By: Rendani Luthada-Raswiswi, Samson Mukaratirwa and Gordon O´Brien
Fishmeal prices have been raised even further because of competition with domestic animals, shortage in world fishmeal supply, and increased demand. Increased fishmeal prices have contributed to the quest for alternatives necessary to replace fishmeal as a global research priority. The use of animal protein sources as a replacement for fishmeal in fish diets has had a positive impact on the feed conversion ratio, variable growth rate, final weight, and survival rate of different types of fish species of different size groups.
By producing fish with minimal environmental impact and maximum benefit for society, aquaculture is predicted to contribute more effectively to economic development, international food safety, nutritional wellbeing, and poverty reduction. Aquaculture production (66 million tons) exceeded global beef production (63 million tons) for the first time in 2012. Increased aquaculture production means that more than half of the fish being consumed by humans worldwide is produced by aquaculture.
The quality of the protein ingredient used in feed formulation is generally known to have effects on the nutritional value of fish diets produced. The demand for feed resources, particularly for prime quality protein fishmeal, has increased because of the global supply of fish as aquaculture production increases. For both carnivorous and omnivorous species used in aquaculture, fishmeal has been used as an essential protein source, and many aquaculture formulations/feeds have a higher percentage of fishmeal than feeds of other animal species. Fluctuations in supply, price, and quality of fishmeal present considerable risks because fishmeal is dependable solely on an ingredient by people.
Therefore, the identification, development, and utilization of alternatives to fishmeal in diets in aquaculture remain a high priority as a risk reduction strategy. Competitive price, full availability, ease of handling, shipping, storage, and use in feed production are features that a candidate ingredient must possess to be a viable alternative feedstuff to fishmeal in aquaculture feeds.

Additionally, it should have high protein content, favorable amino acid profile, high nutrient digestibility, low fiber levels, starch, non-soluble carbohydrates, which are nutritional characteristics. The more expensive fishmeal has been replaced by several sources of plant protein, single-cell protein, and animal protein in part or in full.
Due to higher protein and lipid content, superior essential amino acids, and excellent palatability, animal protein sources have commonly been considered ideal substitute protein sources to replace fishmeal in formulating fish diets. The purpose of this study was to conduct a systematic review of published articles on animal protein sources used in aquaculture and assess the results of recommended diets against the control diet.
Materials and Methods
A systematic search of published literature on Google Scholar and EBSCOhost from 1999 to 2019 was carried out using the following terms or phrases: Fishmeal replacements in fish feeds, fishmeal alternatives in fish diets, animal protein sources in aquaculture, insects in fish feeds, terrestrial by-product, and fishery byproducts. Meta-analysis was conducted for final weight, specific growth rate, feed conversion ratio, and survival rate.
Results
There were 1030 articles obtained from search engines, and additional records were identified through other sources. Eligibility was evaluated for 217 articles, and 18 articles were included in the systematic review and meta-analysis.
Fish Species Used and Recommended Levels of Animal Protein Sources
Results from the review articles showed that animal protein sources replacing fishmeal ranged from insects (Mopane worms (Imbrasia belina), grasshoppers (Zonocerus variegatus), field crickets (Gryllus bimaculatus), blowfly maggot (Chrysomya megacephala), black soldier fly (Hermetia illucens) and superworm (Zophobas morio), terrestrial animal by-products (fermented feather meal, feather meal, poultry by-products, meat and bone meal, and blood meal), and fishery by-products (fish silage, shrimp head meal and krill meal).
Furthermore, a variety of fish species such as Oreochromis mossambicus, Clarias gariepinus, Oreochromis niloticus, Sparus aurata, Dicentrarchus labrax, Scophthamus maeotinus, Lutjanus guttatus, Ophiocephalus argus, Red tilapia (O. mossambicus × O. niloticus × Oreochromis aureus), and Acipenser glueldenstaedtii (which were not selected but reported because it is important to know when reporting for protein sources used) have been used. Animal protein sources inclusion levels in the diets ranged from 0%, 5%, 10%, 20%, 25%, 30%, 40%, 50%, 60%, 75%, to 100%.
Recommended levels of animal protein sources in feeds were 20% for feather and shrimp head meal for C. gariepinus, 20% of meat and bone meal for Op. argus, 25% of superworm, poultry by-product and grasshopper meal for L. guttatus and C. gariepinus respectively, 30% of krill meal for A. glueldenstaedtii, 20–50% of fermented feather meal for O. niloticus, 50% of poultry by-products and fish silage for O. niloticus and Red tilapia (O. mossambicus × O. niloticus × O. aureus), respectively, 60% of mopane worm meal for O. mossambicus and 100% of field cricket meal for C. gariepinus.
Values for Final Weight, Specific Growth Rate, Feed Conversion Ratio, and Survival Ratio
The specific growth rate ranged from 0.56% to 7.89%. Feed conversion ratios of 1.25, 1.51, and 2.20 were reported for O. mossambicus, C. gariepinus, and C. gariepi- nus, which were fed insect meal (I. belina, Z. variegatus, and G. bimaculatus), respectively. For terrestrial by-products (fermented feather meal, feather meal, poultry by-products, poultry by-products, and meat and bone meal), feed conversion ratios of 1.73, 1.34, 1.20, 140, and 1.24 were obtained for O. niloticus, C. gariepinus, L. guttatus, O. niloticus, and Op. argus, respectively. Feed conversion ratios of 1.35, 2.50, and 1.10 were obtained in Red tilapia (O. mossambicus × O. niloticus × O. aureus), C. gariepinus, and A. glueldenstaedtii fed fishery-by products (fish silage, shrimp head meal, and krill meal), respectively. Survival rate ranged from 83% to 100%, except for Red tilapia (O. mossambicus × O. niloticus × O. aureus) and C. gariepinus, which were fed fish silage and shrimp head meal, respectively, where the survival rate was not reported.
Meta-Analysis
For the meta-analysis, data from studies analyzed were grouped into final weight, specific growth rate, feed conversion ratio, and survival rate. Samples analyzed were 1335, 1430, 1450, and 1307 for final weight, specific growth rate, feed conversion ratio, and survival rate, respectively. Results showed the overall effect size of 9015. The level of heterogeneity observed were I2 = 99.70%, I2 = -17.73%, I2 = -25.79%, and I2 = 101.08% for final weight, specific growth rate, feed conversion ratio, and survival rate, respectively.

Discussion
Human health benefits, competitive price, fish safety, efficiency, customer acceptance, minimal contamination, and ecosystem stress are factors in selecting feeds. Growth performance measured by final weight and specific growth rate showed that excess protein could not be used efficiently for growth because of growth energy used for the deamination and excretion of absorbed excess amino acids.
After all, each fish species had a specific protein limit. When dietary protein levels increase, the feed conversion ratio decreases. Recommended levels reported for insect meal in this review shows that a total fish- meal replacement has not been successful. Limitations of using insects include their (i) varying nutritional value, which is dependent on the species, stage of development, and the substrate used to feed the insect, (ii) low con- centration of sulfur-containing amino acids, and (iii) absence of eicosapentaenoic and docosahexaenoic.
Fermented feather meal, blood meal, poultry by-products, feather meal, meat and bone meal are some of the terrestrial animal by-products used in aquaculture diets. Terrestrial by-products have been reported to have great potential as fishmeal replacement because they are readily available, economical sources of protein and have more complete amino acid profiles than vegetable proteins.
The use of feather meal in aquaculture feeds is limited by the fact that fish are unable to digest it. Fishery by-products are products generated from fishery industries. Skin and fins, scales, heads and bones, viscera, and muscle trimmings are the main by-products produced in fishery industries with (1–3%), (5%), (9–15%), (12–18%), and (15–20%), respectively Limiting factors of using fishery by-products include the cost of the collection of fish waste, timely processing, and quality control.

Furthermore, fish waste varies highly in its physical nature and proximate composition; and some fish waste such as from seafood is only available during the fishing season. Results for final weight, specific growth rate, feed conversion ratio, and survival rate, shows that there is a statistically significant difference among studies. The level of heterogeneity (I2 index) was very high for both the final weight and survival rate with values 99.98 and 101.08, respectively.
Final weight, specific growth rate, feed conversion ratio and survival rate of fish in experiment or in farming in general are affected by many factors such as age of fish, fish species, stocking density, feeding level and frequency, protein source, and water quality parameters such as water temperature, dissolved oxygen, and pH.
Variety of fish species, size, inclusion levels, recommended levels of protein found were reported, and these are the reasons our meta-analysis indicated heterogeneity in studies. Despite all the heterogeneity observed, 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.
Conclusions
Despite the limitations in the use of insects, terrestrial by-products, and fishery by- products as replacement of 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. However, future studies have recommended to (i) identify a fishmeal replacement that has no limitations, (ii) assessing the suitability of readily available animal meat or by-products as fishmeal replacement.
This is a summarized version developed by the editorial team of Aquaculture Magazine based on the review article titled “Animal Protein Sources as a Substitute for Fishmeal in Aquaculture Diets: A Systematic Review and Meta-Analysis” developed by: Rendani Luthada-Raswiswi, Samson Mukaratirwa and Gordon O´Brien. The original version was published in April 2021 through Applied Sciences.
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