Replacing fish meal with locally available feed ingredients to reduce feed costs in cultured Nile tilapia (Oreochromis niloticus)

Francis Pius Mmanda^1,2,3, Torbjörn Lundh¹, Anna Norman Haldén⁴, Matern S P Mtolera², Rukia Kitula² and Jan Erik Lindberg¹

¹ Department of Animal Nutrition and Management, Swedish University of Agricultural Sciences, PO Box 7024, SE-75007 Uppsala, Sweden
Torbjorn.Lundh@slu.se
² Ministry of Livestock and Fisheries, PO Box 2847, Dodoma, Tanzania
³ Institute of Marine Sciences, University of Dar es Salaam, PO Box 668, Zanzibar, Tanzania
⁴ Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences, PO Box 7028, SE-75007 Uppsala, Sweden

Abstract

A 60-day growth trial was conducted to evaluate growth performance, nutrient utilisation, carcass traits and feeding costs in Nile tilapia juveniles (1.47± 0.31 g body weight) fed diets in which 50% of fishmeal dry matter (DM) in the reference diet (REFD) was replaced with cattle blood, fish frames, freshwater shrimp or brewery spent yeast on a DM basis. The fish were fed 10% of body weight three times a day for the first 30 days, and then 5% of body weight twice a day for the remaining 30 days of the feeding trial. Due to high feed intake, the highest weight gain, final weight and average daily weight gain were recorded in fish fed REFD. Feed conversion ratio was lower in the diet with cattle blood than in the other diets and the protein efficiency ratio were higher for REFD than for the other diets. There were no differences in survival rate, condition factor, hepatosomatic index and viscerosomatic index between treatments. Initial and final whole body composition differed, but there were no differences in carcass traits between treatments. Feed costs per kg feed and feed costs per weight gain were reduced when fishmeal was replaced with locally available feed ingredients, with the largest reduction in feed costs per kg feed (34%) and per weight gain (27.1%) obtained with brewery spent yeast. The results indicate that the economics of small-scale tilapia production in Tanzania can be improved by replacing fishmeal with good-quality, low-cost, locally available feed ingredients.

Kew words: carcass traits, feed ingredients, feed utilization, growth performance

Introduction

Aquaculture is one of the world’s fastest growing and most food producing sector, with a total production of 82 million metric tonnes which accounted for 46% of the total world fish production in 2018 (FAO (Food and Agriculture organisation) 2020). A major part of the growth in this sector is taking place in Asia, while there is a low growth rate in Africa.

In Tanzania, aquaculture practices have been operating since the 1950s (Mallya, 2007), but remained limited in scope until the 1980s due to poor farming methods and technologies, poor management and low availability of good-quality fish feeds and seeds (Mmanda et al 2020; URT 2016). The number of earthen fish ponds has now increased, from 14,100 in 2004 (Mallya 2007) to 26,445 in 2019, producing in total around 18,082 MT annually (URT 2019). Fish farming in Tanzania is dominated by small-scale rural freshwater ponds. This small-scale aquaculture helps to increase the diversity of food production in Tanzania and to reduce the risk of poverty (Mulokozi et al 2020).

Nile tilapia (Oreochromis niloticus) is the most commonly cultured fish species in Tanzania (Chenyambuga et al 2014; Kaliba et al 2006; Mmanda et al 2020). The popularity of Nile tilapia is due to its market acceptability, fast growth rate, resistance to disease and ability to grow on a wide range of diets. It is also very tolerant to a wide range of environmental conditions, has the ability to reproduce readily in captivity and has high prolific rate, and good carcass taste (Fitzsimmons 2000; Murnyak 2010). To reduce their production costs, in the past most tilapia fish farmers relied on locally available feed ingredients to supplement the diet of their cultured fish (Mmanda et al 2020). In Tanzania, studies have evaluated fly maggots (Hezron et al 2019), cassava leaves (Madalla et al 2016) and moringa leaves (Madalla et al 2013) as feed ingredients for tilapia.

Fish meal is considered the ideal conventional protein source in commercial fish feeds for most fish species in the aquaculture industry, due to its essential amino acid and fatty acid profile and its high content of vitamins, minerals, attractants and other unknown growth factors (El-Sayed 2006; Kubiriza et al 2016; NRC 2011; Tacon and Metian 2008). The continuous increase in aquaculture production and the expansion of other food industries create enormous demand for fish meal and fish oil in commercial feed, with the price increasing accordingly (Tacon and Metian 2008). Therefore, identification of cheap, non-conventional feed protein ingredients would improve the long-term sustainability of tilapia culture, both with respect to resource utilisation and due to lower feeding costs.

Globally, the effects of fish meal alternatives on growth performance of cultured tilapia species have been extensively studied (e.g. Kubiriza et al 2016; Liti et al 2006; Mugo-Bundi et al 2015; Nhi et al 2018). However, in general there is limited information on the use of alternative protein sources to fishmeal for tilapia diets in Tanzania.

Therefore, the aim of the present study was to investigate the impact on growth performance, nutrient utilization, carcass traits and feed costs of replacing fishmeal on a dry matter basis with locally available feed ingredients in farmed Nile tilapia.

Materials and methods

Study site

The study was conducted in July-August 2019 at the Institute of Marine Sciences Mariculture Centre (IMS-MC) in Pangani, Tanzania (05°25´54.80"S; 038°57´28.87"E). The climate in Pangani is tropical, with mean annual temperature of 27°C and mean annual rainfall of 1214 mm.

Experimental design

A 60-day growth trial with all males Nile tilapia juveniles was performed to study growth performance and carcass traits when the fish were fed diets in which fishmeal was replaced with locally available feed ingredients. The juveniles (n=225) were distributed (15 fish/tank) between 15 plastic tanks (1000 L total volume) filled with 900 L of brackish water. The tanks were divided into five triplicate treatment groups and the fish in each treatment group were fed a reference diet (REFD) with fishmeal or one of four test diets in which locally available ingredients replaced 50% of fishmeal. The feeding trial was conducted in a complete randomised design.

Experimental fish

A total of 300 all males Nile tilapia fingerlings with an average weight of 0.35 g were purchased (Ruvu Fish Farm Ltd, located in the Coastal region of Tanzania) and transported to IMS-MC. For the first month, the fish were fed by hand four times a day with starter commercial fish feed (Aller parvo ex, 0-3 grade; 44% crude protein (CP); Aller Aqua group). After this, the fish were acclimatized for a two-week period prior to the start of the experiment, during which they were fed a locally made fishmeal diet. After acclimatization, 225 fish were selected and placed in the 15 plastic tanks (1000 L), which were filled with brackish groundwater (salinity 2-5 ppt) pumped from a borehole. The water in the fish culture unit was continuously aerated using air stones.

Fish diets and feeding

Test diets were formulated by substituting 50% of fish meal dry matter (DM) in the reference diet (REFD) with brewery spent yeast meal (BSYD), freshwater shrimp meal (FSHD), cattle blood meal (CBD) or Nile perch fish frames meal (FFD) (Table 1).

The other feed ingredients used in the diets were full fat soybean, sunflower seed cake, wheat pollard, maize bran, cassava flour and sunflower oil. A vitamin and mineral premix was included in REFD and CBD, to simulate the composition of diets usually used for tilapia (Gasco et al 2018). It was estimated that the test ingredients used in FFD, FSHD and BSYD covered the mineral needs of tilapia (Mmanda et al 2019). Fish pellets were produced using a pelleting extruder machine (DGP 60, Zhengzhou, China), fixed with a 2 mm matrix. The pellets produced were air-dried in an enclosed warehouse for 24 h before being packed into separate airtight containers and transported to IMS-MC for storage at 4 °C until use.

During the first 30 days of the experiment, the fish were fed three times daily (08:00 h, 12:00 h, 15:00 h), with a daily allowance of 10% of body weight (BW). For the following 30 days up to the end of the experiment, the fish were fed twice daily (08:00 h and 15:00 h) with a daily allowance of 5% of BW. In both experimental periods, the feed allowance corresponded to apparent satiation. The amount of feed offered to the experimental fish daily was recorded for feed intake and other feed utilisation indices assessment.

Growth performance, somatic indices and carcass traits

At the start of the experiment and every two weeks throughout the experimental period, a total of five fish were randomly selected from each experimental tank. Their individual BW was recorded using an electronic balance and their individual total length was measured with a ruler. The number and weight of fish stocked in each tank were assessed every two weeks throughout the 60-days of experimental period for survival rate determination and diets adjustment, respectively.

At the end of the experimental period, three fish were randomly chosen from each tank for assessment of BW, organ weight, hepatosomatic index (HSI) and viscerosomatic index (VSI). Before the assessments, the fish were anaesthetised using clove oil (100 mg L^-1).

For carcass quality determination, BW and length of the anaesthetised fish were recorded. The anaesthetised fish were sacrificed and filleted. The fillet samples were weighed and stored in a freezer (-20 °C) before transport to Sokoine University Laboratory for fillet colour determination using a Konica Minolta Chroma meter (Model CR-400, Osaka, Japan).

Proximate analysis of treatment diets and whole fish body

Five fish were chosen from each tank for whole body fish proximate analysis. Dry matter (DM) content was determined by drying 2 g samples of each fish and each diet to constant weight in an oven (E 115, WTB binder 7200, Tuttlingen, Germany) at 105 °C overnight (12 h) according to AOAC (1990). Crude protein (CP) content was quantified by the standard Kjeldahl nitrogen method (Kirk and Sawyer 1991), using a 2200 Kjeltec auto-distillation unit (Foss, Tecator, Sweden) according to AOAC (1990). Lipid content (ether extract, EE) was quantitatively determined using petroleum ether (ST 243 Soxtec^TM, Hilleroed, Denmark), following the method described by AOAC (1990). Crude fibre (CF) content was determined using an ANKOM 200 fibre analyser (ANKOM, New York, USA) in accordance with methods validated by AOAC (1990). Ash content was determined as the residue remaining after incineration of 1 g of sample in a weighed porcelain crucible in a muffle furnace at 550 °C for 3 h according to AOAC (1990). The AOAC (1990) methods used were as follows: DM (930.04; 930.15), ash (930.05; 942.05), CP (954.01), EE (920.39) and CF (962.09). Nitrogen-free extract (NFE) content was calculated by subtracting the sum of crude protein, crude lipid, ash and crude fibre from the corresponding dry matter values.

Measurements of water quality parameters

The source of water used was groundwater and the quality of water parameters in the culture tanks was monitored daily throughout the experimental period. The parameters pH, dissolved oxygen (DO) and temperature were measured on-site twice a day (09:00 h and 15:00 h) using a HQD portable meter (HQ40D & pH101, Loveland, Colorado, USA). Salinity was also measured on-site twice a day using a hand-held refractometer (RHS-10 ATC, Shenzhen, China). Ammonia, nitrate and nitrite concentrations in water samples from each culture tank were analysed twice per month using a photometer (Palintest 7100 photometer, Nottinghamshire, England). The reagents used during analysis were Palintest nitrite (Nitriphot No. 1 & 2 tablets) for nitrite, Palintest ammonia (Ammonia No. 1 & 2 tablets) for ammonia and Palintest nitrate (Nitratest powder, Nitricol tablets) for nitrate. Ammonia, nitrate and nitrite concentrations in the water samples were determined by dilution techniques according to the manufacturer’s instructions at a ratio of 1:10 for ammonia, 1:20 for nitrate and 1:10 for nitrite. The calibration reading value was 0 to 1.0 mg L^-1 for ammonia, 0 to 20 mg L^-1 for nitrate and 0 to 1500 mg L^-1 for nitrite. The concentration of un-ionised ammonia was calculated as percentage of total ammonium nitrogen (TAN) according to Durborow et al (1997).

Growth and nutrients utilization parameter calculations

Weight gain (WG), percentage WG (%WG), specific growth rate (SGR) and condition factor (K) were calculated according to Sveier et al (2000) as follows:

WG = W_f-W_i, where W_f is final body weight and W_i is initial body weight

%WG = [(W_f-W_i)/Wf] × 100

SGR = [(ln (W_f) - ln (W_i)/ T] × 100, where T is experimental period (days)

K = (TBW/TL³) × 100, where TBW is total body weight (g) and T  length (cm).

Feed conversion rate (FCR), protein efficiency ratio (PEP), survival rate (SR), protein productive value (PPV) and specific growth rate (SGR) were calculated according to Qi et al (2012) as follows:

FCR = FI/WG, where FI is feed intake (g/day) and WG is weight gain (g/day)

PER = WG/PI, where WG is weight gain (g) and PI is protein intake (g)

SR = (N_f/N_i) × 100, where N_f is final number of fish and N_i is initial number of fish

PPV = PG/ PI, where PG is protein gain (g) and PI is protein intake (g)

The somatic indices (VSI and HSI) were calculated according to Kubiriza et al (2016) as follows:

VSI = 100 × (FVM/FBM), where FVM is fish visceral mass (g) and FBM is fish body mass (g)

HSI = 100 × (LM/BM), where LM is liver mass (g) and BM is body mass.

Data analysis

The experimental data were subjected to one-way analysis of variance (ANOVA), using the SAS programme, version 9.4, and considering tank as fixed effect and diet as random effect. The values obtained (mean and standard error) were compared by multiple comparison using the Tukey’s test and differences were considered significant at P<0.05.

Results

Nutrient content of diets

The CP content was 308 g kg^-1 DM in REFD, while the CP content of the test diets ranged from 280 to 391 g kg^-1 DM (Table 2). The content of the other nutrient components ranged from 88.2 to 128 g kg ^-1 DM for EE, from 70.5 to 161 g kg^-1 for CF, from 203 to 403 g kg^-1 DM for NFE and from 137 to 170 g kg ^-1 DM for ash. The content of lysine ranged from 14.2 to 19.2 g kg^-1 DM, the content of tryptophan from 2.9 to 4.0 g kg ^-1 DM and the content of methionine + cysteine from 10.5 to 13.8 g kg^-1 DM (Table 2).

Growth performance, feed utilisation, somatic indices and fish body composition

The reference diet gave the highest total weight gain (WG), average daily weight gain (ADWG) and specific growth rate (SGR) (Figure. 1, Table 3).

Figure 1. Growth performance over a 60-day feeding period of Nile tilapia ( Oreochromis niloticus) fed different diets (REFD: Reference diet (fishmeal); CBD: cattle blood diet; FFD: fish frames diet; FSHD: freshwater shrimp diet; BSYD: brewery spent yeast diet)

The CBD, FFD and BSYD diets produced lower WG than REFD, all four test diets produced lower ADWG than REFD, and FSHD and BSYD produced higher SGR than REFD (Table 3). There were no differences in condition factor (K) and survival rate (SR) between treatments.

Feed intake (FI) was higher for REFD than for the other diets (Table 3). Feed conversion ratio was lower for REFD than for CBD, while PER was higher for REFD than for the other diets. There was no difference in PPV, VSI or HSI between treatments (Table 3).

There were differences between diets REFD and FSHD in initial content of DM, CP, CF and EE in whole fish body and in final content of DM in whole fish body (Table 4). There were also differences in the final content of CP for all four test diets, in the final content of CF in all dietary treatments and in the final content of EE for diets FSHD and BSYD (Table 4). There were no differences between the initial NFE values in whole fish body and the final values in whole fish body in any of the dietary treatments.

Fish fillet colour analysis

The colour analysis (Minolta Chroma meter, Osaka, Japan) of fish fillets showed no differences (P>0.05) between dietary treatments in terms of lightness (L*; 39.7 ± 0.65), redness (A*; 1.96 ± 0.16), yellowness (B*; 5.24 ± 0.17), entire colour index (ECI; 2.91 ± 0.52), hue (3.11 ± 0.23), chroma (5.65 ± 0.08) and hue angle (69.6 ± 1.49).

Water quality parameters

Average tank water temperature was slightly higher (P<0.002) in treatment REFD (23.98 °C) than in the other treatments (23.9 ± 0.04 °C). There were no differences (P>0.05) between treatments in other water quality parameters. The values obtained for these (mean ± SD) were 6.25 ± 0.58 mg L^-1 for DO, 8.74 ± 0.06 for pH, 3.72 ± 0.09 ppt for salinity, 1.47 ± 0.39 mg L^-1 for ammonia, 5.00 ± 1.56 mg L ^-1 for nitrite and 57.32 ± 7.46 mg L^-1 for nitrate.

Discussion

The feed costs and the cost of producing fish biomass could be markedly reduced by replacing fish meal on a dry matter basis with locally available high-quality feed ingredients. Thus, the cost of producing test diets relative to the reference diet was reduced by 33.8 when brewery spent yeast was used and the cost of producing 1 kg biomass of fish was reduced by 27.1% with brewery spent yeast. Similarly, Soltan et al (2008) found that replacement of up to 45% fish meal with a plant protein mixture in Nile tilapia diets reduced feed costs per kg diet by 11.4% and feed costs per kg weight gain by 6.7%. However, 100% replacement by the protein plant mixture was required to reduce the feed costs to 26%. In the present study, this level was achieved with 50% replacement of fish meal with brewery spent yeast. The results in the present study indicate cost savings in replacing fish meal in diets for tilapia with locally available feed ingredients, which can improve the production economics for small-scale fish farmers in Tanzania. Fish feed generally accounts for over 50% of production costs in both semi-intensive and intensive aquaculture production systems (Watanabe 2002). In commercial fish feed, fish meal accounts for 20-60% of the feed costs (De Silva and Anderson 1995). However, prior to the present study there was limited information on the economic values of fish meal alternatives in feed for cultured Tilapia across East Africa region, particularly in Tanzania (Ogello et al 2014).

The common practise in fish nutrition studies when studying the potential of protein-rich feed ingredients to replace other protein feed ingredients is to make the replacement on a protein basis. In contrast, we choose to study the replacement effect on a dry matter basis as this would fit better in a practical setting for a small-scale fish farmer in Tanzania with limited possibilities to get the feed ingredients analysed with respect to the protein content. On the other hand, using dry matter as the basis for the replacement would make it possible to formulate diets by dry weight contribution as the dry matter content in the feed ingredient would differ marginally between ingredients. However, as a result the dietary protein content, as well as the content of other nutrient components, may differ due to ingredient-specific differences in the nutrient composition.

Fish growth performance was better in the reference diet (REFD) than in the diets in which 50% of fish meal DM was replaced. This was mainly related to the positive correlation coefficient (r=0.86) between feed intake (which was highest for REFD) and growth performance of the juveniles. In addition, the protein efficiency ratio (PER) was higher on reference diet than in the diets with the local feed ingredients. However, there were no differences in survival rate and condition value (K) between the dietary treatments in this study which indicate that all treatment diets had similar proportional impacts on fish length in relation to weight. The high survival rate showed that the culture conditions during the study were suitable for tilapia juveniles (Abdel-Tawwab et al 2010; Ahmad et al 2004; Ayisi et al 2017; Ighwela et al 2011). The implication of the lower feed intake on the diets with cattle blood, fish frames, freshwater shrimps and brewery spent yeast, compared with that on the fish meal reference diet, will be the need for longer time in culture to reach the targeted final body weight. This may have an impact on the overall production costs, but will depend on how labour and facilities are valued. However, as the feed conversion ratio was comparable between diets (except for cattle blood) the same total amount of feed would be used to reach the targeted final body weight. Thus, the feeding costs will be determined by the cost of formulating the diets.

The feed utilisation indices values found in the present study were within the range reported in Nile tilapia in previous studies (Abdel-Tawwab et al 2010; Al-Souti et al 2012; Damusaru et al 2019; Fry et al 2018; Soltan et al 2017). The values of the two somatic indices (VSI and HIS) obtained in this study were also in line with those reported in previous studies (Abdel-Tawwab et al 2010; Ayisi et al 2017; dos Santos et al 2019; Obirikorang et al 2016).

The CP content of the diets ranged between 280 and 391 g kg^-1 DM, which in all cases should meet the dietary CP requirements of Nile tilapia juveniles (El-Sayed and Teshima 1992; Liti et al 2006). However, there are indications of a positive impact on growth performance of a high level of dietary CP (Abdel-tawwab 2004; El-Sayed 2006). This may have had a positive impact on the performance of juveniles fed test diets FFD, FSHD and BSYD. The lack of difference in protein efficiency ratio between the test diets suggests that the essential amino acid (EAA) supply was comparable between the diets. Balanced and high availability of EAA can be expected to enhance growth performance, while EAA imbalance and poor EAA availability will reduce growth performance (Ogello et al 2017).

Kirimi et al (2017) reported poor growth performance in Nile tilapia fed diets where cattle blood was used as a protein replacement. In the present study, however, with the exception of poor FCR compared with the fish meal diet, the performance data for CBD did not differ from those obtained for the other test diets. Earlier studies have often found superior performance of tilapia on diets with fish meal compared with diets containing alternative feed ingredients (Abdel-Tawwab et al 2010; Al-Souti et al 2012; El-Sayed 1998; Goda et al 2007; Liti et al 2006; Mathia and Fotedar 2012; Mugo-Bundi et al 2015; Nhi et al 2018). In addition to differences in nutritional properties between feed ingredients, variation in growth performance indices may be due to environmental conditions, culture systems, size and age of fish and duration of culture period, as well as other unknown factors (Abdel-Tawwab et al 2010; Ahmad et al 2004; dos Santos et al 2019; Liti et al 2006; Nhi et al 2018).

The differences between initial and final whole-body chemical composition in tilapia observed in the present study have also been reported by others (Al-Souti et al 2012; El-Sayed 1998; Goda et al 2007; Mugo-Bundi et al 2015). Variation in the whole-body chemical composition of fish can be explained by differences in deposition rate in muscle and/or different growth rates, different levels of nutrient (CP, ash, CF) content in the dietary treatments, differences in fish size and physiological ability of the cultured fish to convert diets into absorbable nutrients (Abdel-Tawwab et al 2006; Mugo-Bundi et al 2015). The initial whole-body CP levels were lower than the CP levels found at the end of the feeding trial in this study which is in agreement with Al-Souti et al (2012). Moreover, the initial whole-body EE levels were higher than the EE levels found at the end of the trial. In contrast, initial and final whole-body ash and NFE content remained unchanged, confirming previous observations (Goda et al 2007; Mugo-Bundi et al 2015). The marked reduction in whole-body content of CF is a reflection of a decrease in the relative proportion of chitin and bones as the muscle mass increases with age (Sánchez-Muros et al 2016). The differences in whole-body chemical composition were not reflected in any of the fillet quality traits.

Water quality plays a significant role in the biology and physiology of fish (Cho and Kaushik 1990). However, the quality of water varies from one region to another due to type and source of water used, farming system (tanks, cages or ponds), climate conditions, geology, geomorphology, land use and level of precipitation (Elisante and Muzuka 2017; Makori et al 2017; Nkotagu 1996). The water quality values in the present study were within the range of values reported in the literature for groundwater in Tanzania (Elisante and Muzuka 2017; Makoba and Muzuka 2019) and can be considered suitable for cultured tilapia (Balogun et al 2005; Makori et al 2017; Monsees et al 2017; Wang et al 2006). The water quality parameters recorded were stable throughout the experimental period (60 days) and did not differ between treatments.

Conclusions

• Replacement of fish meal in the diet for juvenile Nile tilapia with cattle blood, fish frames, freshwater shrimp and brewery spent yeast, reduced feed costs per kg feed and per kg body weight gain
  
  
• While feed intake, growth performance and protein efficiency ratio was superior in fish fed the fish meal reference diet, there were no differences among the studied locally available feed ingredients
  
  
• These results indicate that the economics of small-scale tilapia production in Africa including Tanzania can be improved by using good-quality, low-cost, locally available feed ingredients to replace fish meal

Acknowledgement

We are grateful to Mr. Muhidin A. Khamis (manager), and his staff at Pangani Mariculture Centre for their immense support during growth performance data collection; to Animal, Aquaculture and Range Sciences laboratory technicians at Sokoine University of Agriculture. In addition, many thanks to Professor Faustine P. Lekule (managing director) at Tanfeed International and his staff for support in production of treatment diets (pellets) used in this study. The Swedish International Development Cooperation Agency (Sida) is gratefully acknowledged for financial support provided through the Bilateral Marine Science Programme between Sweden and Tanzania and through a four-year research project grant (SWE-2010-194)

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