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Article

Gradual Replacement of Soybean Meal with Brewer’s Yeast in Fingerling Nile Tilapia (Oreochromis niloticus) Diet, Resulting in a Polynomial Growth Pattern, Independent of Whether Reared in a Biofloc or Clear-Water System

by
Nguyen Huu Yen Nhi
1,2,*,
Trinh Thi Lan
1,
Kartik Baruah
2,
Torbjörn Lundh
2 and
Anders Kiessling
2,*
1
Department of Aquaculture, Faculty of Agriculture and Natural Resources, An Giang University, Vietnam National University, Ho Chi Minh City, 90116 Long Xuyen, An Giang, Vietnam
2
Department of Applied Animal Science and Welfare, Faculty of Veterinary Medicine and Animal Sciences, Swedish University of Agricultural Sciences, 75007 Uppsala, Sweden
*
Authors to whom correspondence should be addressed.
Aquac. J. 2024, 4(4), 255-269; https://doi.org/10.3390/aquacj4040019
Submission received: 30 June 2024 / Revised: 21 September 2024 / Accepted: 2 October 2024 / Published: 15 October 2024
Browse Figure
Versions Notes

Abstract

:
A 60-day feeding experiment was conducted to examine whether (i) soybean meal (SBM) protein in the diet of Nile tilapia (Oreochromis niloticus) can be replaced with protein from spent brewer’s yeast (SBY); (ii) co-rearing with biofloc alters fish growth, feed conversion and protein efficiency compared with rearing in clear water; and (iii) accumulated protein quantity and quality in biofloc acts as a possible feed source for the fish in periods of low feed intake. The fish were reared in either a bio-recirculating aquaculture system (Bio-RAS) or a clear-water RAS (Cw-RAS). In Bio-RAS, the mechanical and biological filters used in Cw-RAS were replaced with an open bioreactor that delivered heterotrophic-based biofloc to the rearing tanks and also acted as a sedimentation trap for effluent water before recirculating it back into the rearing unit. The fish were fed four iso-nitrogenous and iso-energetic diets (~28% crude protein, ~19 MJ kg−1 gross energy) in which SBM protein was replaced with increasing levels of SBY, with triplicate tanks per inclusion level. The results revealed that average fish growth was greater in a biofloc environment compared with clear water and also greater at higher inclusion levels of SBY. However, in both rearing environments, fish growth displayed a second-degree polynomial distribution with increasing SBY inclusion level, with a peak between 30% and 60% inclusion. Fish in the biofloc environment showed better feed conversion ratio and protein retention, likely through ingesting both given feed and biofloc. Biofloc contained a significant amount of accumulated protein with a high biological profile, thereby constituting a possible feed reserve for the fish. A conclusion underlined by the apparent improved feed conversion of Bio-RAS reared fish, where that ingestion of biofloc will reduce the need for external feed per unit growth.

1. Introduction

Soybean meal (SBM), known for its high protein content, high digestibility and relatively well-balanced amino acid profile, is a commonly used plant protein source in the diet of farmed animals [1,2,3], including fish species [4]. However, the extensive use of SBM is associated with environmental impacts arising from farming practices [5,6]. Moreover, there are arguments in favour of using SBM for direct human consumption rather than as animal feed [7]. Previous studies have examined the use of alternative cost-effective ingredients to replace SBM as the main feed protein source in animal feeds. For instance, in juvenile channel catfish, it has been shown that cottonseed meal can replace 100% solvent-extracted SBM when supplemented with iron from ferrous sulphate heptahydrate [8]. In juvenile hybrid tilapia, Yue and Zhou [9] found that cottonseed meal with lysine can replace approximately 60% of SBM in the diet.
Spent brewer’s yeast (SBY), a single-cell protein, is generally available locally and is relatively more cost-effective than SBM [4]. SBY is an abundant by-product from the brewing industry and has a high nutritional value [10]. The use of SBY also has environmental implications, in that its use as animal feed increases the circularity of nutrients back into the feed systems and reduces the risk of becoming effluent, imposing constraints on the surrounding ecosystem. SBY also has other advantages in addition to its content of macronutrients. SBY also contains immunostimulatory compounds, such as β-glucans, nucleic acids and mannan oligosaccharides [11]. Numerous studies have shown that even at low inclusion levels, SBY can enhance the immune response in various species, including Pacific white shrimp [12], juvenile Jian carp [13], red drum [14], seabream [15] and rainbow trout [16]. Furthermore, a small quantity of yeast has been shown to be a promising feed additive for regulating gut bacterial communities in largemouth bass and red drum [14,17]. SBY also improves disease resistance and stress tolerance in many farmed fish [14,18]. For instance, Abdel-Tawwab et al. [19] found that feeding Nile tilapia with baker’s yeast (Saccharomyces cerevisiae) for 12 weeks caused a significant reduction in mortality when the fish were challenged with the pathogenic bacteria Aeromonas hydrophila. In another study conducted on Galilee tilapia (Sarotherodon galilaeus), supplementing a commercial diet with live baker´s yeast for six weeks markedly enhanced the growth performance of the fish and resistance to environmental copper toxicity [20]. Additionally, SBY has been found to improve the physiological responses and gut microbiota of juvenile beluga [21] and to enhance resistance to ammonia–nitrogen stress in Pacific white shrimp [12]. SBY is also reported to have positive effects on the growth performance of several aquaculture species, such as Pacific white shrimp [12], hybrid striped bass [22,23], juvenile pikeperch [24], juvenile beluga sturgeon [21] and Nile tilapia [18,25,26].
Biofloc in water is a natural construct in which algae, bacteria, protozoans, zooplankton and nematodes form small flocs that act as natural feed pellets for fish or shrimp [27]. By adding a carbon source such as glycerol, starch, molasses, sugar or wheat to the water, the carbon–nitrogen ratio (C:N) can be adjusted to favour a higher content of heterotrophic bacteria and thereby more the effective removal of toxic nitrogenous compounds. These nitrogenous compounds are then transformed into new protein, simultaneously promoting a more stable water environment [27,28,29,30,31,32,33]. In addition, a stable biofloc environment has been shown to reduce the risk of disease outbreaks compared with fish farming systems that rely on clean incoming water, owing to a zero-water exchange approach and an enhanced immune response [34,35,36,37,38]. The use of biofloc technology has been associated with improved growth performance of tilapia [26,29,37,38,39,40,41,42] and other farmed fish species [36,43,44,45,46].
While an accumulating body of evidence demonstrates the health and nutritional benefits of biofloc for both fish and shrimp, there are also some drawbacks associated with biofloc systems. One significant disadvantage is that biofloc may compete for limited resources, particularly oxygen, with fish and shrimp in the same aquatic environment. In addition, larger floc particles and dead microbes tend to settle and accumulate at the bottom of the pond or tank, creating suitable environments for anaerobic bacteria growth, posing a risk of toxic compounds being produced. To address these challenges, in this study we used a new tank design, in which the filter system of a recirculating aquaculture system (RAS) is replaced with a bioreactor unit designed to manage the excess organic material. This bioreactor unit processes the organic material and then reintroduces a more suitable concentration of flocs back to the farming unit, to the benefit of fish and shrimp. This system, denoted Bio-RAS [47], was first tested by Nhi and colleagues [26,42,48] and further evaluated by Ekasari et al. [49]. By using the Bio-RAS, we aimed to distinguish the effects of co-farming fish with a live microbial community, without the confounding effects relating to the aggregation of organic material in the conventional fish farming unit. The combination of clear-water RAS and Bio-RAS equipment allowed us to investigate the direct effects on fish of replacing SBM with SBY in their diet and the additional effect of SBM replacement in the presence of a metabolically active microbial community in the water surrounding the fish. According to Nguyen, Trinh, Baruah, Lundh and Kiessling [42], tilapia reared in biofloc are capable of maintaining growth at a higher rate than similar tilapia kept in clear water, even when the protein content of the diet is reduced. This indicates that the flocs generated are an integral component of the diet for biofloc-reared tilapia, i.e., biofloc may improve the biological value of dietary protein. It may also produce new nutrients, and could possibly function as an additional feed source for reared fish or shrimp [42]. An additional aim of the present study was therefore to measure the changes in the content of nutrients, such as protein and lipid, of the biofloc.

2. Materials and Methods

2.1. Experimental Conditions

A 60-day experiment was carried out on an experimental farm located at An Giang University, Long Xuyen city, An Giang province, Vietnam. The Nile tilapia (O. niloticus) used, of the GIFT strain [50], were transported from a hatchery in Cu Chi, Ho Chi Minh city, Vietnam, in sealed 0.5 m3 plastic bags filled with oxygen-saturated water and containing 1 kg fish per bag. Upon arrival at the research station, all fish were dipped in a solution of 3% NaCl for 5 min to eliminate the risk of parasite infection. The fish were then kept in two separate tanks (3 m3) for a period of two weeks to allow them to acclimatise to indoor environmental conditions. At a mean body weight of 50.3 ± 0.7 g, the fish were randomly distributed among 24 composite settling tanks, each with capacity of 500 L. The stocking density used was 20 fish per tank.
The experimental set-up, in which fish were reared in either clear-water RAS (Cw-RAS) or a Bio-RAS, was as described in our earlier study [42]. The Cw-RAS comprised 12 parallel-connected 500 L tanks connected to a sedimentation tank containing sand and stones (1–2 mm diameter), which functioned as a mechanical and biological filter. The water source was municipal tapwater, which was de-chlorinated and aerated for 24 h before use. Water was circulated at a rate of 3 L min−1 into each tank, with about 30% of the water being replaced every two days. The experimental Bio-RAS, set up beside the Cw-RAS, comprised 12 tanks identical to those used in Cw-RAS, but connected in parallel to four serial-connected 10 m3 composite tanks that functioned as bioreactors for microbial growth and the settling of sludge. Two weeks before the start of the experiment, biofloc was initiated as described by Pérez-Fuentes et al. [51]. In brief, Bacillus subtilis, with molasses as the carbon source and blood meal (a product of Huong Hoang Nam Company, Ho Chi Minh City, Vietnam) as the nitrogen source, were added to each of the bioreactor tanks, at a C:N ratio of 10:1. All 24 experimental tanks were aerated via one air stone connected to a low-pressure electrical blower (Resun GF-370, Shenzhen Xing Risheng Industrial Co., Ltd. Shenzhen, China). The four bioreactor tanks were equipped with four air stones and an internal circulation water pump (DAB FEKA VS 750M-A, Mestrino, Italy). This was to ensure that well-blended live biofloc was pumped to the experimental tanks and that heavy fibrous sludge was kept at the bottom of each bioreactor tank. Sedimented sludge was removed from the bioreactor tanks every two weeks by siphoning from the bottom of the tank.
The experiment followed a completely randomised design with four dietary treatment groups and the two parallel recirculation systems (biofloc (B) and clear-water (C)), which were organised as separate entities. The diets, which contained varying proportions (0, 30, 60, 100%) of the SBY protein replacing SBM, were labelled according to each diet and water environment as follows: B0% and C0% (control); B30% and C30%; B60% and C60%; B100% and C100%. Three replicates were maintained for each experimental group. This study was conducted at An Giang University as part of a PhD degree at the Swedish University of Agricultural Sciences, Uppsala, Sweden, in accordance with the ethical permit for feed trials in fish (Dnr. 5.8.18-16347/2017), as overseen by the Swedish Board of Agriculture.

2.2. Experimental Diets

Four iso-nitrogenous (28% protein) and iso-energetic (19 MJ kg−1) diets, in which SBM protein was replaced with SBY at a level of 30%, 60% and 100% on a protein basis, were produced. The level of fishmeal was kept constant, and methionine was added to the diets to cover the fish requirement for methionine (Evonik, Essen, Germany, 99% purity). The diet composition is shown in Table 1, and the chemical composition and amino acid levels in the diets are indicated in Table 2. The SBY was a by-product obtained from Hung Thinh company in Hoc Mon district, Ho Chi Minh City, Vietnam. The other ingredients were obtained from local markets in Long Xuyen City, Vietnam. All ingredients were thoroughly mixed and then cold-pelleted feed was made with an electric meat grinder (Quoc Hung Company, Can Tho City, Vietnam), producing feed pellets with diameter and length in the range 2–3 mm. All diets were sun-dried for two days, and then weighed and stored in sealed plastic bags in small portions at 5 °C until use. The fish were fed manually twice a day (between 07:00 and 09:00 h and between 16:00 and 18:00 h) until satiation. The amount of feed used per day and tank was recorded throughout the experiment.

2.3. Measurements and Calculations

All fish were measured monthly for weight and length. All fish were starved on the day before measurement, but fish in the Bio-RAS could still ingest biofloc. All fish from each tank were anaesthetised by ethylene glycol monophenyl ether at 0.5 mg L−1 to reduce activity sufficiently to perform measurements, based on Nhi [52].
Feed conversion ratio (FCR), total feed intake per fish (FI), total protein intake (PI), protein conversion ratio (PCR), specific growth rate (SGR) and survival rate (SR) were calculated as [53,54]:
FCR = Total feed intake per replicate/total wet weight gain per replicate
PI (g) = Feed intake (g) × protein in the diet (%)
PCR = [Total body protein gain/total protein intake] × 100
SGR (%/day) = [(ln final Wt − in initial Wt)/days] × 100
SR (%) = (Total number of fish harvested/total number of fish cultured) × 100

2.4. Water Quality and Biofloc Monitoring

Water temperature (°C) in all fish tanks was recorded daily at 07:00–08:00 h and 13:00–14:00 h. Dissolved oxygen (DO, mg L−1) and pH were measured every third day, using a Hach HQ30d Multi-Parameter Meter (Hach, USA). Nitrite–nitrogen (NO2-N, mg L−1) and total ammonia–nitrogen (TAN, mg L−1) were measured twice a month according to standard methods [55]. Water quality parameters were measured at the water intake and outlet of the experimental bioreactor and filter tanks.
The biomass of organic components in biofloc was measured using a water filter bag (1 µm) at the water outlet from the bioreactor tank to the rearing tanks. Biofloc samples were collected at the beginning, middle and end of the experiment. During each sampling event, three samples were taken on three consecutive days and analysed for total nitrogen, fat and amino acids.

2.5. Chemical Analysis

Triplicate feed and biofloc samples were analysed as follows: Dry matter was determined by drying in an oven at 105 °C to constant weight. Ash content was determined by incineration of the sample at 550 °C for 4 h. Crude protein was calculated as 6.25 × % N analysed by the Kjeldahl method, ether extract (EE) was measured using the Soxhlet method, and crude fibre (CF) content was analysed using standard methods [56]. Amino acid content was determined by high-performance liquid chromatography (HPLC) according to [57]. Nitrogen-free extract (NFE) was calculated as NFE = 100 − (% protein + % lipid + % fibre + % ash) [56]. Gross energy content (kcal kg−1) was calculated according to [10], using a value of 5.64, 9.44 and 4.11 kcal g−1 whole body for protein, lipid and carbohydrate, respectively.

2.6. Statistical Analyses

Statistical analyses were conducted using the general linear model procedure (GLM) in Statistical Analysis System (SAS® 9.4) and t-test (using the same software). For the values presented in Table 3 (fish responses), a two-factorial main effect model was used, i.e., a two-way ANOVA with a rearing system (Cw-RAS and Bio-RAS) and SBY inclusion level as independent variables. The model comprised response variable = inclusion level, rearing system, inclusion level × rearing system (interaction), and error. Non-significant factors were then step-wise removed. In the event of a significant difference (p < 0.05), Tukey multiple range tests were used for comparing individual treatment groups (Table 3). In analysing the biofloc (values presented in Table 4), a main factorial model (one-way ANOVA) was used, with time as independent variable (experiment start, middle and end). Because samples were obtained from the joint Bio-RAS bioreactor tank (see the Materials and Methods section for a description of the tank arrangements), these samples represent a pooled biofloc from all 12 experimental Bio-RAS tanks, and thereby did not enable separation between SBY mixture inclusion levels, only changes over time. The polynomial distribution curve presented in Figure 1 was tested for significance by a second degree model (individual body weight at 60 days = SBY inclusion and (SBY inclusion × SBY inclusion), per rearing system. The curve presented in Figure 1 was based on average weight at each SBY inclusion level. The water quality variables given in Table 5 were compared pairwise by sampling occasion using a t-test.

3. Results

The growth performance, feed utilisation and survival rate of tilapia reared in the Bio-RAS and Cw-RASs and fed diets with different inclusion levels of SBY are shown in Table 3 and Figure 1. The initial weight and length of fish assigned to the different treatments did not differ significantly (p = 0.94 and 0.69, respectively) (Table 3). However, by day 30, the growth of fish in the Cw-RAS and Bio-RAS units differed significantly, with higher growth in Bio-RAS fish (p = 0.01) (Table 3). By day 60, the difference between the two rearing systems was even greater (p < 0.0001) (Table 3). No significant interaction was seen between SBY inclusion level and rearing system, either at 30 or 60 days (p > 0.3, results not shown).
The replacement of SBM with SBY had significant effects on growth already at day 30 (p < 0.0001), and even greater effects at day 60 (Table 3). However, growth with increasing SBY inclusion level tended to follow a polynomial rather than linear distribution already at day 30 (p < 0.1, Table 3) and showed a significant polynomial distribution at day 60 (p = 0.003 and p < 0.0001 for Bio-RAS and Cw-RAS fish, respectively) (Figure 1 and Table 3).
There was a trend for a similar pattern between SBY inclusion levels (p < 0.1) and a highly significant effect of the rearing system (p = 0.002) on body length and SGR (Table 3). FCR improved in parallel with growth rate, with Bio-RAS fish displaying lower FCR than Cw-RAS fish (p = 0.0003) (Table 3). The lowest FCR value was seen at 30% SBY inclusion in Bio-RAS fish (Table 3).
Protein conversion was lower on average in Cw-RAS fish than in Bio-RAS fish (p = 0.0004) (Table 3). In Cw-RAS fish, protein conversion only declined with full replacement of SBM, i.e., at 100% SBY inclusion, but not significantly so (p > 0.05) (Table 3). In Bio-RAS fish, a 30% SBY inclusion level showed a significant (p < 0.05) higher level than both 0% and 100% SBY-fed fish. The 60%-inclusion-fed fish displayed a similar conversion level to the 0%-fed fish but did not differ significantly (p > 0.05) from the 30%-inclusion-fed fish. The 100%-SBY-inclusion fed fish displayed the lowest protein retention; however, this was not significantly different from the SBY 0%-fed fish (p > 0.05) (Table 3). When protein retention in biofloc was included in the conversion calculation (only relevant in Bio-RAS), a 40% increase in protein retention was observed, indicating that the biofloc represented significant protein enrichment (Table 3 and Table 4).
The amino acid composition and total dry matter, protein and lipid content of biofloc at the start, middle and end of the experiment are shown in Table 4. Overall, there was a significant (p < 0.05) increase in protein and a significant decrease (p < 0.05) in lipid concentration in biofloc over time (Table 4). There was pronounced and highly significant (p < 0.0001) increase in total biofloc biomass, expressed as dry matter per m3 water, throughout the experiment (Table 4). The concentrations of most essential amino acids in biofloc remained stable through the experiment. The only exceptions were lysine and methionine, the concentrations of which showed a significant (p < 0.0001) decrease to the mid-point of the experiment and then stabilised or even increased slightly, and phenylalanine and histidine, which showed a significant increase (p < 0.05) in concentration throughout the experiment.
Fish mortality was low, with no significant differences between any of the treatments (p > 0.2) (Table 3). Water quality also remained stable throughout the experiment, independent of treatment, with the exception that TAN was present in slightly higher average concentrations in Bio-RAS water (Table 5).

4. Discussion

The general interactive effect of diet and water biota, i.e., clear water versus biofloc environment, on the performance of farmed tilapia, aligned well with earlier findings [26,48]. The improvement in growth and feed utilisation in Bio-RAS compared with CW-RAS fish was therefore independent of dietary protein source. A similar effect has been seen in shrimp when varying the available total protein fraction in the diet [42]. In our previous studies using both Bio-RAS and Cw-RAS, replacing fishmeal with yeast resulted in a gradual decrease in growth and protein retention in tilapia, but Bio-RAS fish consistently exhibited better growth rates and lower feed conversion than Cw-RAS fish [26]. In fact, fish raised in the Bio-RAS and given only yeast protein displayed similar final weight to fish fed 100% fishmeal protein but reared in clear water, while freshwater prawns kept in clear water showed a gradual decrease in growth, with yeast meal replacing fishmeal [48]. In contrast, prawns raised in a Bio-RAS environment displayed a tendency for increased growth with increased dietary yeast level [48], which is the opposite to the pattern we observed in tilapia. It can therefore be concluded that co-farming fish with biofloc can compensate for the decreased biological value of alternative protein sources such as SBY, at least in species capable of utilising biofloc as a nutrient source. The results obtained in the present study also indicate that a positive synergy can arise when protein sources are properly mixed (Figure 1). This confirms the claim that biofloc can compensate, at least in part, for a reduction in total protein in the diet [42].
Before discussing the possible underlying mechanisms for these observations, some more general nutritional aspects must be considered. All diets tested in this study had a protein content in accordance with that recommended by Jauncey [58] for tilapia, i.e., a crude protein content of 25–30% (Table 2). However, [59] recorded a 5–15% lower digestibility of yeast compared with fishmeal and SBM concentrate, which would result in lower digestible protein level in the diet of fish when SBM is replaced with SBY. It would have been desirable to include a measurement of apparent digestibility as a variable in the study, but the biofloc environment made trap collection impossible without biofloc confounding the samples. In addition, the fish were still too small for repeated faeces collection by stripping at the end of the experiment, and it was too risky to conduct this procedure during the trial itself. Previous studies have shown that the level of protein in the diet of O. niloticus can be reduced from 33.2% to 25.7% if the dietary lipid content is increased from 5.7% to 9.4% and the carbohydrate content from 32% to 37% [60], indicating that the diets in our experiment likely provided sufficient protein even at higher SBY inclusion levels. Nevertheless, a lower digestibility of SBY protein can, at least in part, explain the decrease in fish growth in terms of increasing from 60% to 100% SBY inclusion (Figure 1). In order to construct isocaloric and protein-balanced diets, the level of total fat varied between the diets. However, based on Chou and Shiau [61], Abdel-Ghany et al. [62] and Miritunjoy et al. [63], the differences in lipid content between the diets likely made only minor contributions to the observed differences in growth between the different dietary groups. This is further supported by findings by Furuya et al. [64] that the dietary protein source is the major limiting factor affecting growth performance in tilapia.
We observed a significant improvement in feed conversion and enhanced protein utilisation in Bio-RAS fish, suggesting that biofloc contributed much more than just lipids or energy to the nutrition of fish reared in this system. The microbial communities within biofloc can synthesise essential nutrients (e.g., vitamins, amino acids, bioactive components) and enzymes which may be lacking in the fish diet. This microbial synthesis likely provides additional nutritional benefits to the fish, potentially supporting better nutrient utilisation, as observed in this study. This warrants further investigation in additional studies.
The effect of biofloc may comprise two components, one related to pure nutrition and the other to bioactive aspects. From a nutritional perspective, the biofloc in this study contained high levels of amino acids, 39.6–44.6% protein and 0.61–2.79% lipid on a dry matter basis. This composition aligns well with a fully nutritional diet except for that the crude lipid level is low. The nutrient content of the biofloc was similar to that of biofloc analysed by Long, Yang, Li, Guan and Wu [37], which contained 41.13% crude protein and 1.03% crude fat. On the other hand, biofloc collected by Azim and Little [29] from a zero-exchange indoor system rearing tilapia fed different protein levels from 24% or 35% crude protein was found to contain 37.9–38.4% crude protein, 3.16–3.23% crude lipid, 11.8–13.4% ash and 18.6–19 kJ g−1 energy, which is nearly twice the level of lipids found in our final biofloc samples. Floc density (g dry matter m−3) increased from 8.2 g m−3 at the start of our experiment to 71.4 g m−3 at the end. The density was higher than that reported by Avnimelech [28] and was likely an underlying cause of the significant difference in fish growth between the two systems. In terms of protein retention, including biofloc yielded a 40–45% increase compared with retention in fish alone (Table 3). Our results align well with those from previous studies on tilapia reared in intensive biofloc environments [26,29,37,38,39,40,41] and on other fish species [36,43,44,45,46].
The good ability of SBY to replace fishmeal as a protein source is well-documented [37,65,66]. Øverland et al. [67] achieved the successful replacement of fishmeal in the diet of Atlantic salmon using the yeasts Candida utilis and Kluyveromyces marxianus. Similarly, our previous study indicated that the 50–60% replacement of fish meal with SBY is possible in a clear-water rearing system [26], whereas total replacement is only achievable in the Bio-RAS.
Based on the data obtained in the present study, there was a tendency (p > 0.05) for improved growth in Cw-RAS fish, and a significant increase (p < 0.05) in the growth of Bio-RAS fish when using a mixture of SBM and SBY protein (Table 3). This aligns with earlier observations by Barros, Lim and Klesius [8], who replaced SBM with 0%, 50% or 100% cottonseed meal (CSM) in the diet of juvenile channel catfish and found that a diet with both protein ingredients (50% SBM replaced with 27.5% CSM) showed a better performance than a diet with no SBM. Furthermore, Hassaan et al. [68] found that diets containing four levels of yeast extract rich in nucleotides and β-glucan (0, 5, 10, and 15 g kg−1 diet) improved growth and had beneficial effects on haematological and biochemical blood parameters, lipid profile, and the histological structure of liver and gut in tilapia. Another trial by Oliva-Teles and Gonçalves [65], testing the effect of partial replacement of fishmeal with SBY (0, 10, 20, 30, or 50%) in the diet of juvenile sea bass, demonstrated that diets with multiple protein sources were superior in terms of feed efficiency. These findings indicate that diets supplemented with SBY have higher protein retention and protein efficiency ratio, and lower FCR, than diets without SBY [65]. Abass, Obirikorang, Campion, Edziyie and Skov [18] made similar findings when adding the yeast Saccharomyces cerevisiae (0, 3, 5, and 7%) to the diet of tilapia, i.e., diets with multiple protein sources (with yeast) displayed better growth, stress tolerance and disease resistance than diets without yeast (0%). As pointed out above, we found a similar effect in Cw-RAS fish (trend) and Bio-RAS fish (p < 0.05) fed a diet containing 70% SBM and 30% SBY. This effect is well demonstrated in Figure 1, where final body weight at 60 days clearly and significantly (p < 0.003) followed a second-order polynomial distribution. From the data, it is clear that the optimum inclusion rate of SBY to replace SBM is somewhere between 30% and 60%. However, the number of inclusion levels tested was too small to yield any more information than the graphical indication in Figure 1. Based on the pattern shown in Figure 1, one could also speculate that the regression might be more complex when biofloc is present compared with the clear-water situation. Further research is needed to confirm this. A very interesting area for future research is to optimise the dietary inclusion levels of the two protein sources, not least from a least cost perspective.
The underlying reason for the polynomial weight distribution might very well relate to gut-positive probiotic factors like nucleotides and β-glucans, as studied by Hassaan, Mahmoud, Jarmolowicz, El-Haroun, Mohammady and Davies [68]. Thus, biofloc-exposed fish might have had the benefit of additional bioactive substances and also a complementary amino acid profile to that of SBY alone. This could also explain why the partial replacement of fishmeal with SBY had less prominent effects in our earlier studies on fish kept in a biofloc environment [26,42,48] using fishmeal as replacement protein. Considering that fishmeal has a more complete amino acid profile than SBM and lacks the antinutritional factors of soybean, the replacement of fishmeal with SBY would be more of a quantitative, rather than qualitative, addition to the fish diet, and thereby give a linear distribution of fish weight with protein source replacement. On the other hand, the reduction in growth with high levels of SBY protein in both the Cw-RAS and Bio-RASs could be attributable to the metabolic overload of antioxidant systems [69,70], when metabolising high levels of purines both from biofloc and from the yeast. However, it is unlikely this is the sole explanatory factor for the fish weight distribution, as the curves were more or less parallel for the two water environments, indicating that the nutritional effect remained similar whether the fish had access to biofloc or not.
Another interesting area for future research is the effect of biofloc on the digestibility of different nutrients, either by affecting the composition of the gut biota, as shown by, for example, Huyben [69], or direct effects on the digestive system of the fish. However, digestibility studies were not possible in the present system, as mentioned above, due to the risk of contamination by the floc or disturbing the fish too much by using stripping.
Overall, the SBY diets in this study were accepted by the tilapia, as indicated by the limited differences in growth between dietary groups, independent of the rearing system. However, in the clear-water environment, there was a significant reduction in the growth of fish given 100% SBY compared with all fish given diets with SBM inclusion. No apparent difference in growth was observed between 100% SBM and 100% SBY when the fish were reared in a biofloc environment. Moreover, a combination of SBY and SBM in the diet improved feed efficiency and growth performance compared with either 100% SBM or 100% SBY, particularly if biofloc was present in the water. This finding may have direct implications for the design of future aquafeeds, where microbial protein feed sources are likely to increase.
Biofloc analysis revealed a significant accumulation of protein in the flocs, both in terms of concentration and especially of volume. However, the lipid concentration in the biofloc decreased, even though total volume of lipid increased during the 60-day trial. This is another finding with direct implications for the aquaculture industry. This increase in biomass could significantly reduce the environmental impact of fish and shrimp farming if it is used as fertiliser or as a nutrient source for fish/shrimp, instead of being released to a water recipient. Its re-use could also improve production economics and the health of the fish/shrimp.

Author Contributions

Conceptualization: A.K., T.L. and N.H.Y.N.; Methodology. N.H.Y.N., T.T.L., A.K. and T.L.; Validation: A.K., T.L. and K.B.; Formal analysis and investigation: N.H.Y.N., T.L., T.T.L. and A.K., Resources, A.K. and T.L.; Data curation, N.H.Y.N., T.T.L. and A.K.; Writing—original draft preparation, N.H.Y.N.; Writing—review and editing, N.H.Y.N., A.K., T.L., T.T.L. and K.B.; Visualization, A.K.; Supervision, A.K. and T.L.; Project administration, T.L. and A.K.; Funding acquisition, T.L. and A.K. All authors have read and agreed to the published version of the manuscript.

Funding

The study including the PhD scholarship for Nguyen Huu Yen Nhi was funded by the Sida/SAREC MEKARN II (‘Mekong Basin Animal Research Network’).

Institutional Review Board Statement

The study was part of a PhD degree at the Swedish University of Agricultural Sciences, Uppsala, Sweden, in accordance with the ethical permit for feed trials in fish (Dnr. 5.8.18-16347/2017), as overseen by the Swedish Board of Agriculture.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data is available at request from the THV-adm@slu.se/Nhi et al PhD manuscript 4.

Acknowledgments

The authors also wish to thank the laboratory staff at the National Institute of Animal Husbandry, Ministry of Agriculture and Rural Development, Vietnam, and the staff and some students at the Aquaculture Department, Faculty of Agriculture and Natural Resources, An Giang University, Vietnam, for their support and assistance during this study.

Conflicts of Interest

The authors declare no conflict of interest.

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Aquacj 04 00019 g001
Figure 1. Change in body weight (BW, g), given as LS-mean± SEM (Standard error of the mean), of Nile tilapia fingerlings (Oreochromis niloticus) fed different levels of spent brewer’s yeast (0% 30%, 60% and 100% on protein basis) replacing soybean meal and kept in different rearing systems. Bio-RAS = Biofloc recirculating aquaculture system. The R2 of the second-degree polynomic curve fit and standard error of the mean are based on the average of three replicate tanks, explaining the high fit (R2). Both models shown are significant (p < 0.0001 and p < 0.003 for Bio- and CW-RAS, respectively) when including the complete dataset in the main factorial GLM model (general linear model procedure, SAS® 9.4).
Figure 1. Change in body weight (BW, g), given as LS-mean± SEM (Standard error of the mean), of Nile tilapia fingerlings (Oreochromis niloticus) fed different levels of spent brewer’s yeast (0% 30%, 60% and 100% on protein basis) replacing soybean meal and kept in different rearing systems. Bio-RAS = Biofloc recirculating aquaculture system. The R2 of the second-degree polynomic curve fit and standard error of the mean are based on the average of three replicate tanks, explaining the high fit (R2). Both models shown are significant (p < 0.0001 and p < 0.003 for Bio- and CW-RAS, respectively) when including the complete dataset in the main factorial GLM model (general linear model procedure, SAS® 9.4).
Aquacj 04 00019 g001
Table 1. The ingredient composition (% dry matter) of four experimental diets for Nile tilapia fingerlings (Oreochromis niloticus) with different levels (0%, 30%, 60%, 100% on a protein basis) of spent brewer’s yeast (SBY) replacing soybean meal.
Table 1. The ingredient composition (% dry matter) of four experimental diets for Nile tilapia fingerlings (Oreochromis niloticus) with different levels (0%, 30%, 60%, 100% on a protein basis) of spent brewer’s yeast (SBY) replacing soybean meal.
Diet
IngredientsSBY0 (Control) aSBY30 bSBY60 cSBY100 d
Blood meal1.31.72.12.8
Fish meal1.01.01.01.0
Soybean meal4028160
Spent brewer’s yeast015.230.450.5
Rice bran25.023.822.721.0
Wheat flour23.021.018.616.0
Fish oil5.75.34.84.3
Methionine0.360.360.360.36
Premix (vitamin-mineral) e2.02.02.02.0
CMC f2.02.02.02.0
Total100100100100
a 0% spent brewer’s yeast. b 30% spent brewer’s yeast replacing soybean, based on protein. c 60% spent brewer’s yeast replacing soybean, based on protein. d 100% spent brewer’s yeast replacing soybean, based on protein. e Vitamin and mineral premix content per kg: vitamin A 4,000,000 UI; vitamin D3 800,000 UI; vitamin E 8500 UI; vitamin K3 750 UI; vitamin B1 375 UI; vitamin C 8750 UI; vitamin B2 1600 mg; vitamin B6 750 mg; folic acid 200 mg; vitamin B12 3000 μg; biotin 20,000 μg; methionine 2500 mg; Mn, Zn, Mg, K and Na 10 mg. f Carboxymethyl cellulose, imported from Korea.
Table 2. Proximate chemical composition, amino acid content (% dry matter) and energy content of four experimental diets for Nile tilapia fingerlings (Oreochromis niloticus) with different levels (0%, 30%, 60%, 100% on a protein basis) of spent brewer’s yeast (SBY) replacing soybean meal.
Table 2. Proximate chemical composition, amino acid content (% dry matter) and energy content of four experimental diets for Nile tilapia fingerlings (Oreochromis niloticus) with different levels (0%, 30%, 60%, 100% on a protein basis) of spent brewer’s yeast (SBY) replacing soybean meal.
Diet
SBY0 (Control) aSBY30 bSBY60 cSBY100 d
Dry matter92.693.991.792.2
Ash7.57.67.26.9
Crude protein28.628.828.928.8
Crude lipid11.39.99.07.5
Crude fibre3.23.33.23.2
NFE49.550.449.650.9
Gross energy (MJ.kg−1)19.619.119.819.1
Essential amino acids
Arginine1.541.661.631.52
Histidine0.550.690.760.39
Isoleucine0.730.720.700.65
Leucine2.002.082.112.06
Lysine1.601.752.081.99
Methionine0.590.540.650.67
Phenylalanine1.621.851.731.51
Threonine0.750.850.950.97
Valine0.890.930.961.05
Total10.2711.0711.5710.81
a 0% spent brewer’s yeast (control diet). b 30% spent brewer’s yeast replacing soybean meal, based on protein. c 60% spent brewer’s yeast replacing soybean meal, based on protein. d 100% spent brewer’s yeast replacing soybean meal, based on protein.
Table 3. LS-means of growth performance variables **, feed utilisation and survival rate of Nile tilapia fingerlings (Oreochromis niloticus) kept in a Bio-RAS (B) or clear-water RAS (C) and fed spent brewer’s yeast (SBY) at four different inclusion levels (0, 30, 60, 100 indicates a 0% 30%, 60% and 100% replacement of soybean meal protein with SBY protein).
Table 3. LS-means of growth performance variables **, feed utilisation and survival rate of Nile tilapia fingerlings (Oreochromis niloticus) kept in a Bio-RAS (B) or clear-water RAS (C) and fed spent brewer’s yeast (SBY) at four different inclusion levels (0, 30, 60, 100 indicates a 0% 30%, 60% and 100% replacement of soybean meal protein with SBY protein).
Dietary TreatmentSEMptotal *** ValuepY Valuepw Value
C0C30C60C100B0B30B60B100
Initial length, cm14.514.514.414.414.514.414.414.50.040.690.380.23
Final length, cm18.0 a18.8 ab18.8 ab18.5 a19.4 b19.6 b19.0 b18.7 ab0.300.0020.10.002
Initial body weight (g)50.450.449.850.650.350.450.450.00.480.940.930.93
Body weight (g) day 30101 ab102 ab102 ab94 b108 ac114 c106 ac106 ac2.3<0.00010.01<0.0001
Body weight (g) day 60 (final) **158 a166 a164 a148 c176 a199 b181 a172 a3.90.02<0.0001<0.0001
Specific growth rate (SGR), %/d1.9 ab2.0 ab2.0 ab1.8 b2.1 ac2.3 c2.2 cd2.0 abd0.10.0020.050.0006
Feed conversion rate (FCR)1.65 ab1.64 ab1.59 ad1.86 b1.46 ac1.28 c1.37 cd1.60 a0.090.00050.0150.0003
Protein conversion ratio (PCR), %39 ab40 ab40 ab35 a45 bd51 c47 cd41 ab2.30.0040.020.0004
PCR + Biofloc *, %-‖--‖--‖--‖-65 ce71 d66 c60 e2.30.00010.020.0001
Survival rate, %9798100100981001001001.40.300.240.39
SEM = Standard error of the mean; means within rows with different superscript letters are significantly different (p <0.05). -‖- equals the value in the row above. pW value = p value calculated between the two rearing systems (i.e., CW-RAS and Bio-RAS). pY value = p value calculated between different SBY inclusion levels. * Accumulated protein content in biofloc (concentration (as given in Table 4) × water volume) => protein retained in both fish and biofloc versus total amount given in diet. ** Body weight distribution at day 60 weighing as presented in Figure 1. *** Interaction between rearing system and SBY inclusion level was not significant for any variable (p > 0.3) and is therefore not shown.
Table 4. Proximate chemical composition and amino acid content (% of dry matter) of biofloc biomass in different periods of the experiment.
Table 4. Proximate chemical composition and amino acid content (% of dry matter) of biofloc biomass in different periods of the experiment.
PeriodSEMp-Value
Start 1Middle 2End 3
Dry matter (g m−3)8.20 c25.78 b71.41 a3.92<0.0001
Protein39.58 b43.80 ab44.62 a0.980.02
Lipid2.79 a1.50 ab0.61 b0.410.03
Essential amino acids
Arginine1.441.601.520.050.19
Histidine0.60 b0.71 ab0.77 a0.030.02
Isoleucine0.770.820.820.040.52
Leucine2.062.002.100.040.20
Lysine1.34 a1.20 b1.21 b0.02<0.0001
Methionine0.56 a0.44 b0.49 ab0.02<0.0001
Phenylalanine1.53 b1.59 ab1.68 a0.030.05
Threonine1.211.231.230.040.89
Valine1.241.281.350.040.15
Total10.7210.8611.180.220.37
1 0, 2 30th and 3 60th day of the experiment. 2 Biofloc was sampled in triplicate through three consecutive days at each sampling period, being start, middle and end, i.e., a total of 27 samples (9 per period) were obtained and analysed. Different superscript letters indicate statistically significant differences (p ≤ 0.05).
Table 5. Water quality parameters (mean ± standard deviation) in the Bio-RAS and clear-water (Cw-RAS) rearing system.
Table 5. Water quality parameters (mean ± standard deviation) in the Bio-RAS and clear-water (Cw-RAS) rearing system.
Temperature, °CDO, mg L−1pHTAN, mg L−1NO2-N, mg L−1
MorningAfternoonMorningAfternoon
Bio-RAS28.6 ± 0.3629.2 ± 0.444.81 ± 0.477.06 ± 0.227.95 ± 0.300.753 ± 0.2030.014 ± 0.002
Cw-RAS28.3 ± 0.5729.2 ± 0.604.65 ± 0.366.68 ± 0.237.24 ± 0.310.409 ± 0.2990.015 ± 0.003
DO: dissolved oxygen; TAN: total ammonia nitrogen; NO2-N: nitrite-nitrogen.
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Nhi, N.H.Y.; Lan, T.T.; Baruah, K.; Lundh, T.; Kiessling, A. Gradual Replacement of Soybean Meal with Brewer’s Yeast in Fingerling Nile Tilapia (Oreochromis niloticus) Diet, Resulting in a Polynomial Growth Pattern, Independent of Whether Reared in a Biofloc or Clear-Water System. Aquac. J. 2024, 4, 255-269. https://doi.org/10.3390/aquacj4040019

AMA Style

Nhi NHY, Lan TT, Baruah K, Lundh T, Kiessling A. Gradual Replacement of Soybean Meal with Brewer’s Yeast in Fingerling Nile Tilapia (Oreochromis niloticus) Diet, Resulting in a Polynomial Growth Pattern, Independent of Whether Reared in a Biofloc or Clear-Water System. Aquaculture Journal. 2024; 4(4):255-269. https://doi.org/10.3390/aquacj4040019

Chicago/Turabian Style

Nhi, Nguyen Huu Yen, Trinh Thi Lan, Kartik Baruah, Torbjörn Lundh, and Anders Kiessling. 2024. "Gradual Replacement of Soybean Meal with Brewer’s Yeast in Fingerling Nile Tilapia (Oreochromis niloticus) Diet, Resulting in a Polynomial Growth Pattern, Independent of Whether Reared in a Biofloc or Clear-Water System" Aquaculture Journal 4, no. 4: 255-269. https://doi.org/10.3390/aquacj4040019

APA Style

Nhi, N. H. Y., Lan, T. T., Baruah, K., Lundh, T., & Kiessling, A. (2024). Gradual Replacement of Soybean Meal with Brewer’s Yeast in Fingerling Nile Tilapia (Oreochromis niloticus) Diet, Resulting in a Polynomial Growth Pattern, Independent of Whether Reared in a Biofloc or Clear-Water System. Aquaculture Journal, 4(4), 255-269. https://doi.org/10.3390/aquacj4040019

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