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Protein Fishmeal Replacement in Aquaculture: A Systematic Review and Implications on Growth and Adoption Viability in the Philippines

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22 May 2023

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23 May 2023

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Abstract
Aquaculture is growing rapidly as a food-producing sector and in recent years, fishmeal prices have climbed by more than twofold on a global scale. This review of previous studies was performed to contribute to the extant literature on the aquaculture sector to aid cost reduction of aquafeeds by identifying substitute protein that can replace fishmeal. The review followed the Preferred Reporting Items for Systematic Review and Meta-Analyses (PRISMA) using the SCOPUS and WOS (Web of Science), DOAJ (Directory of Open Access Journals), Academia, and Pubmed Central databases with the following search terms: “fishmeal,” “alternative protein source” and “aquafeeds.” This resulted in 5,331 articles from the SCOPUS and WOS databases. Finally, the titles and abstracts of the articles were screened, giving a total of 162 articles that were used in the study; another 58 articles came from open databases. Results have shown that 100% replacement of fishmeal with blood meal did not affect the growth of fish as well as 75% to 100% combination of poultry-by-product (PBM), feather meal (FEM), and blood meal (BM). Moreover, a 10% replacement of fishmeal using seaweed (Gracilaria arcuata) has no adverse effect on feed efficiency and growth performance of tilapia, a 50% replacement of fishmeal using black soldier fly (Hermetia illucens), and 25% replacement using soybean (Glycine max) also showed better results for fish growth. With that, this review shows that alternative protein can be a great alternative to the aquaculture sector in reducing the cost of aquafeeds since alternative proteins are much cheaper than the usual fishmeal.
Keywords: 
Subject: Biology and Life Sciences  -   Aquatic Science

Introduction

Aquaculture is growing rapidly as a food-producing sector globally and flourishing day by day (Hodar et al., 2020; Syed et al., 2022; Habib et al., 2020; Mengo et al., 2023).It has been introduced in various regions of developing nations, including Africa and Asia, to provide local rural communities with the opportunity to raise their standard of living and a means of escaping poverty (Olaganathan & Kar Mun, 2017), generating household income (Moisa et al., 2022: Tran et al., 2023). Fish meal makes up between 50 and 70 percent of the total material in fish feed (Jannathulla et al., 2019); it is highly considered a feed protein source since it has an excellent composition of amino acids and is easy to digest (Olsen & Hasan, 2012). Moreover, the feed cost is 60% to 70% of an aquaculture farm’s total operating expenses out of all input costs. In contrast, the decreasing fish catches (Macusi et al., 2022) and consistent growth in fishmeal consumption create a gloomy future for the aquaculture industry, but not if there is a paradigm shift toward the utilization of non-fish components for fish feed production. Over the next 20 years, aquaculture is projected to expand due to increased demand for fishmeal. Fish oil (FO) and fish meal (FM) could increase pressure on the diminishing stocks of marine fish production (Aladetohun & Sogbesan, 2013; Oliva et al., 2022). In recent years, fishmeal prices have climbed more than twofold globally (FAO, 2013; Lin et al., 2022; Bansemer et al., 2023). In Asia alone, fishmeal consumption for Nile tilapia climbed from 0.8 million tons to 1.7 million tons during the same period, while fish feed output increased from 40% in 2000 to 60% in 2008 (Tacon & Metian, 2008). According to FAO (2001), lowering the amount of fish meal and fish oil in feeds is a huge step toward mitigating the pressure on global marine resource scarcity. Substituting fishmeal at the farm level could reduce expenses associated with production (De Francesco et al., 2007). The essential amino acid compositions of alternative protein sources for fish are not comparable with that of fishmeal; however, mixing several alternative protein sources with various limiting amino acids such as lysine, methionine, threonine, and tryptophan has been strongly suggested (Ogunji & Wirth, 2001). Fish meal (FM) is obviously inadequate to support the huge demand for fish feed with rising aquaculture production, and use of feed has to be declined (Wang et al., 2023; FAO 2022). Therefore, it’s an urgent need to find an alternative protein source to replace FM (Wang et al., 2023; Galkanda et al., 2020). Several sources of plant protein, single-cell protein, and animal protein have partially or entirely replaced the more expensive fishmeal. Animal protein sources have traditionally been regarded as the best alternative to replace fishmeal in the formulation of fish meals due to their higher protein and fat content, superior essential amino acids, and excellent palatability. (Yigit et al., 2006). On the other hand, plant ingredients that contain high protein content, high digestibility of crude protein, and low anti-nutritional components can replace fishmeal as a substitute alternative protein source for fish (Dersjant-Li, 2021). Plant proteins are almost similar to fishmeal in protein content and amino acid digestibility. However, their amino acid profile does not match the amino acid requirement of some fish species as fishmeal does. For example, methionine is the limiting amino acid in soybean meal (SBM), while corn gluten meal is deficient in lysine. Wheat gluten meal is limited in lysine and arginine (Ogello et al., 2014). According to De Francesco et al. (2007), the impact of plant protein as a partial replacement for fishmeal shows contrasting results on the chemical composition of muscles. Soy products, including soybean meal and soy protein concentrate (SPC), have been researched as potential protein substitutes for fishmeal (Trejo-Escamilla et al., 2017) because of their high digestibility, high protein content, well-balanced amino acid, low price, and steady supply, soybean meals are widely used as the most effective substitute for fish meal in feeds for aquaculture (Zhou et al., 2005). In addition, soybean concentrate can replace fishmeal for up to 40% to 100% (Dersjant-Li, 2021). Another plant protein that is used for fishmeal replacement is seaweeds; it contains a good level of minerals, vitamins, carotenoid pigments, bioactive compounds, fatty acids, and amino acids, which are highly required components in fish feed making (Qiu et al., 2018). According to some studies, the partial substitution of fishmeal by seaweeds can positively affect growth, feed utilization, body composition, and resistance to stress and diseases (Guroy et al., 2013). Methionine is an amino acid found in large quantities in some seaweed species, such as Palmaria palmata. However, it is found in much lower amounts in other species of brown seaweed, such as Laminaria digitata (Fleurence, 2004). Cocoa bean shell has also been reported to contain 13.2% to 17.7% crude protein and 13.0% to 16.1% of fiber (Chung et al., 2003). However, theobromine content of 1.3% in cocoa shell limits its usage for feeding, which is a downside as a replacement for fishmeal. Another protein used as a replacement for fishmeal is cacao pod husk (CPH); it is a by-product during cacao production. Using this product as a replacement for fishmeal will eliminate environmental waste since it can be obtained at little to no cost to aquaculture farmers (Ashade, 2010). Navya (2007), studied the growth of Nile tilapia (Oreochromis niloticus) fingerlings fed varied levels of cocoa pod husk diets and discovered that fish weight gains and specific growth rates are lower with above 10% inclusion level than those of the control animals fed fishmeal-based diets. The high fibre content of the cocoa pod husk was the reason for the decrease in growth. Cocoa pod husk also has anti-nutritional factors such as theobromine; however, according to a study by (Ocran (2020), the negative effect of anti-nutritional factors can be eliminated through fermentation. Following the study of Ogello et al. (2014), the main terrestrial by-product meals used as a replacement for fishmeal are blood, insect, feather, and meat and bone. Regardless of its high crude protein content, these alternative proteins commonly lack amino acids, which limits the growth of the aquaculture species. One of the additional animal protein sources that can be utilized to replace fishmeal is poultry by-products. It was thought to be a significant replacement for fishmeal, particularly in rainbow trout since it has a similar composition of amino acids to fishmeal (FM) (Bureau et al., 2000). On the other hand, maggots are usually considered not to have any economic value. However, according to Ajani et al. (2004), it has the potential as a good source of animal protein in fish diets. Adesulu and Mustapha (2000) reported that some essential amino acids, including cystine, histidine, phenylalanine, tryptophan, and tyrosine are present in maggot meal and are higher than that in fishmeal and soybean meal. Utilizing maggot meal as a source of protein for a fish diet is a good way of reducing the cost of waste disposal in the poultry industry, which can help generate additional income for the fish and poultry industry. This review paper was performed to help the aquaculture sector reduce the cost of aquafeeds by identifying sources of substitute protein that can be used in place of fishmeal and to assess the progress in feed development that can be an alternative choice to existing commercial feeds in the aquaculture industry in the Davao region, Philippines.

Methodology

This review paper followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) to address and evaluate the objectives of the study. In order to further understand the possible alternative protein sources for fishmeal and to assess its effect on the growth of cultured species, a comprehensive literature review using the methods used in an earlier paper, e.g., Macusi et al., 2022 and Page et al., 2021, was conducted. The literature searched in this review was limited to the year 2000 and the present on four citation databases: Scopus/WOS, DOAJ (Directory of Open Access Journals), Academia, and PubMed Central. Data searching was first used to locate the records, and then duplicates were eliminated. The articles that did not match the eligibility requirements were then removed throughout the subsequent screening and data extraction process. By looking through t abstracts or contents, the remaining articles were evaluated to check relevance to the topic of interest to meet the qualifying requirements. The literature reviewed was chosen based on inclusion criteria in the final phase based on the publications that passed the eligibility evaluation. The terms “fishmeal,” “alternative protein source,” and “aquafeeds” were used to make sure the search focused only on the literature related to the study.
Exclusion and inclusion criteria were applied to screen the articles used in this review. A total of 5,331 was found in the Scopus database by using the keywords above (see Figure 1); it was then reduced to 1,714 by eliminating the duplicate articles found in the database. After removing the duplicates, articles were again screened to 288 by removing the articles that did not match the criteria for inclusion based on the title of the articles. Following the inclusion of criteria based on the abstract, 162 articles were record screened on the Scopus/WOS database. The same method was used on the open-access databases: DOAJ, PubMed, and Academia. One hundred twenty-four (124) articles were found in the three databases; 66 duplicate articles were removed, with fifty-eight (58) articles recorded, screened, and remaining based on the inclusion criteria. A total of forty (40) articles were included in the review on the basis that they passed the eligibility assessment.

RESULTS

Figure 2 shows the distribution of scientific production of fishmeal for the aquaculture industry; Egypt (18%), Brazil (12%), China (9%), Malaysia (6%), Thailand (5 %), and the USA (5%) top the list. While Figure 3 presents the co-occurrence map of authors’ keywords, while Figure 4 presents the co-occurrence map for titles and abstracts. Forty-nine (49) author and index keywords and 44 text data from the articles’ abstracts and titles were extracted and visualized in the co-occurrence map.
Table 1 presents the co-occurrence classification for the index and author keywords in terms of links, total link strengths, and occurrences. ‘Oreochromis niloticus,’ ‘growth, ‘Cichlid,’ ‘tilapia,’ and ‘Nile tilapia’ are keywords with the highest occurrences. In contrast ‘Cichlid,’ ‘Oreochromis niloticus,’ ‘diet,’ ‘growth rate,’ and ‘growth’ are the keywords with the highest total link strengths. The cluster analysis of keywords shows three clusters, as presented in Table 1. Under cluster 1, Cichlid, growth, growth rate, and Oreochromis niloticus have the highest link strength referring to the cultured Nile tilapia (Oreochromis niloticus). Under cluster 2, animal feed, animal food, diet, and food intake have the highest total link strength, which refers to the feed diet. For cluster 3, aquaculture, growth performance, immune response, and Nile tilapia have the highest total link strength, which refers to the effect of the diet on the growth of tilapia or cultured species.
In terms of abstract and keywords (see Figure 4), the most common words based on the cluster analysis revealed four clusters. Words with the highest occurrences include ‘difference,’ ‘feed conversion ratio,’ ‘meal,’ ‘fish meal,’ ‘response,’ and ‘crude protein.’
Table 2 presents the occurrence classification of texts from abstracts and titles in terms of links, total link strength, and occurrences. Under cluster 1, words with the highest total link strength include meal, fishmeal, difference, and replacement which refer to the feed or diet used in the study. Under cluster 2, crude protein, digestibility, feed conversion ratio, and fish meal have the highest total link strength, which has reference to the performance of the diet or feeds used. For cluster 3, immune response, resistance, response, and survival have the highest total link strength, again with reference to the effect of the diet on the growth performance of the fish. Under cluster 4, the liver, gene, muscle, and expression have the highest total link strengths, which refer to the main organ examined in fish to check diet toxicity and immune response.
Figure 4 and Figure 5 show an overlay visualization of frequently used terms from the the fishmeal studies’ keywords, titles, and abstracts from 2000 to 2022. These present the trend in fishmeal research across the globe during the period. The recent studies are quite varied and include growth performance, gene expression, disease resistance, dietary supplement, replacement, resistance, response, health, and survival.
Table 3 below summarizes the alternative proteins that can be used as a fishmeal replacement in aquafeed for culturing fish. Of all these replacements, blood meal can replace the fishmeal 100% with positive growth on the fish. In contrast, poultry-based by-products, feather meal, and bone meal can replace it with 75-100% effectivity, similar to the fishmeal diet. Seaweed can replace about 10% of the fishmeal diet in tests, while soybean meal can replace about 25% of the fishmeal diet, and insect-based diets can replace 50% of the fishmeal diet.

DISCUSSION

Growth effect of alternative protein for fishmeal

From the result of this review, a variety of alternative proteins is used to replace fishmeal in fish diets, including animal and plant-based meals. Growth performance, as determined by final weight and specific growth rate, revealed that extra protein could not be utilized efficiently for growth because growth energy was required to deaminate and extract ingested excess amino acids (Luthada-Raswiswi et al., 2021). In the study conducted by Zlaugotne et al. (2022), feed ingredients impact fish and the environment since it is necessary to evaluate feed materials and whether or not an alternative is possible would be more effective and have less impact on the environment. The alternative fish feed must have high nutritional content and quality and high protein content, adequate amino acids, and digestibility and palatability. In addition, alternative fish feed should have insoluble carbohydrates, fiber, and heavy metals that need to be low because it affects the fish growth process and low feed conversion ratio; feed costs must be economically justified and feed production (Nagappan et al., 2021).

Animal meal replacement and their input to the growth

Previous research conducted by Aladetuhon and Sogbesan (2013) stated that adding blood meal to the experimental diet promotes the growth of the fish from the start of the trial, the specific growth rate (SGR), weight gain (WG), biweekly growth rate (BGR), protein retention (PR), and food conversion ratio (FCR) has gradually increased and at its peak with 100% blood meal replacement. It is said that the survival rate is high in all the diets with blood meal as a dietary supplement for fishmeal. Additionally, previous research has discovered that fish fed replaced fishmeal up to 75% to 100% with the combination of poultry by-product meal (PBM), feather meal (FEM), and blood meal (BM) showed a better or similar specific growth rate and weight gain compared with the fish fed control diet (Lu, Haga & Sato, 2015). It resulted in no negative impact on the final body weight, weight gain, or specific growth rate of rainbow trout. It reported that rainbow trout performed better in growth when fed with a mixture of poultry by-product meal, feather meal, and blood meal. Furthermore, insect meal is a protein replacement for fishmeal that is highly considered to be one of the most interesting protein substitutes. According to a study by Melechon et al. (2022), replacing 50% of fishmeal with different larvae of insect meal like Hermetia illucens (HI) and Tenebrio molitor (TM) appears to have a better result for growth, protein utilization, and more digestive functions. In addition, liver histology and intermediary metabolism did not show any relevant changes, supported by intestinal histological differences between insect meals. In contrast, regardless of the limitations in the use of insects, terrestrial by-products, and fishery by-products as replacements for fishmeal, these animal protein sources have shown positive effects on feed conversion ratio, specific growth rate, final weight, and survival of different fish species of different size groups.

Plant-based meal replacement and their input to growth

Soybean meal is considered to be one of the most suitable and reliable sources of an alternative component for substituting fishmeal in commercial fish diets (Zhou, Mai, et al.,2004). During seven weeks feeding trial, 25% of the dietary protein from a fish meal could be substituted with soybean meal without significantly affecting the tilapia’s ability to thrive (Dersjant-Li, 2021). In contrast, high levels of soybean meal (40%-60% for juvenile fish) cause a reduction in growth and survival rates (Liu et al., 2017). Similarly, T. macdonaldi can only tolerate up to 34.17% of soy protein concentration (SPC) substitution before it develops some adverse effects on the fish, mainly due to the non-digestible carbohydrates and enzyme inhibitors present in soybean meal and soy protein concentrate (Olmos et al., 2022). On the other hand, the study of Silva et al. (2015) on utilizing seaweed as a protein feed replacement to fishmeal shows that the inclusion level of up to 10% in practical diets has no adverse effect on feed efficiency and growth performance of Nile tilapia. These were in agreement with the data obtained by Al-Asgah (2016), who found that increasing incorporation of red seaweed Gracilaria arcuata up to 10% shows no adverse effect on the growth of African catfish. In contrast, the high inclusion level of G. arcuata, up to 20% to 30% in the diets of African catfish, results in poor growth performance, feed utilization, and feed intake. However, future studies have recommended identifying a fishmeal replacement with no limitations and assessing the suitability of readily available alternative proteins as fishmeal replacement (Luthada-Raswiswi et al., 2021).

Alternative protein sources benefit, implications to food security, and their limits

The most pressing problem facing the aquaculture industry remains the feed cost, and there is considerable pressure on feed companies to develop less expensive formulations that maintain efficient growth at a lower cost per unit gain (Hardy, 2010). To meet this goal, feed companies should lower the fishmeal levels further. Replacing the usual fishmeal with alternative protein sources can significantly benefit the fishing industry since these protein sources are far less expensive than fishmeal. On the other hand, alternative protein allows flexibility in feed formulations when feed ingredients fluctuate, which can also benefit the fishing industry greatly. According to Mulumpwa (2018), a fish product to be adequately available on the market may rely on how alternative protein is incorporated into fish feeds. Using alternative proteins as a replacement for fishmeal has the potential for increasing fish production, hence improving food security. However, challenges to be resolved are food acceptance, food safety issues, and legislation, which can be dealt with by the coordination of government and industry. Moreover, lack of support, mainly, financial from the government could perhaps be one of the limiting factors for the adoption of alternative protein as a replacement for fishmeal.

Adoption viability of alternative protein in the aquaculture industry

The spread of aquaculture production and intensification requires the search for high-quality, new efficient feed ingredients with low cost and sustainable importance (Ashour et al., 2021). Fishmeal, the most expensive component in aquatic diets, is considered one of the most critical challenges in the development of the aquaculture industry. Given the projected increase in production of these species and associated aquafeed demand, substituting fishmeal with alternative protein sources in these diets will considerably reduce the total quantity of fishmeal used (Hua et al., 2019). Significant gains in aquaculture production to supply additional protein, especially for freshwater fish, may also be made by combining alternative proteins or plant-based meals and animal-based meals to meet the needed requirements for fish growth (Holdt & Edwards, 2014). While detailed knowledge is required to balance multiple species, these systems have the added benefits of nutrient bioremediation and positive consumer perception (Park et al., 2018). Given these challenges, there is enormous potential for technological improvements to consistently produce high-quality alternative protein products with enhanced nutritional profiles. Some protein sources, such as fish byproducts and insect meals, are viable and promising alternatives to conventional fishmeal. Feed supplements can also be used to balance the nutrient composition of the feeds and functional ingredients can be used to facilitate the replacement of fishmeal with alternative ingredients. Furthermore, using multiple protein sources allows flexibility in feed formulations when ingredient prices fluctuate, as feed manufacturers often use cost as a determinant in selecting ingredients (Pelletier et al., 2018). Therefore, developing and optimizing alternative protein sources for aquafeeds will ensure a socially and environmentally sustainable future for the aquaculture industry.

Summary and conclusion

This review paper was performed to inform the aquaculture sector to reduce the cost of aquafeeds by identifying sources of substitute protein that can be used in place of fishmeal and to assess the progress in feed development that can be an alternative choice to existing commercial feeds in the aquaculture industry in the Davao region, Philippines.
The literature review followed the Preferred Reporting Items for Systematic Review and Meta-Analyses (PRISMA) using the SCOPUS/WOS (Web of Science), DOAJ (Directory of Open Access Journals), Academia, and Pubmed Central databases with the following search terms: “fishmeal”, “alternative protein source” and “aquafeeds”. This gave a result of 5,331 journal articles from the SCOPUS/WOS databases and 1,714 of which were removed for duplicates. Finally, the titles and abstracts of the articles were screened, giving a total of 162 articles that were used in the study. In comparison, additional 58 articles came from the open DOAJ, Academia and Pubmed databases. Moreover, lack of support, mainly, financial from the government could perhaps be one of the limiting factors for the adoption of alternative protein as a replacement for fishmeal.

Author Contributions

Conceptualization, E.D.M., M.A.C., and A.C.S.; methodology, E.D.M., E.Q.B., M.A.C., A.C.S., A.H., N.F., and M.D.S; software, E.Q.B., M.A.C.; validation, E.D.M, M.A.C., A.C.S., A.H., N.F., M.D.S.; formal analysis, E.D.M., M.A.C., A.C.S., E.Q.B.; investigation, E.D.M, M.A.C., E.Q.B., N.F., A.H., and M.D.S.; resources, E.D.M., A.C.S. ; data curation, E.D.M, and M.A.C. writing—original draft preparation, M.A.C..; writing—review and editing, E.D.M, M.A.C., A.C.S., A.H., N.F., M.D.S.; visualization, E.Q.B., M.A.C.; supervision, E.D.M, A.C.S., N.F., and M.D.S.; project administration, E.D.M.; funding acquisition, E.D.M.. All authors have read and agreed to the publication of this manuscript.

Funding

The first author received funding from the Department of Agriculture, Philippine Rural Development Project (DA-PRDP) and the Department of Science and Technology Region 11 (DOST-XI) with the study entitled: “Enhancing food security, social inclusion, and sustainability in the milkfish aquaculture through the use of indigenous raw materials as feed components”.

Data Availability Statement

The data can be requested from the authors

Conflicts of Interest

The authors declare no conflict of interest

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Figure 1. Flow of information using the Preferred Reporting Items for systematic Review (PRISMA).
Figure 1. Flow of information using the Preferred Reporting Items for systematic Review (PRISMA).
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Figure 2. Distribution of scientific production globally, with Egypt, Brazil, China, Malaysia, Thailand, and the USA top the list.
Figure 2. Distribution of scientific production globally, with Egypt, Brazil, China, Malaysia, Thailand, and the USA top the list.
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Figure 3. Co-occurrence network map based on keywords.
Figure 3. Co-occurrence network map based on keywords.
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Figure 4. Co-occurrence network map based on titles and abstracts.
Figure 4. Co-occurrence network map based on titles and abstracts.
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Figure 4. Overlay visualization of most frequently-used keywords on fishmeal studies from 2000-2022.
Figure 4. Overlay visualization of most frequently-used keywords on fishmeal studies from 2000-2022.
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Figure 5. Overlay visualization of most frequently used terms from abstracts and titles on fishmeal studies from 2000-2022.
Figure 5. Overlay visualization of most frequently used terms from abstracts and titles on fishmeal studies from 2000-2022.
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Table 1. Occurrence classifications of texts from keywords (four keywords from the three clusters that have high total link strengths are in bold).
Table 1. Occurrence classifications of texts from keywords (four keywords from the three clusters that have high total link strengths are in bold).
Keywords Links Total Link Strength Occurrences
Cluster 1
Amino acid 22 36 5
Artificial diet 33 77 10
Bacterium 33 72 7
Cichlid 46 272 34
Digestibility 29 75 14
Enzyme activity 34 96 12
Fatty acid 17 27 5
Feeding 32 55 9
Fish 24 39 11
Fish culture 21 39 6
Food supplementation 27 57 8
Growth 44 179 39
Growth rate 46 188 25
Growth response 32 67 8
Lipid 21 33 5
Oreochromis 14 22 5
Oreochromis mossambicus 11 26 6
Oreochromis niloticus 45 264 47
Performance assessment 22 33 5
Phytase 11 14 5
Protein 34 96 14
Saccharomyces cerevisiae 26 48 6
Survival 28 44 5
Tilapia 42 159 31
Cluster 2
Animal feed 31 101 8
Animal food 32 118 10
Antioxidant 25 48 7
Body weight 27 60 5
Cichlids 30 99 9
Diet 41 199 23
Diet supplementation 36 95 9
Dietary supplement 29 95 8
Dietary supplements 29 95 9
Disease resistance 18 32 6
Fish meal 26 42 5
Food intake 35 109 10
Metabolism 36 95 9
Nutrition 21 30 5
Cluster 3
Animal tissue 29 66 7
Aquaculture 36 119 22
Feed utilization 10 14 5
Fish nutrition 8 10 5
Fishmeal 4 6 6
Gene expression 28 48 10
Growth performance 39 91 23
Hematology 11 17 5
Histopathology 29 57 6
Immune response 36 96 14
Nile tilapia 38 156 30
Table 2. Occurrence classifications of texts from abstracts and titles (four keywords from the three clusters that have high total link strengths are in bold).
Table 2. Occurrence classifications of texts from abstracts and titles (four keywords from the three clusters that have high total link strengths are in bold).
Abstract/Title Links Total Link Strength Occurrences
Cluster 1
Alternative protein source 35 98 12
Aquaculture 41 191 28
Aquafeed 39 155 21
Difference 43 224 42
Fish growth 39 83 13
Fish meal 42 250 34
Health 42 128 20
Impact 40 130 19
Meal 43 257 38
Oncorhynchus mykiss 27 77 10
Plant 41 142 22
Plant protein 32 86 11
Production 35 105 18
Protein source 41 157 22
Rainbow trout 27 83 11
Replacement 41 216 30
Use 43 195 29
Cluster 2
Body composition 37 114 23
Crude protein 37 169 31
Digestibility 38 133 21
Dry matter 37 109 16
Energy 41 127 22
Feed conversion ratio 38 211 39
Fingerling 38 115 24
Fish meal 43 154 21
Nutrient digestibility 37 87 15
Protein efficiency ratio 38 147 27
Soybean meal 37 84 14
Cluster 3
Basal diet 31 60 12
Dietary supplementation 33 82 17
Final weight 36 88 15
Immune response 40 125 21
Juvenile Nile tilapia 34 66 12
Resistance 38 114 22
Response 41 192 31
Survival 36 119 22
Survival rate 33 83 19
Cluster 4
Dietary 29 53 10
Expression 32 81 14
Fatty acid 28 64 12
Fish fed diet 32 48 10
Gene 34 111 17
Liver 42 154 29
Muscle 33 103 19
Table 3. Summary of different alternative proteins and their effects on the growth of cultured fish.
Table 3. Summary of different alternative proteins and their effects on the growth of cultured fish.
Alternative Protein Percentage replacement (%) Growth effect on Fish References
Blood meal 100 Positive increased the growth of fish Aladetuhon & Sogbesan, 2013
PBM, FEM, BM 75 to 100 Similar specific growth rate and weight gain compared with the fish-fed control diet Lu, Haga & Sato, 2015
Seaweed (Gracilaria arcuata) 10 No negative effect in feed efficiency and growth performance of Nile Tilapia Silva et al., 2016 and Al-asgah, 2016
Black Soldier Fly (Hermetia illucens) 50 Better results for growth, protein utilization and digestive functions Melencion et al., 2022
Soybean meal
(Glycine max) 		25 Without significant effect on tilapia’s growth Liu et al., 2017
Legend: PBM (Poultry by-product), FEM (Feather meal), BM (Bone meal).
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Copyright: This open access article is published under a Creative Commons CC BY 4.0 license, which permit the free download, distribution, and reuse, provided that the author and preprint are cited in any reuse.
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