM-substitution level) in aquaria.

The differences in growth performance between the caged and aquaria fish in the present study may be attributed to different culture conditions. The aquaria experiment in the present study took place in indoor laboratory environments, while the cage experiment was conducted in a fertilized earthen pond. This setup probably allowed for some extra nutrition from natural food in the pond, which may have supplemented potentially deficient dietary amino acids. HFM has been reported to be deficient in certain essential amino acids (Falaye 1982; Tacon et al 1984; Mendoza et al 2001); therefore, the interaction between the components of pond’s natural food and feather meal may have improved the essential amino acid supply from the latter, thus resulting in better utilization and growth performance of fish in the cages. It should however be noted that these results were derived at an overall moderate level of performance, which can be considered as typical for the given setting, representing semi-intensive production under East African conditions.

The findings from the aquaria experiment are similar to those reported by other investigators. Falaye (1982) did not observe a significant decrease in growth parameters of Oreochromis niloticus when 50 % of fish meal was substituted for HFM. Similar results were reported by Viola and Zohar (1984), who concluded that up to 50 % of fish meal could be replaced by poultry by-products in diets of tilapia hybrids without deleterious effects on fish growth. However, Bishop et al (1995) reported a slightly higher substitution level (66 %) of fish meal protein for HFM protein in diets for Oreochromis niloticus without significant reduction in growth. The higher substitution level reported by these authors as compared to that from the aquaria experiment of the present study may be attributed to differences in culture conditions. The present experiment was conducted in aquaria, which were cleaned every day, while that of Bishop et al (1995) was conducted in concrete tanks where some development of autotrophs and heterotrophs was possible.

The decrease in growth observed in fish fed diets containing over 4.5 % HFM (i.e. substitution rates above 50 %) and kept in aquaria may be due to sub-optimal intake of essential amino acids (Jauncey and Ross 1982; NRC 1983; Santiago and Lovell 1988) from HFM, which might have hindered proper utilization of dietary HFM protein and its subsequent synthesis to body protein. Attempts have been made to improve the nutritive value of feather meal-based diets for some aquatic species by supplementation of deficient amino acids (Tiews et al 1979; Hughes 1990; Steffens 1994). However, Falaye (1982) reported a decreased performance of fish growth when HFM contributed over 50% of the animal protein even after some deficient amino acids were supplemented. The author suggested that growth inhibition might have involved factors other than amino-acid imbalances.

Reports on utilization of supplementary amino acids are variable and conflicting, with some authors reporting improved growth of fish after supplementation (Murai et al 1982; Webster et al 1991), while others report no response in growth (Ng and Wee 1979; El-Sayed 1990). Other investigators have suggested that the utilization of amino acids is dependent on meal frequencies (Webster et al 1991): channel catfish fed once a day, may not sufficiently utilize supplemented synthetic amino acids for protein synthesis, but growth was improved to the level of the control when diets containing L-lysine were fed twice a day. Under natural or semi-natural conditions, Oreochromis niloticus feed continuously during day time (Getachew and Fernando 1989; Zenebe and Getachew 1998), thus based on the hypothesis of meal frequency, utilization of free amino acids might be enhanced. Bowen (1980) reported that tilapias can thrive well on naturally occurring dissolved amino acids. This mode of feeding would ensure that free amino acids were supplied continuously at the site of tissue formation. The observation by Bowen (1980) and the lack of differences between the control and the diets containing HFM in the cages in growth performance in the present study suggest that the supply of amino acids from natural food may be an economically attractive strategy of supplementing limiting amino acids in tilapia diets.

The method used to process feathers in the present study produces two categories of essential amino acids, a batch of free amino acids and those contained in the remaining polypeptides and intact protein. The set of free essential amino acids is likely to be irreversibly absorbed before those in the polypeptides and intact protein are liberated for tissue protein synthesis (Yamada et al 1981; Cowey and Walton 1988), eventually leading to poor utilization of feather meal. However, the continuous supply of amino acids from natural food could enhance utilization of feather meal by upgrading the profile of both free essential amino acids, and those contained in polypeptides and protein after liberation.

In the present study, ADC_p declined with increasing levels of HFM in the diets. This trend agrees with that reported by Degani et al (1997) and Yang et al (2006), who observed a similar decrease in ADC_p with increasing levels of feather meal in Carp (Cyprinus carpio L.) and gibel carp (Carassius auratus gibelio Bloch), respectively. The regression slope for apparent protein digestibility (b=-0.098) of feather meal based diets in the cage experiment was less negative than the values calculated for fish in aquaria (b=-0.26), suggesting a less pronounced depression of protein digestibility in a pond environment. Several factors emerging from the pond environment may have contributed to these differences: Algae or algal based diets are reported to stimulate secretion of copious amounts of gastric acid in Oreochromis niloticus and Oreochromis mossambicus (Bowen 1981; Getachew 1987, 1989); this may have led to a more acidic medium and eventually in an enhanced ADC_p. On the other hand, ADC_p in the cage environment was probably even systematically underestimated herein, as it was technically not feasible to properly account for the additional intake of natural food in the digestibility study.

In conclusion, the present study demonstrated that hydrolyzed feather meal could substitute freshwater shrimp meal at least up to 50% in the diets of Oreochromis niloticus if the level of growth performance aimed at is below maxiumum. If fish have the chance to feed on materials from a pond under semi-intensive culture conditions, an even higher substitution rate may be possible without compromising growth.

Acknowledgements 

The authors thank the Austrian Development Cooperation through ÖAD North-South Dialogue scholarship programme and the Department of Water, Atmosphere and Environment of BOKU-University of Natural Resources and Applied Life Sciences Vienna, for providing financial support to this project. Members of Sagana Aquaculture Center and Kenya Marine and Fisheries Research Institute (KMFRI) are acknowledged for their immense support to the project. We are grateful to Silke Drexler for her help in the preparation of this paper.

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Received 24 February 2009; Accepted 8 May 2009; Published 5 August 2009

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