Responses of Rainbow Trout to Fishmeal Replacement with Terrestrial/Aerial Animal Proteins

McLean, Ewen; Smith, Sofea; Brodeur, Ford; Barrows, Frederic T.

doi:10.3390/fishes11040198

Open AccessEditor’s ChoiceReview

Responses of Rainbow Trout to Fishmeal Replacement with Terrestrial/Aerial Animal Proteins

by

Ewen McLean

^1,*

,

Sofea Smith

²,

Ford Brodeur

³ and

Frederic T. Barrows

⁴

¹

Aqua Cognoscenti LLC, 479 Henslowe Lane, West Columbia, SC 29170, USA

²

Department of Kinesiology & Physical Therapy, University of Central Florida, Orlando, FL 32816, USA

³

Anthropocene Institute, Palo Alto, CA 94301, USA

⁴

Aquatic Feed Technologies LLC, Islamorada, FL 33036, USA

^*

Author to whom correspondence should be addressed.

Fishes 2026, 11(4), 198; https://doi.org/10.3390/fishes11040198

Submission received: 5 March 2026 / Revised: 20 March 2026 / Accepted: 23 March 2026 / Published: 26 March 2026

(This article belongs to the Special Issue Sustainable Aquaculture and Seafood Production)

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Abstract

Research designed to reduce or eliminate fishmeal (FM) in trout feeds, for reasons that have changed over time, has been conducted for over a century. Reducing the dependency on FM remains one of the most urgent issues facing the industry. Feed represents the most expensive operational cost of fed aquaculture, and is responsible for ecosystem disturbance following nutrient discharges. Rainbow trout, the second most farmed salmonid globally, can be raised completely without FM or fish oil (FO), with its growth and efficiency not differing from trout fed FM-based feeds. However, ingredient choice and nutrient supplementation strongly influence physiological responses, efficiency, and long-term outcomes. As land animal proteins are increasingly used in place of FM, both with and void of dietary FO, their distinct biological effects warrant focused evaluation. Although numerous studies have synthesized findings across various alternative protein categories including those with insect proteins and animal by-products, this literature is widely disseminated and sometimes difficult to access. The present contribution focuses on terrestrial/aerial animal proteins that have been used to totally replace FM in rainbow trout feeds. Attention is given to their effects on physiological control processes that may influence production efficiency. Areas worthy of future study are identified and include long-term performance and health dynamics, the refinement of nutritional and formulation strategies, and the broader evaluation of biological interactions and system-level outcomes.

Keywords:

insect meal; poultry by-product meal; alternate proteins; trout; amino acid balance; physiological response

Key Contribution: The paper assembles a broadly distributed information base on the complete removal of fishmeal (FM) from trout feeds using animal proteins. Emphasis is given to the consequences of FM replacement on trout’s production processes. The impact of feed manipulations on the product quality and consumers’ acceptance is considered. Areas deserving of future research are indicated.

1. Introduction

Globally, rainbow trout is the second most farmed salmonid, overshadowed only by Atlantic salmon. With a worldwide presence in all but a few equatorial and African nations (Figure 1), trout production stands at around a million tons annually [1], of which approximately 315,000 are larger individuals (≤2 kg) grown in seawater. This equates to a production in excess of 1.8 billion individuals a year [2] with a market value, in 2024, of US$ 4.5 billion. The species is generally cultivated in intensive monocultures using ponds, raceways, tanks, cages, net pens and recirculating aquaculture systems in various configurations. Some producers employ monosex (all female) and sterile (triploid) stocks, which decreases fish aggression and eliminates reproduction and, hence, decreases the energy being diverted away from growth [3]. Because monosex and sterile fish avoid injuries due to interactions with males, they generally express a higher overall quality at harvest and are more uniform in size. Once harvested, trout have a shelf life of 10–14 days on ice and may be sold as head-on-gutted, skin-on or skinless filets, or as cutlets/steaks. Increased awareness of the health benefits and culinary versatility of trout has resulted in growth in international trade and, associated with this, there have been shifts towards processed and value-added products. These include frozen, smoked, dried and marinated varieties, terrines, pâtés, dips and even bottled, canned and packaged ready-to-eat preparations, with and without seasonings [4,5]. Trout are also sold in the pet food market as canned flakes, pâtés, dried pellets and as gravies, while offal from primary processing may be rendered for oil, to produce protein cakes and other products [6,7,8].

Feeding trout fresh raw meat has been a general characteristic of trout culture from its emergence in the late 1800s, even through to the 1950s [9,10,11,12,13,14,15,16], although dry feeds were used sporadically [17]. The elucidation of salmonid vitamin requirements [18,19,20,21] ultimately invalidated the need for fresh liver supplements in dry feed, which led to the development of integrated pellets similar to those used today [22]. In aquaculture, feed is the most expensive input [23], representing up to 44% of the total operational cost of trout farms across the European Union [24], and even more elsewhere [25,26]. Feed is also the main contributor to nutrient discharge, and in salmonids a positive relationship exists between the feed conversion ratio/efficiency (FCR/FCE) and environmental impacts [27,28].

Until comparatively recent times trout feed manufacturers relied heavily on proteins and oils of marine origin, such as fishmeal (FM) and fish oil (FO). Reduction, or industrial fisheries, account for approximately 1000 billion individual fish [29] and the 5.5 million tons of FM produced in 2024 was worth around US$ 8 billion [30]. Employing an FCR of 1.2, temperature of 14 °C, and a 12% FM inclusion rate in feeds, trout aquaculture was responsible for at least 2.6% or 145,000 t of the global FM supply in 2024, or around 2.1% or 1.46 Mt of feed [31]. FAO [32] foresees FM production as being relatively stagnant, with even potential increases in the use of fishery by-products, until 2032.

Figure 1. Top five (black) and main producer countries (red), for the production of rainbow trout, accounting for over half (682,000 tons) of their production. Secondary producer states (teal) and countries (blue) where trout are farmed or stocked as game fish. Sand represents countries where the species is absent. Gray stars indicate the top five fishmeal producers [33]. Map generated using MapChart.net.

Others [34,35] paint a bleaker picture and predict future shortages of forage fishes. This is in line with the prediction of a continued rise in over-fishing, the exploitation of presently under-fished stocks, and climate-induced changes, which, even in the absence of fishing, will decrease marine biomass by 5% for each degree of warming [36]. In attempts to temper global fisheries’ decline, the World Trade Organization developed the Agreement on Fisheries Subsidies (AFS; [37]) that requires industrialized fisheries nations to end the high rate of subsidies which deflate the real cost of catching forage species for FM production. The AFS, however, is generally considered a “paper tiger” because contents are protective (e.g., subsidies can still be granted for fishing if stocks are considered sustainable, rebuilding, or even of unknown status; Articles 4.3 and 5.3), and enforcement and policing are problematic.

Other than impacting exploited population structures, industrial fisheries compete for the food sources of marine animals [38], while reducing the supply of fish for direct human consumption [39,40]. In addition to the damage caused to marine ecosystems [41,42,43], reduction fisheries also account for indirect mortalities through by-catch discards, slippage, and the collateral mortalities of other marine animals [44,45,46]. Nonetheless, in all likelihood, fishery subsidies will continue since they support coastal communities, existing infrastructures (e.g., landing sites and boat building facilities), and related industries. Subsidies also act to provide food security and as means of boosting export earnings; all while increasing the pressure on fisheries’ sustainability. Lately, there has been an intensification in consumers’ awareness of the environmental, ethical and social consequences of reduction fisheries and the use of FM in aquaculture [47,48,49,50]. More informed buyers now evaluate these and other issues, such as animal welfare, worker safety, and even slavery, as part of their purchasing decisions [51,52,53,54]. These values and the predicted shortfalls in FM supplies accentuate the need to diversify our protein supplies.

Not surprisingly, trout and other carnivore aquacultures have come under increasing pressure to move away from marine resource-based feeds towards alternative, more sustainable ingredients [55,56]. This has encouraged the aquafeed and production sectors to evaluate the utility of many single cell and plant proteins as partial and total replacements for FM, the ramifications of which have been previously considered [57]. Many terrestrial animal proteins have also been evaluated for their ability to supplant FM in trout feeds. These include, for example, American Periplaneta americana [58] and Turkestan Blatta lateralis [59] cockroach meals, hydrolyzed animal skin meals [60], and many others (reviews [56,61,62,63]). These proteins diversify the aquafeed industry away from FM dependency while potentially lowering its carbon footprint and strengthening its resilience against supply chain disruptions. Here, we examine the impacts of their use on the physiological control processes and production efficiency of rainbow trout.

Only literature sources that used feeds completely devoid of marine-derived ingredients were examined. This precluded, for example, many reports that incorporated ≤5% fish protein concentrates and hydrolysates, krill meals, zooplankton and others.

2. Methodology

The present review was built using various search engines, including Google and Semantic Scholar, Web of Science, Scopus and other electronic and government catalogs. The citation listings for each included paper (snowballing), back issues of relevant journals and publishers’ websites, key authors’ web pages when available, proceedings volumes, meeting abstracts and references to various existing bibliographies were also searched. No limitation was placed on language or geographical origin during the investigation.

3. Candidate Proteins

Declining FM supplies, rising prices and changing stakeholder attitudes have incentivized industry and researchers to seek more sustainable sources of protein, especially for carnivorous species. This has led to evaluations of insects, vermi meal, poultry derivatives, including feather meal and egg powder, dairy by-products such as casein, cheese waste, and fermented spin-offs, animal scraps encompassing meat and bone, hair/bristle meals, and skin and blood products. In addition, further processing steps that create protein concentrates, isolates, and hydrolyzed and fermented ingredients which express higher crude protein (CP) levels, modified essential amino acid (EAA) profiles, and better digestibility have been tested. These investigations have necessitated the evaluation, not only of biology, but also of technological suitability and safety. Protein meals are also particularly vulnerable to fraudulent activities. For example, products may be mislabeled (geographical origin and content), have erroneous documentation and experience product tampering (additions and substitutions), and/or be produced using inappropriate processing methods that may breach intellectual property rights [64]. Many animal meals are difficult to distinguish visually and are open to fraud and traceability questions. Most meals are powdered, usually varying by color, smell and taste. Although blood meal is perhaps an exception, even color is not necessarily a standard for specific meals. Colors and aromas are relatively easy to camouflage, as too are powder contents. An infamous 2008 case of the latter was an illustration of this, where melamine was added to boost milk protein which was incorporated into many products, including baby milk formula [65], resulting in problems affecting hundreds of thousands of children, and six deaths were reported [66]. Over 45 countries received contaminated products, with the levels of melamine in animal feeds being the highest (≤21 g kg⁻¹) of all the commodities examined. Generally, the doctoring of foods and feeds has a financial motivation [64] and high-cost alternative proteins act as an inducement of fraud. For example, cricket protein powder at $2800–$6425 ton⁻¹ and whey protein at $2200–$5007 ton⁻¹ versus $400–$600 ton⁻¹ for poultry by-product meal (PBM) and feather meal (FEM) places the insect meal (IM) and whey at greater risk for fraud (dilution/substitution). The development of appropriate regulations that minimize fraudulent activities thus represents an essential concern, as too does the improvement of monitoring methods to verify supply chains’ transparency and products’ authenticity.

Regarding the latter, Badillio et al. [67] examined δ¹⁵N values for fish fed PBM and determined a dietary composition of 12.7 and 4.2 for FM and PBM-based feeds respectively. After 80 d of feeding with FM feeds, the isotropic trophic discrimination was 2.0 while that for PBM −0.1 (p < 0.05), thereby illustrating the utility of the method in obtaining quantifiable estimations of the retention of different proteins based on their isotopic composition. Switching diets after 80 d to the control feed resulted in isotopic equilibrium to that of the control muscle after 15 d of refeeding. Taipale et al. [68] measured δ¹³C values to calculate the dietary origin of fry fed on marine or freshwater crustacea or fish feeds. They reported that the DHA content of fry fed the marine crustacea exceeded that of the fish feed. Campbell et al. [69] provide a comprehensive overview of the value and application of isotopic methods as tools to authenticate fish being fed on marine resource-free diets. Other than isotopic methods, the certification of the provenance of trout feeds has been examined using chemometrics, proteomics, and contemporary molecular techniques. For example, a combination of DNA barcoding with next-generation sequencing allows for the discovery of multiple species in feeds but these methods require further evaluation before their application to validate the FM-free status of salmonids.

The value of different IMs varies (Figure 2) and, depending on the source, this variation can be considerable, opening the supply chain up for fraud [70]. There is thus a need to develop methods that can distinguish between insect species for purposes of traceability and to support legislation. Belghit et al. [71] reported on the use of high-throughput tandem mass spectrometry-based proteomics as a means of discriminating between insect species. They discovered that the protein yields and amino acid (AA) profiles differed between the four species examined (black soldier fly, Hermetia illucens {BSF}, yellow mealworm, Tenebrio molitor {YMW}, lesser mealworm or darkling beetle, Alphiotobius diaperinus {LMW}, and house cricket, Acheta domesticus), with both profiles providing a clear distinction between species.

3.1. Insect Meals

Although insects have been used as food by humans for unknown millennia [72,73], the use of silkworm Bombyx mori to feed fish was a central part of the mulberry dike pond system of the Zhujiang delta over 2000 years ago [74]. The potential offered by insect larvae as an ingredient in salmonid feeds was recounted by Atkins [75] in studies with Atlantic salmon fingerlings in 1885. Fish fed bluebottle (Calliphora erythrocephalon) and green flesh fly (Lucilia cesar) larvae for 138 d returned animals that were 58% larger than fingerlings reared on meat-based feeds. Since that time, products from at least 16 species of insect have been examined as FM alternatives [76,77]. The interest that insects have garnered is evident due to the extensive number of reviews on the subject. These consider methods of insect production, their composition and safety as ingredients, and obstacles to and solutions for insect use. Mainly, however, reviews have centered on the impacts of IMs on fish performance, including their effects on growth, fish immunity and filet quality (e.g., [76,77,78,79,80,81,82,83,84,85,86,87,88,89,90]).

Many studies that have appraised the effects of replacing FM with IMs in rainbow trout feeds have employed only partial replacements (e.g., [91,92,93,94,95,96]) and this complicates their rigorous evaluation as alternative proteins since their potential negative consequences may be concealed. For example, Mushtaq et al. [97] evaluated trout fed a 50:50 FM/IM feed versus a 100% IM feed and reported a similar growth to the control (FM-fed) fish for the 50:50 mix but a significantly reduced growth for the 100% IM-fed trout (>25% growth reduction over 120 d; p < 0.05). Other examples are abundant. The variable results obtained when feeding IMs of the same species should not be too surprising since chemical evaluation and digestibility studies have uncovered major differences depending, for example, on the insect feedstock (e.g., Table 1; [98,99,100], age at harvest, and processing technology used. Likewise, the composition of insect larvae or adults can be manipulated through modifications in feedstock [101] and this might be used to produce IMs that are mimetic of FM. For example, Kovtunova et al. [102] manipulated the EAA profile of housefly (Musca domestica) maggots by rearing them on microelement-enriched substrates, while the flaxseed oil supplementation of feedstock resulted in more favorable n3–n6 ratios in house crickets, LMW and BSF meals [103]. The silencing of AA transporters, as exemplified in the Malpighian tubules of BSFL, has led to increases (p < 0.05) in His and Val [104]. Clearly, the manipulation of IM to contain specific nutritional profiles, tailored to a species’ life cycle demands, represents a viable area for future research effort.

IMs are generally prepared in powdered or flour form, and this substrate can be manipulated further to produce protein concentrates and isolates, a process which involves drying, defatting, protein solubilization, the separation of insoluble fractions, and protein precipitation and drying (reviews [105,106]). This can result in exceptional protein levels [107,108,109]. Notably, however, due to the presence of non-protein nitrogen compounds, including chitin exoskeletons, uric acid and β-alanine [101], the crude protein contents of IMs may be over-valued by 6.9–11.9% [110,111,112] and higher (20–28% [71]). As discussed, and as in [71,111], a correction of the nitrogen-to-protein factors from 6.25 to 4.2–5.4 might provide a more accurate reflection of insects’ protein levels.

As noted above, the lipid content of insect feedstocks may affect total lipid content of IMs, which can limit their dietary inclusion rates. A high lipid content may affect the flowability of the feed into processing equipment and can coat feed carbohydrates, thus reducing gelatinization and decreasing feed pellet quality. IMs are often considered to be Lys and Met limiting. Today, processed meals from eight insect species (Table 1) have been approved for aquafeed use in the European Union (Amendment of Regulation [EC] No 999/2001; Regulation [EU] 2021/1925) with the proviso that animal by-products can not be used as feedstock [112,113]. Lähteenmäki-Uutela et al. [114] and FAO [115] provide a global perspective on legislation relating to the use of insects as feed ingredients.

3.2. Annelids

A number of polychaete and oligochaete worms have been evaluated as FM replacements in trout feeds. For example, Simms [116] provided an early indication of the use of a tubificid annelid, the mud worm Tubifex rivulorum, as a trout feed with some success. The potential for using lumbricids (earthworms) to replace FM has also been examined in a variety of studies with trout [97,117,118,119,120,121,122,123,124,125]. However, when employed as a single protein source to replace FM, decreased growth generally ensues.

The production of annelids faces many of the same problems experienced by insect farmers when it comes to up-scaling [111]. These include matters surrounding culture methods, including feedstock standardization and challenges in harvesting, voiding and processing, packaging and storage. Food safety and regulatory uncertainty (both facility and products) and a lack of government support represent additional obstacles to industry scaling and sustainability. Few studies with trout have yet to consider meat quality and the organoleptic effects of annelid meals, including their impacts on fish and filets’ coloration, and limited information has been presented regarding the effect of annelid meals on general trout physiology. Nevertheless, when used as an ingredient in poultry (Gallus gallus domesticus, Coturnix coturnix) feeds, worm meals impact the intestinal microbiome, hematology, cellular immune responses, carcass dressout, breast color, juiciness, and flavor [126,127], and, given the reports of Marjanovic et al. [124], similar responses might be anticipated in rainbow trout. Further research in this area with trout is deserving of future inquiry.

3.3. Rendered Animal Meals

Rendered animal meals (see [128]) vary in terms of their protein content and digestibility and AA composition and availability. These variations can result due to the form of processing that the material receives and/or the types and quality of tissues rendered. In general, many of the nutritional issues encountered can be resolved using complementary formulations wherein a variety of products are used to offset, for example, EAA imbalances and poor palatability. There are some concerns regarding drug residues and disease-causative organisms in rendered products. The now infamous bovine spongiform encephalitis (BSE) prion outbreak that gave rise to Creutzfeldt–Jakob disease in humans in the 1980s and 1990s remains an unsettling topic that underlays legislation banning the import and use of meat and bone meals (MBM) as livestock feeds and even as fertilizer in many countries. Their use as insect feedstock is also prohibited. Drug residues also pose issues for PBM. For example, fluoroquinolones, which are recognized as critical antibacterials by the WHO, have been detected in bird feathers 15 weeks post treatment, and it has been suggested that caution should be applied before using feathers in feeds to circumvent issues with antimicrobial resistance [129]. Other potential chemical contaminants likewise cause apprehension, but legislation and control, such as those emplaced by the US FDA and EU, regulate feed hygiene and constrain the use of veterinary drugs to reduce such risks.

3.3.1. Poultry By-Products

Poultry, which include various breeds of chickens, ducks, turkeys, quails and geese, represents over 25% of global meat production. For example, the global chicken industry is estimated to produce around 173 million tons (Mt) in 2025 [130]. For geese, production is estimated to be 4.6 Mt [131], and turkeys approximately 4.8 Mt [132]. Although varying geographically and across species/breeds, around 20% of the bird carcass is considered to be non-edible weight, and parts of these leftovers (e.g., neck, frames, offal, and undeveloped eggs), aside from feathers, may be rendered, using various processes (see [61,133]) into PBM. Other than the raw material and processing methods used, the quality of PBM varies in relation to its composition, protein, and EAA availability and digestibility [134,135,136,137]. The incorporation of PBMs into aquafeeds and the assessment of their value as ingredients has been highly researched with a wide variety of species (e.g., reviews: [138,139,140,141]), including those with rainbow trout. Egg flour or powder has also been investigated as a substitute for FM in trout feeds with some success.

3.3.2. Feather/Hoof/Bristle/Hair Meals

Feathers represent around 6% of poultry body weight [141]. They contain between 85 and 87% protein, 90% of which is in the form of indigestible keratin. The protein is highly resistant to proteolysis due to the presence of α-helix and β-sheets that are cross-linked with disulfide and hydrogen bonds [142]. Accordingly, to improve digestibility, feathers are treated with heat (133 °C) under pressure (30–50 psi) in the presence of Ca(OH)₂. This process degrades keratin into smaller peptides and AAs but may destroy some EAAs [143]. The treatment of hydrolyzed feathers with keratinase enzymes can increase feathers’ crude protein content [144] and digestibility. Lys and Met are severely deficient in FEM (Table 1), perhaps partly explaining the depressed growth reported following its incorporation into trout feeds. However, the observed responses could equally reflect different processing conditions, or the impact of other dietary factors since, when incorporated as 20% CP, no effects on trout’s FI, growth, FCR, PER or survival were reported (Table 2; [145]). Tiews et al. [146] examined the prospective usefulness of bristle meal for trout but observed depressed growth.

Pfeuti and colleagues [147,148] examined the effect of extracting proteins (10–20% of diet) from FEM, comprising hog hair, chicken feathers, hooves and horns, using a pre-treatment with sodium sulfite to unfold keratin’s disulfide bonds and a protease to cleave peptide bonds, thereby producing a mixture of small peptides and AAs. They compared these treatments using two meals that differed in their chemical composition in trout feeds containing skim milk powder at 25%, blood meal (BLM) at 5% and supplemental Arg at 0.15–0.3% of the diet. The pre-treatment increased the availability of Arg from the meals and improved the digestibility of CP and AAs.

Similarly to feathers, hooves, horns, bristle and hair are high in keratin and, like feathers, can be treated using the above-noted methods to liberate small peptides and free AAs. Likewise, keratinolytic microbes that produce keratinases offer the potential to degrade keratin to produce more digestible protein. However, further research in this area of microbial biotransformation is still wanting [149]. Nevertheless, keratinase-treated pig hooves have been successfully employed as a partial FM replacer in African sharptooth catfish’s, Clarias gariepinus, juvenile feeds [150]. It is notable that Gachango et al. [151] undertook a feasibility study to examine the acceptability of bristle and hoof meals as alternative sources of protein to FM and reported a general willingness to employ such products by both the formulation and production sectors, provided prices did not exceed that of FM-based feeds.

3.3.3. Meat and Bone Meals

MBMs comprise viscera (e.g., liver, lung, and heart), tongue, brain, tails, ears and mechanically recovered frame meat. MBM constituents vary geographically based on eating traditions and cultural heritage. As with PBM, MBM quality varies with the species used and the processing methods applied. In principle, MBMs are prepared by cooking unused material, and then sieving, de-oiling, drying and grinding it into meal [61]. Differences in EAA and protein digestibility (~85%) and EAA profiles exist between MBMs, with Ile and Met being limiting. The quality of MBMs and availability of EAA is influenced by raw materials and their mix [152] and processing conditions, especially the temperature and pressure employed. For example, Lys availability decreases by <50% with increased processing temperatures [153,154]. As partial replacements for FM in trout feeds, MBMs have proven successful, especially when diets are fortified with Cys and Trp [155].

3.3.4. Blood Meals

BLM is rich in Lys and Met, and is a good source of Leu and Phe, but is low in Ile (Table 1). BLM protein quality is highly influenced by processing methods. Ring drying (steam heating) coagulates the blood, which is then centrifuged and dried prior to powdering. Due to the reduced exposure to heat, ring drying results in improved EAA availability and higher levels of Lys. BLM so produced exhibits an 87% CP content, although this may vary with the species, blood collection method and presence of contaminants. As a feed ingredient, BLM does have palatability issues, but these can be reduced with astute blending with other protein alternatives and by gradual adaptation. Ile and Met + Cys are generally considered to be limiting. Partial (50–63%) substitutions of FM with BLM in trout feeds had no effect on the growth, FCR, PER, protein digestibility, dressout, filet color, filet composition, organoleptic characteristics or survival [156,157].

Table 1. Essential amino acid composition (% protein) of alternative animal proteins compared with that of fishmeal. The maximal dietary requirements for rainbow trout for varying age/size classes and the range of crude protein content for native, hydrolyzed, and isolate and concentrate meals are also included.

CP % ³¹	Val	Trp	Thr	Phe	Met	Lys	Leu	Ile	His	Arg
52–70	1.3–5.1	0.1–1.7	1.8–5.2	1.8–3.9	0.8–1.8	2.7–7.0	3.1–16	1.2–6.2	1.3–2.5	2.5–6.8	Redworm ^13,14,34
42.8	5.4	1.4	5.4	4.5	2.6	7.2	7.9	4.8	2.5	6	White worm ¹⁵
48–90	2.8–7.0	0.4–1.0	1.7–4.4	1.4–4.2	0.9–1.7	3.2–6.4	3.8–9.8	2.0–5.3	0.7–2.9	3.7–8.8	House cricket (A) ^{1,2,3,24,27,32,33}
15–76	3.3–4.2	0.4–0.5	2.3–2.7	1.9–2.3	0.9–1.1	3.5–4.4	4.3–6.4	2.4–2.9	1.5–1.8	4.1–5.0	House cricket (N) ³⁴
43–50	2.2–9.4	0.3–0.7	1.7–2.5	2.3–2.5	1.0–1.1	1.8–4.0	3.1–4.8	1.5–2.9	1.2–1.5	3.0–4.0	Field cricket (A) ^2,12,24,30
45–56	2.9–4.2	0.3–0.8	2.6–3.6	1.8–4.0	1.0–2.0	3.0–5.1	3.8–6.7	1.9–3.7	1.5–2.2	4.6–6.2	Southern field cricket ²
40–60	1.9–5.6	0.7–4.1	0.9–4.5	1.3–6.9	2.2–4.0	5.2–7.3	2.9–7.0	1.5–4.1	2.0–3.5	3.6–6.1	Housefly (L) ^3,9,19,34
56–76	4.4–5.0	1.0–2.4	1.4–3.0	1.6–3.1	0.6–2.3	2.3–5.0	2.6–4.9	1.2–3.2	1.3–2.3	4.1–4.8	Housefly (P) ³⁴
30–65	6.6–9.0	0.5–1.5	3.7–4.4	4.6–5.2	1.5–2.3	6.0–7.4	7.2–7.9	4.7–5.1	3.0–3.2	4.8–6.3	Black soldier fly (L) ^3,4,6,30
32–57	2.4–2.8	0.5–0.7	1.5–1.7	1.6–1.9	0.7–0.9	2.3–2.6	2.8–3.1	1.7–1.9	1.2–1.4	1.9–2.0	Black soldier fly (P) ³⁴
44–60	3.3–3.6	0.5–0.6	1.9–2.0	1.5–2.1	0.7–0.9	2.5–3.1	4.0–4.7	2.4–2.5	1.6–1.8	2.4–2.9	Yellow mealworm (A) ³⁴
44–68	2.1–3.6	0.2–0.6	1.6–2.4	1.8–2.5	0.6–1.2	1.7–3.0	0.8–4.2	1.4–2.5	1.5–2.9	2.2–3.6	Yellow mealworm (L) ^7,8,12,27,29
48–62	5.1–5.8	0.2–1.5	3.9–4.3	4.6–5.2	1.6–1.9	6.2–7.1	6.1–7.3	4.0–4.6	3.8–4.0	5.0–5.4	Lesser mealworm (L) ^10,11
50–70	4.7–5.5	0.9–1.4	4.8–5.1	4.1–5.2	3.0–3.9	2.5–7.0	5.5–7.5	3.5–5.1	2.6–6.6	4.2–6.0	Silkworm pupae ^3,5
51–90	4.5–4.8	0.2	4.5–5.2	2.4–4.8	1.8–2.8	7.6–8	7.7–8.5	4.5–4.8	3.0–6.2	1.2–03.9	Whey protein ³³
51–81	2.9–4.8	0.5–0.8	2.8–4.4	2.4–3.7	0.8–2.0	3.4–6.3	4.2–6.9	2.3–3.6	1.3–2.1	4.6–7.2	Poultry by–product ^20,21,25
78–89	3.2–3.9	0.4–0.6	2.4–4.1	2.5–3.3	1.1–3.0	3.5–5.9	4.5–6.4	2.1–2.7	1.3–3.2	3.9–4.2	Spent hen meal ²⁸
75–85	2.8–7.5	0.8–4.3	2.4–4.8	2.2–4.9	0.6–0.9	1.9–2.6	3.9–8.5	2.0–4.8	0.6–1.1	5.7–6.9	Feather meal ^17,18,25,37
80–90	5.0–5.1	0.2–1.2	3.7–3.8	3.1–3.2	0.8–1.0	2.5–2.8	6.7–6.8	3.5–3.6	0.7–0.9	7.0–7.3	Hair meal ^18,21
46–71	1.3–4.2	0.2–0.8	1.2–4.7	1.1–3.6	0.4–2.1	1.7–6.1	1.8–6.9	0.8–3.7	0.5–2.3	3.1–7.6	Meat/bone meal ^21,22,37
80–90	7.8–10.4	1.2–3.9	3.4–7.1	5.8–8.2	0.5–1.3	7.5–10.7	10.9–14.8	0.6–2.5	3.8–7.5	3.9–4.9	Blood meal ^{21,23,24,25,37}
48–75	2.9–5.9	0.6–1.0	2.4–6.3	2.2–5.4	1.5–2.9	4.5–11	4.2–8.3	2.6–5.0	1.3–7.9	3.7–7.4	Fishmeal ^2,16,21,26
40–45	3.2	1.4	3.7	2.4	2.4	6.3	4.4	2.9	2.1	3.9	Trout dietary requirements ^35,36

Sources: ¹ [99]; ² [158]; ³ [84]; ⁴ [159]; ⁵ [160]; ⁶ [98]; ⁷ [161]; ⁸ [162]; ⁹ [163]; ¹⁰ [164]; ¹¹ [165]; ¹² [166]; ¹³ [167]; ¹⁴ [168]; ¹⁵ [169]; ¹⁶ [170]; ¹⁷ [171]; ¹⁸ [154]; ¹⁹ [172]; ²⁰ [173]; ²¹ [174]; ²² [175]; ²³ [176]; ²⁴ [177]; ²⁵ [178]; ²⁶ [179]; ²⁷ [99]; ²⁸ [180]; ²⁹ [181]; ³⁰ [182]; ³¹ [183]; ³² [184]; ³³ [185]; ³⁴ [186]; ³⁵ [187]; ³⁶ [188]; and ³⁷ [189].

3.3.5. Dairy By-Products

Milk products and their associated materials, such as whey, casein, dried skim milk, buttermilk and other fermented goods, have been tested as components of aquafeeds in several species of fish. Moreover, casein and skim milk have both been extensively used in experimental diets to ascertain the EAA and protein requirements of trout (e.g., [190,191,192,193]). Dried buttermilk and skim milk are relatively low in CP (~34%), whereas whey protein isolates and dried casein may contain up to 90% CP (Table 1), although differences in the EAA profiles occur depending on the product origin (cow, goat, or buffalo; [194]) and time of year. Dairy products have been evaluated for their use in different species of trout for some time [14,17,195,196] and have been assessed as both partial and complete replacements for FM in rainbow trout feeds [197,198,199,200,201,202]. Whey from milk and cheese production may be processed into protein concentrates and isolates or hydrolyzed products that increase the protein content and aid digestibility, respectively.

4. Technical Features of Animal Proteins

4.1. Composition

It has been realized for quite some time [10] that trout, as with other carnivorous species, have a requirement for specific nutrients rather than ingredients. Ideal animal protein alternatives should express a favorable AA profile, high digestibility and palatability, and low levels of fiber and starch. As reasoned by Rombenso et al. [203], it is unlikely that the future use of FM alternatives will be on an individual ingredient basis. Rather, it is more plausible that multiple ingredients will be employed—a strategy that has already provided more promising outcomes than the use of single constituents and has reduced the commercial use of FM in trout feeds [55]. This is not to undermine the importance of research on single-ingredient FM replacements. These have provided invaluable insights into the impact of such on the physiological control processes influencing fish production. The first of seven (and likely more) steps evaluating the potential of an alternative protein (or any other ingredient) is its characterization. The reader is directed to Glencross [204] for intellection of the importance and breadth of each stage of ingredient evaluation. Here, we focus only on the profile range of so-called EAAs and the CP levels of proposed alternative proteins compared to those of FM (Table 1). Other steps of the characterization process, as these relate to rainbow trout, are included within the document either as separate sections or incorporated within the text.

The data presented in Table 1 provide published ranges for EAA derived from two annelids, eight insects, and seven poultry, beef and swine-based meals. The table illustrates the broad ranges of EAA reported, which highlights the problems encountered in evaluating and characterizing raw materials in general. Indications of the limiting EAAs for different sources are, nonetheless, signaled as are the potential protein mixes to avoid such constraints. No relationship appeared to exist between the EAA content and CP levels. The wide variability apparent (Table 1) probably occurs because quantifications were undertaken in different laboratories, likely with assorted equipment, with columns of varying quality, age, use and maintenance, and assorted protocols. The origin, storage, pre- and post-mortem handling, age, sample preparation and other variables, such as the feedstocks and breeds used, likely also influence the findings (vide supra).

From Table 1 it is easy to see why FM has been a mainstay of the trout feed industry for so long, since it satisfies the dietary EAA needs for each life stage. BLM, while being rich in Lys, Leu and His, falls short for Ile and Met. PBM is an economically attractive FM substitute [205] but, depending on its source, may be limited in Lys and Met and potentially Trp. BSFL meal, on the other hand, is ~60% more expensive (Figure 2) and, depending on feedstock, may be limited in Met. There is evidence that astute combinations of alternate animal proteins can effectively achieve FM imitation as this relates to EAA profiles.

Figure 2. Cost of various alternative animal proteins (US$ per ton), methionine and lysine compared to that for fishmeal. Prices can vary greatly depending on the protein content and supply. For example, prices for whey protein concentrate (34% CP) are around US$ 2800 ton⁻¹ while that for 80%⁺ CP can exceed US$ 14,000 ton⁻¹. Kosher and halal commodities may be more expensive. Sources: [179,206,207,208,209,210,211].

4.2. Digestibility

Generally, animal proteins are considered highly digestible. The susceptibility of a protein to proteolysis, or its digestibility, is nonetheless influenced by a number of factors which may alter the rate of processing and absorption of peptides and AA along the gut. For example, the conformational structure of proteins can limit enzymes’ access to binding sites, making them resistant to hydrolysis. However, processing steps, such as cooking or fermentation, usually denature proteins, making them more enzymatically available. Digestion may be further helped (or hindered) in the gut lumen by the prevailing microbiome, which may be modified with alternative proteins (vide infra). The effect of different protein sources on the intestinal microbiome nonetheless appears inconsistent, such that if its beneficial modulation is to be contemplated then further research is required. Dietary chitin can, due to its binding to nutrients and or enzymes, hinder protein and AA digestibility, which in rainbow trout results in reduced growth and FI, and increased FCRs, while causing constipation and intestinal blockage [212,213,214,215,216,217]. Although the literature serves as a valuable source of information on the digestibility of a wide variety of alternative animal proteins applicable to rainbow trout, it is not replete. Moreover, because the digestibility of individual raw materials fluctuates, their regular appraisal should not be ignored. The gold standard for measuring digestibility is in vivo trials, but these are expensive. In efforts to reduce costs and speed up the access to results, in vitro methods, specific to trout, have been developed and evaluated for their utility [23,218,219].

4.3. Palatability

The palatability of feed is dependent upon a variety of factors including, but not necessarily limited to, feeding experience, nutrient and toxin content, taste appeal, appearance/size, hardness and aftertaste. The lack of appeal of proffered feed can lead to fish reaching satiety more rapidly on poorly palatable feeds and expressing reduced growth. Clearly, feed acceptability is complex and this is illustrated in trout by the study of [220] wherein fish refused feeds comprising spent hen meal but ate those incorporating PBM. The alternative proteins had limited differences in terms of their EAA content (cf. Table 1), and were produced, handled and fed in an identical manner to fish of the same size/strain and acclimated to similar holding conditions. Although a number of palatability issues have been encountered with alternative protein-based feeds, these have been more prevalent with plant proteins due to their abundance of antinutritional factors. Nevertheless, alternative animal proteins, as referenced above, have been reported to have acceptability issues, especially when used at higher levels of inclusion. In rainbow trout, trials in which reduced growth is experienced are generally accompanied by a decreased feed intake and poorer FCRs, responses indicative of declining palatability. Even so, there are also studies in which equivalent and superior growth, FCEs and FI are reported with alternative animal proteins (Table 2, Table 3 and Table 4). This inconsistency might be explained by the raw material quality, the effect of other feed ingredients that may not be complementary, the processing methods used, and differences in trial methodologies (length, temperatures, and strains used). Understandably, therefore, prior to use, any alternative animal protein should be rigorously evaluated for palatability, digestibility [204] and others, including the pursuing:

4.4. Pelletability

Pelleting allows for the more efficient transportation and storage of feeds while reducing spoilage and easing the on-farm feed distribution. Since the 1980s, mechanical grinding and mixing, heat, and pressure have been combined to manufacture extruded pellets. These feeds minimize nutrient loss, increase digestibility and, through increased water stability, act to reduce environmental loading (reviews [221,222]). Variations in the cooking extrusion process, such as barrel moisture and temperature, and screw configuration modify the physicochemical characteristics of feed particles. This influences the gelatinization, denaturation, and solubilization of raw materials, which alters their binding capacity and compaction and, hence, the pellet stability (air and water), production of fines, hardness and sinking velocity [223,224]. The importance of these factors is exemplified by [225], who linked poor pellet water column stability to abdominal distension syndrome in sea farmed trout.

The physicochemical characteristics of feed pellets may be further affected by the dietary proteins employed during their formulation [223,226]. For example, trout pellets’ bulk density and buoyancy are altered when FM is switched out with IM/PBM mixes [212]. Schulz and colleagues [227] reported that the addition of gelatin and PBM to a BLM-FEM mix not only improved FCR and PER but also pellet stability and fecal consistency. Furthermore, because feeds’ ingredient quality can vary between batches, this too can influence the extrusion process and quality of the final product. Disturbance in raw material supply chains and price may foster additional complexities to the process because of least-cost diet formulation, necessitating, for example, adjustments to extrusion conditions. Pennels et al. [222] provide a summary of process instability, and its potential causes and solutions.

4.5. Safety Concerns

Other than the possibility of animal feedstuffs being doctored (vide supra), alternative animal proteins present risks to fish (and hence human) health due to their contamination by chemicals (e.g., heavy metals, pesticides, and mycotoxins), allergens (e.g., bovine serum albumen) and microbiological agents (e.g., viruses, bacteria, and fungi). A general overview of potential risk is considered in Glencross et al. [204], and FAO [115] and Baiano [228] focus on the safety of IMs while others still concentrate on single hazards (e.g., mycotoxins: [229]; heavy metals: [230]). As illustrated by BSE (vide supra), the potential exists also for the transfer of prions from alternative animal protein sources (e.g., [231]) and the prion protein PrP^Sc, involved in transmissible BSE, has been detected in trout intestine 7 d following the feeding of infected tissue [232] and in the stratum compactum of everted trout intestinal preparations [233]. Antibiotic residues in PBM have been shown to cause shifts in the intestinal microbiome of cultured fish [234], and the possible transfer of antibiotic resistance genes, for example from IM, represents a growing concern [115,235]. In recent times, the tainting of animal ingredients by microplastics has become an anxiety since it has been established that livestock accumulate these particles in muscle, viscera and blood, which subsequently find their way into aquaculture feedstuffs (e.g., PBM and BLM; [236,237]). These contaminants have various physical, physiological and immune consequences if fed to trout [238,239,240].

Potential exists for the passage of allergens from feedstuffs up the food chain, and this has been demonstrated with feed spiked with the herring worm (Anisakis simplex), invoking an allergic response in a sensitized individual [241]. Since anaphylactic shock has been reported following ingestion of mealworm, superworm, locusts, grasshoppers and silkworm pupae, their use in feeds represent possible safety risks for consumers. This area, together with the transfer of other feed contaminants, such as pharmaceuticals, through the food chain, is a distinctly fertile ground for future research.

4.6. Ingredient Costs

Figure 2 summarizes the cost, in US$ per metric ton, of various alternative terrestrial/aerial animal proteins compared with that of prime FM. The latter has high quality standards in relation to raw material freshness, and is generally higher in protein (≥67% CP) content than standard FMs. It mostly expresses superior digestibility, optimal EAA, vitamin and mineral profiles, low biogenic amine levels and good palatability. Most FMs are fully traceable and processed at low temperature with adherence to HACCP quality assurance programs. A conspicuous feature of some unconventional proteins is the notoriously difficult nature of obtaining accurate pricing from producers–suppliers. Costs, especially those for earthworm and insect meals, have declined over the last 5 years because of scaling effects. While this has generally occurred due to the entry of new players, it is nonetheless fair to state that some pioneers have experienced expansion difficulties and even closure due to competition against cheaper imports. Other than differing according to the geography of their production and market dynamics, prices also diverge in relation to product type and CP content, as exemplified by whey protein powders and concentrates (Figure 2). Global distinctions in labor and energy costs, transportation considerations, and even tariffs each influence the cost of production and ultimately the market value. Prices for other feed ingredients such as PBM, MBM, FEM, BLM and FM are widely available. Mostly, the price per ton of processed animal meals is <50% that of FM, even though crude protein levels show equivalence (Figure 2). However, imbalances in one or more EAAs, relative to FM, are seen with some (Table 1), as too is digestibility, which depends on the raw material quality, processing methods employed, feed production, and storage characteristics, inter alia (e.g., [220,242,243]).

Because there are time-related and geographical differences in the prices of alternative proteins, cost comparisons between them and FM, on a global basis, are challenging. Accordingly, the following reports present the differences in ingredient costs to allow for price differentiation between mixed animal protein and FM-based feeds on a local basis. Examining the replacement of FM with mainly PBM, Alexis et al. [244] reported a 37% reduction in the cost of producing a kilogram (kg) of trout. Similar cost savings were reported by Bilgüven [245] and Pokorný [246] when replacing FM with a PBM and MBM mix, while [247] replaced dietary FM with a mix of BLM and FEM and calculated a 7% saving with no differences in trout performance characteristics. In the latter instance, the comparatively low level of saving reflected the fact that the control formulation was a reduced FM feed (7.5%), and this too was seen in the cost of producing a kg of fish (88¢ for the FM fed trout versus 86¢). Tiews et al. [248] reported an 8% reduction in the price per ton⁻¹ of PBM but a 44% reduction for hydrolyzed FEM, with fish performing equally to trout receiving FM-based feeds.

Dried silkworm was first applied as a feed in trout hatcheries during the early part of the 20th century [249], and although good growth was attained, its price, at 9¢ lb⁻¹, was higher than beef (7.5¢ lb⁻¹), and exorbitant compared to FM (¾¢ lb⁻¹) [Great Depression prices]. In an interesting series of more recent publications from Nepal, however, Roy et al. [250] reported an 8.2% and 3.6% savings on the cost of trout diets in which shrimp meal was substituted by silkworm moth and pupae respectively. Gurung et al. [251] calculated a 60% saving in trout feed costs for diets based on silkworm pupae meal with no difference in gross margins when compared against trout fed shrimp meal-based feeds. Bhagat and Barat [252] calculated even greater savings, determining a 75–62% feed price reduction when replacing shrimp meal with silkworm moths and pupae respectively. The latter cost savings with silkworm may be reflective of a growing local sericulture industry, whereas shrimp meal is imported.

A 14% decrease in trout feed cost was calculated following replacement of FM with a Hermetia/Tenebrio meal [253], whereas [254] calculated an 11.4% increase in feed costs with the addition of IM, but a 9.15%⁺ saving when FM was substituted by mixtures of poultry products and hemoglobin (Hgb) meal. Turek et al. [255] divulged that the cost of adult house crickets and superworm larvae Zophobas morio (a beetle of the family Tenebrionidae) were 25- and 8-fold more costly per MJ energy, respectively, when compared to commercial feed pellets. A mixed diet comprising a meat meal (MM) and IM was 58% more kg⁻¹ when compared against an FM feed [256] that, as might be anticipated, negatively impacted economic conversion and profit indices. While recognized as a sustainable and circular solution for protein production, and although there exists one or two geographically isolated exceptions, evaluations of the cost effectiveness of replacing marine proteins with IM in aquafeeds have been generally negative [257,258]. This is generally due to problems encountered with scaling, energy consumption, regulatory issues and safety. The heightened cost associated with IMs has led to their being touted as possessing qualities in addition to being alternative, more sustainable protein sources (e.g., immunostimulant and probiotic effects). The preceding aside, however, rainbow trout reared on IM-containing feeds have been sold in Europe since 2018.

Knight [259] reported that the cost of a skim milk-based feed was only 43% (C 11.5¢ vs. C 26.5¢ kg⁻¹) that of the standard hatchery feed of the time (fresh beef heart and liver and pork liver in equal parts). However, because the growth performance of fish fed the experimental feed was so poor, the cost of production of trout was >140% higher kg⁻¹. Using various slaughterhouse wastes (BLM, PBM, and MBM) [260] determined that FM substitution resulted in significant (p < 0.01) beneficial differences in production profits.

5. Effects of Dietary FM Replacement on Rainbow Trout

5.1. Growth

The responses of rainbow trout (hatch-264 g) to the complete removal and supplanting of FM from feeds using various IM-based feeds of generally similar protein content is summarized in Table 2. In the thirty-four studies presented, five species of insect were evaluated, with 41.2% reporting decreased weight gain, 52.9% no effect, and only two (5.9%) describing increased growth. Superior growth, relative to that of controls fed a shrimp meal-based feed, was recorded in trout receiving silkworm pupae meal. A third of the trials with Tenebrio molitor (YMW) registered poorer growth than controls, whereas 9 of 15 (60%) had a lower growth when fed BSF preparations. In general, trials that recorded growth equivalence to control diets were attended by similar responses for FI, SGR and FCR. In trials where poorer growth was registered, this was accompanied by increased FCR and decreased FI. Reduced growth was most often seen in fish of ≤65 g. Roy et al. [250] replaced shrimp meal with either silkworm pupae or adult moth and, at the trial’s end, fish fed the pupae diet were larger than control trout < moth-fed animals. No differences (p > 0.05) were observed in FCRs between the pupae and control diets, both of which outperformed (p < 0.05) the moth-based feed. However, survival was better (p < 0.05) for the control group. Similarly, Ref. [251] reported that the complete replacement of shrimp meal with silkworm pupae meal had no effect on fish weight gain but differences (p < 0.05) in survival resulted in overall reductions in group weight gain and increased FCRs. Likewise, Ref. [261] exchanged shrimp meal with BSFL meal and, while reporting no differences in weight gain or SGR (Table 2), witnessed decreased (p < 0.05) PER and increased (p < 0.05) FCR and mortality of the BSFL-fed fish. Overall, the results with trout fed IMs are compatible with the meta-analysis of [83], which considered the impact of 17 insect preparations on 40 species of marine and freshwater fishes. It is noteworthy that the meta-analysis did not appraise 100% FM replacements. Tran and colleagues [83] spotlighted silkworm pupae meal and defatted YMW as being of particular interest, while also calling attention to limiting EAAs in IMs. Imbalances and constraints with the latter (see Table 1), especially for Lys and Met, may partly explain the variability in the growth response of trout.

Table 3 summarizes the results with respect to trout fed diets consisting of PBM as the main source of their dietary protein. Of the 52 trials collated, only 3 (5.7%) record superior growth to trout fed with FM-based feeds. Twenty-seven (51.9%) describe reduced growth, with the remainder (42.4%) showing growth equivalence. As for the response of fish to IMs, poorer weight gain with PBM feeds is associated with inferior FI and SGRs (Table 3). These findings are at odds with the meta-analysis of [140]. Variation in results for fish fed predominantly PBM is not to be unexpected since assorted processing methods are employed [137], leading to differences in CP and EAA profiles, digestibility and AA availability. Indeed, the chemical evaluation of a variety of PBMs from different manufacturers have exposed major differences in protein (55–73%), lipid (10–19%), and ash (11–23%) contents [262]. While control and experimental feeds in the individual trials generally expressed similar CP content, there were differences between studies. More than two-thirds employed PBM in combination with other animal protein sources and, of those where PBM was the sole animal protein source, seven resulted in decreased growth and four in growth equivalence to the control groups (Table 3). This mediocre performance has generally been attributed to deficiencies in Lys and Met ([263,264]; Table 1). Dong et al. [262] also revealed that Phe was a secondary factor limiting AA in PBM.

Using both in vitro (TP-stat) and in vivo methods, differences have also been disclosed in terms of protein and AA digestibility between some PBM samples [136,137,262], further explaining variations in trout response to complete FM replacement. When other proteins are mixed with PBM, performance can improve. Thus, Schulz and colleagues [265] used trout of 23 g fed a 50:50 blood/feather meal for 70 d, which yielded an average FCR of 1.62 and PER of 1.24 versus the FCR of 0.86 and PER of 2.33 in the controls. Using an equal combination of blood–feather–poultry meal, however, superior responses, with no differences in performance, compared to a control feed, were attained. The authors [227] considered this be the result of changes in the gross amino acid content and profile.

The growth response of trout following the complete replacement of FM by a miscellany of proteins is given in Table 4. As with other ingredients (Table 2 and Table 3), contrasting outcomes occur due to differences in raw material quality and processing modifying protein AA digestibility. For example, this has been recorded for BLM and MBM [154,266]. In trout, Ref. [267] determined the digestibility of CP for MM and MBM to be 91% and 78% respectively, contrasting to white (trimmings and offal of white-fleshed fish) and brown (whole oily forage species) FM (92% and 90% respectively), which also expressed enhanced feed efficiency and PER. The authors suggested that these results reflected the variation in the AA composition between proteins. However, due to the use of trout of varying size/age groups between FM (30–50 g) and animal proteins (3.5–4.0 g), as well as the variable CP content of feeds, this conclusion is not readily defensible. Indeed, the total replacement of dietary FM with MBM had no impact on animal performance [268] and mixtures of MBM and dried skim milk proved suitable for the rearing of rainbow trout fry [199]. The potential for applying skim milk (35%) and liver (10%) to raising trout fry was also studied by [269] who compared this diet against fish grown using liver alone over 60 d. They found that the control fish gained 55% more weight than fish fed the liver dry feed. Takeuchi and colleagues [190,191] also employed the milk protein casein (0–54%) to determine optimum dietary protein-to-lipid ratios in rainbow trout fry, but [270] indicated that the total replacement of FM by casein decreased the growth and FCE of trout which, they surmised, may have been due to inadequate EAA availability or lack of lipid in the feed.

Table 2. Example responses of rainbow trout of various sizes, reared at temperatures ranging between 11 and 21 °C for 28–154 d, to the complete substitution of shrimp and FM with insect products. H = Hermetia illucens; T = Tenibrio molitor; A = Acheta domestica; Z = Zophobas Morio; and S = Bombyx mori. La = live adults; p = pupae; and a = adults. Complimentary animal protein sources incorporated into the feeds included meat meal = MM, poultry by-product meal = PBM feather meal = FEM, and blood meal = BLM. ↑/↓ indicates different (p < 0.05) from controls, ↔ indicates equivalence (p > 0.05).

Reference	Response			S	Z	A	T	H	Days	~°C	wt (g)
[271]	↓ wt gain, length							40	90	17.1	5
[272]	↓ wt gain, length							40	90	17.1	5
[273]	↓ wt gain, SGR, FCR						20				10
[274]	↓ wt gain, SGR, FI; ↔ FCR, S							30	90	14.1	34.2
[274]	↓ wt gain, SGR, FI, FCR; ↔ S						30		90	14.1	34.2
[255]	↔ wt gain, S, FCR; ↓ PER					La			60	14.3	264.3
	↔ wt gain, S, FCR, PER				La
	↔ wt gain, S, FCR, PER				50%	50%
[256]	↓ wt gain, SGR, FCR; ↔ PER, FI, S	8 MM						27.5	150	11	67
[275]	↓ wt gain, SGR, ↑ FCR							40	90	17.1	5
[276]	↔ wt gain; ↑ FCR							15	84	17	48.9
[250]	↔ wt gain, SGR, FCR							50 p	77		0.3
[250]	↓ wt gain, SGR, ↑ FCR							50 a	77		0.3
[277]	↓ wt gain						24		84		47.2
[215]	↓ wt gain, FI, SGR; ↑ FCR							pre-p	90	17.1	5.2
[124]	↔ wt gain, SGR, FCR, FER, S	15 PBM					44.3		90	20.9	15
[124]	↔ wt gain, SGR, FCR, FER, S	4 BLM					44.3		90	20.9	15
[261]	↔ wt gain, SGR; ↓ PER, S; ↑ FCR							50	90	19.5	5.4
[278]	↔ wt gain, SGR, FCR, S							19.5	56	14	68.3
[254]	↔ wt gain, SGR, FCR, FI, S	11.4 PBM	8 BLM				10		56	15.9	875
[254]	↔ wt gain, SGR, FCR, FER, S	6.5 FEM	8 BLM				10		56	15.9	875
[279]	↔ wt gain, SGR, FCR, FI, PER						40		90	15	23
[251]	↔ wt gain, SGR, S; ↓ FCR							48	90	16.9	0.24
[212]	↓ wt gain; ↑ FCR; ↔ S	20 PBM						26.4	84	13.9	45.7
[280]	↔ wt gain, FCR, PER, FI							40	27	16.9
[281]	↔ wt gain, SGR, FCR, PER							20	56	15.5	133.1
[282]	↔ wt gain, SGR, FCR, PER							20	56	15.5	133.1
[283]	↑ wt gain, SGR; ↔ FCR			50 p					56		0.32
[283]	↓ wt gain, SGR; ↑ FCR			50 a					56		0.32
[284]	↔ wt gain, SGR, FCR, PER, FI						20		154	13	78.3
[213]
[285]
[286]	↔ wt gain, FCR, S, SGR, PER							32	133	13	112.9
[252]	↑ wt gain, FI, SGR, PER, ↓ FCR			45.3 p					150	13	0.1
[252]	↓ wt gain, FI, SGR, PER, ↑ FCR			44.9 a					150	13	0.1
[287]	↔ wt gain, SGR, S							60	28	12.3	0.4
[253]	↓ wt gain, SGR; ↑ FCE						47		60	12	65

Abbreviations: FCR = feed conversion ratio; FER = feed efficiency ratio; FI = feed intake; S = survival; PER = protein efficiency ratio; and SGR = specific growth rate.

Table 3. Example responses of rainbow trout of various sizes, reared at temperatures ranging between 10.5 and 20.5 °C for 56–197 d, to the complete substitution of FM with poultry by-products (PBM). ↑/↓ indicates different (p < 0.05) from controls, ↔ indicates equivalence (p > 0.05). Complimentary animal proteins included meat meal = MM, feather meal = FEM, blood meal = BLM, and meat and bone meal = MBM.

Reference	Response	MBM	BLM	MM	FEM	PBM	Days	~°C	wt (g)
[288]	↓ wt gain, FE; ↔ S			10		50	84	12	0.2
[263]	↓ wt gain, SGR; ↔ PER, PPV				54		72	11	16.7
[92]	↔ wt gain, PRE, S; ↑ FCR					63.8	56	15	0.5
[289]	↔ wt gain, PER, FCR, FI, S; ↓ LPV			10	10	22	72	14	30.3
[145]	↔ FI, wt gain, S, FCR, PER		4.6		20	12	56	18	104
	↔ FI, wt gain, S, FCR, PER		4.5		19	12
	↔ FI, S, FCR, PER, ↓wt gain		4.6		17.5	12
	↔ FI, wt gain, S, FCR, PER		4.2		16.4	12
	↔ FI, wt gain, S, FCR, PER		4.3		14.8	12
	↓ FI; ↔ wt gain, S, FCR, PER		5		16	12
[290]	↔ wt gain, SGR, FI, S		5	20		40	120	10.5	122.5
[291]	↔ wt gain, FCR, FI, S					59	80	14	1.4
[292]	↓ FCR; ↑SGR; ↔ wt gain					40.24	90	14.5	150
[293]	↔ wt gain, SGR, FI, S; ↓ PER; ↑ FCR			14	8	34	98	14.1	16.7
[293]	↔ wt gain, SGR, PER, S, ↑ FCR			9	5	21	98	14.1	16.7
[294]	↓ wt gain, SGR, FI; ↔ FCR, S			9	7	42	70	14.5	20.5
	↓ wt gain, SGR, FI; ↔ S; ↓ FCR			9	7	28
	↓ wt gain, SGR, FI; ↔ S; ↓ FCR			9	7	21
[294]	↓ wt gain, SGR, FI; ↔ FCR, S			9	9	27	84	14.5	23.6
	↓ wt gain, SGR, FI; ↔ S; ↓ FCR			9	9	31.5
	↓ wt gain, SGR, FI; ↔ S; ↓ FCR			4.5	4.5	36
	↓ wt gain, SGR, FI; ↔ S; ↓ FCR				4.5	40.5
[294]	↔ wt gain, SGR, S, FI; ↑ FCR; ↓ PER		14		8	34	84	14.1	16.7
[295]	↔ wt gain	4.8	4.8		4.8	4.8	120	11	783
[296]	↓ wt gain, SGR, PPV; ↔ FI S; ↓ FCR					60.7	112	15.4	28.8
[296]	↓ wt gain, SGR, PPV; ↔ FI S; ↓ FCR					60.7	112	20.2	28.8
[296]	↓ wt gain, SGR, FI; ↔ S					60	56	15	1.5
[296]	↓ wt gain, SGR, FI; ↔ S					60 + LH	56	15	1.5
[264]	↓ wt gain, SGR, PER; ↑ FCR					45	60	14.5	50
[254]	↓ wt gain, SGR; ↔ FCR; S		8		18	7.9	56	15.9	875
	↓ wt gain, SGR; ↔ FCR S		8		13.1	13.5
	↔ wt gain, SGR, FCR, FI, S		8		6.5	1.4
[297]	↓ wt gain, SGR, PER; ↑ FCR ↔ FI					50	56	14.5	15
[297]	↓ wt gain, SGR, PER; FI; ↑ FCR			6		32	56	14.5	15
[298]	↑ wt gain, SGR; ↔ FI, FCR, PER, S				70.2		156	20.2	35
[299]	↔ wt gain, FCR, FI, FC, PRE, ERE			5	5	27	84		71.9
[300]	↓ wt gain, SGR; ↑ FI.			1	6	10	84	17	378
[301]	↓ PER; ↑ FCE ↔ wt gain		10			24.2	84	15	34
[302]	↔ wt gain, FI, SGR, FCR			5	5	27	182	15	0.2
[302]	↔ wt gain, FI, SGR, FCR			3	3	25	182	15	0.2
[303]	↓ wt gain, FI; ↑ FCR; ↔ S		9.1			14.3	84	14.5	19.5
[303]	↓ wt gain, FI; ↑ FCR; ↔ S		12			23.4	84	14.5	19.5
[304]	↔ wt gain, FI, SGR, FCR		5			56	56	15.3	15
[245]	↓ wt gain, FI, PER; ↑	5				36	70	~13.2	50.6
[305]	↑ wt gain, SGR; ↔ FCR; ↓PER					59	140	18	4.1
[67]	↔ wt gain, FCR, S; ↑ SGR; ↓PER					59	80	14	1.4
[306]	↓ wt gain, SGR, FER, PER; ↑ FCR					53	70	10.5	29
[244]	↔ wt gain, S, FC, PRE		1.4			30	197	12	1.3
[244]	↑ wt gain, FC, PRE; ↔ S		1			35	197	12	1.3
[307]	↓ wt gain		1.4			30	197	12	20
[307]	↔ wt gain		1			35	197	12	20

Table 4. Example responses of rainbow trout of various sizes, reared at temperatures ranging between 11 and 21 °C for 28–98 d, to the complete substitution of FM with miscellaneous animal proteins. Complimentary animal protein sources incorporated into the feeds included poultry by-product meal = PBM feather meal = FEM. ↑/↓ indicates different (p < 0.05) from controls, ↔ indicates equivalence (p > 0.05). A = alpaca; BLM = blood meal; C = milk products; D = Dendrodrilus subrubicundus; E = Eisenia foetida; EF = egg flour; Ea = live Enchytraeus albidus; L = Lumbricus terrestis; MM = meat meal; MP = milk products; N = Eudrilus eugenige; O = oligochetes; S = sheep; and SH = skin hydrolysates.

Reference	Response	MP	MM	BLM	O	SH	MBM	C	Days	~°C	wt (g)
[60]	↔ wt gain, FI, FCR					29.6 A			40	11.5	60
[60]	↔ wt gain, FI, FCR					29.6 S			40	11.5	60
[298]	↓ wt gain, SGR, FI; ↑ FCR						71.5		91	9.3	36.4
[125]	↑ wt; ↔ S				Ea				43	10.5	0.15
[117]	↓ wt gain; ↑ FCR				48 N				84	15.5	128
[198]	↔ wt gain, SGR, FCR							35.1	126	19.3	50.5
[308]	↓ wt gain, SGR, PER; ↑ FCR, FI, S							55 EF	90	12.9	0.38
[259]	↓ wt gain; ↑ FI, FCR	50	25						35	18.5	0.7
[293]	↓ wt gain, FI, SGR; ↑ FCR		42	9					84	14.5	20.6
[124]	↔ wt gain, FI, SGR, FCR				34					20.9	15
[269]	↓ wt gain	35	10						60
[97]	↓ wt gain, SGR, FI; ↑ FCR				45.2				120		7.5
[119]	↓ wt gain, SGR, FI, PER; ↑ FCR				71 D				50	16	17
[118]	↔ wt gain, FI, SGR, FCR	50 A				70				7.5	31
	↔ wt gain, FI, SGR, FCR	56 L
	↓ wt gain, FI, SGR, PER; ↑ FCR	59 E
	↓ wt gain, FI, SGR, PER; ↑ FCR	59 E
[256]	↓ wt gain, SGR, PER; ↔ FI; ↑ FCR		27.5						150	11	67.2
[146]	↓ wt gain; ↑ FCR	10.7
[309]	↔ wt gain, FI, FE						19.5		60	16.8	19
[310]	↔ wt gain, SGR, FCR		4.76			98		4.76		10	1.9
[310]	↔ wt gain; ↓ SGR, FCR		9.52			98		9.52			1.9

The replacement of FM using earthworm-based meals has been reported to increase [125], decrease [119] and have no effect [118,124] on trout growth. Stafford [311] reported differences in weight gain for trout fed exclusively on redworm Eisenia foetida when compared with fish fed Allolobophora longa or Lumbricus terrestris (Table 1). She suggested that the poorer growth of fish fed redworm likely resulted due to it ejecting a foul-smelling fluid which reduced its palatability and thus the feed intake. Additionally, reduced growth may have reflected the presence of coelomic hemolytic factors [312]. Indeed, Kobayashi et al. [313] describe a lysenin–sphingomyelin complex in the coelomic fluid of E. fetida that was lethal to 11 species of fish within 120 min of exposure. The application of raw red wrigglers, Dendrodrilus subrubicundus, or night crawlers, Dendrobaena veneta, as feeds for over 60 d returned trout of similar weight to fish fed a commercial diet (Table 1; [311]). Annelids possess crude protein levels of 54–71% [314], being more than competitive against IMs, and with a credible EAA profile when compared against FM (Table 1). As with insects (vide supra), protein and fat content can be manipulated using different feedstocks [315], although more research is needed in this area. However, earthworms bioaccumulate heavy metals [316,317], and Cu, Fe, Pb and Zn concentrated in trout tissues fed Dendrodrilus subrubicundus meal within 50 d (p < 0.05; [119]). The potential exists for the carryover of microbes and a variety of volatile compounds from earthworms to feed even when freeze dried [318]. Metal and other contaminant accumulation is clearly feedstock dependent such that these issues might be prevented with the use of uncorrupt raw materials, as exemplified by food-grade discards.

Although not differing in terms of their measured productive parameters, trout fed diets of hydrolyzed sheep or alpaca skins as replacements for FM nevertheless returned poorer (p < 0.01) apparent digestibility for protein and fat [60].

5.2. Morphology and Histology

Potentially, differences in the growth response due to the application of alternative proteins might impact the body conformation of trout. Body shape is an established quality characteristic in salmonids [319], as it can influence esthetic appeal to consumers, with well-formed animals implying good health and sustainable methods of culture. Moreover, lower K values in trout have been associated with increased filet yields, cutlet area and fattiness [320], the latter of which may influence organoleptic identity. Indeed, when fish were fed on a 50:50 mix of live adult house cricket and superworm Zophobas morio larvae, adult trout returned condition factors (K = (W/L³) × 1000) that were higher (p < 0.05) than fish fed commercial pellets [255]. On the other hand, feeding fish BSF [286], YMW larva meals [285], PBM [296], egg flour [308] or mixed protein meals [145,299] did not affect K, and a decline (p < 0.05) in K was recognized following FM replacement with a mix of PBM/FEM [263] or live white worms [125]. Whether these contrasting responses reflect the proteins employed, length of trial, dissimilar trout strains, different size/ages of experimental animals, husbandry, or a combination of these and/or other factors is difficult to discern. Nevertheless, the importance of how substitute proteins may modify fish conformation should not be underestimated. Interestingly, filet yields are unaffected in trout fed BSF meal [286], PBM [292,307] and a mixed diet [299]. External anal lesions and rupturing were observed in trout fed dried BSF pupae meal—a condition that led to Aeromonas hydrophila infection. The authors [215] suggested that the rupturing may have been caused by the accumulation of chitin particles, thereby explaining decreased FI and growth. Finally, Ref. [321] examined the response of two different populations of trout fed BSF meal, and discovered increased damage to the dorsal and pectoral fins in one of the groups.

Together, the viscerosomatic index (VSI) and hepatosomatic index (HSI) provide an indication of energy reserves and, hence, a rough estimation of an animal’s nutritional well-being. A high VSI is often associated with elevated dietary lipid accumulations and this may indicate a need to modify formulations. Most studies with poultry-based (e.g., [244,299,300]), insect (e.g., [255,284,286]) and mixed IM/MM (e.g., [256]) replacement of FM, however, report a null effect on VSI. Nonetheless, the replacement of FM with PBM resulted in declining (p < 0.05) VSI in one study [244] and increases in others [263,304]. High HSIs are generally attendant with poorer growth in fish, and glycogenic hepatomegaly is often affiliated with the expansion of hepatocytes due to the excessive accumulation of glycogen, the presence of large vacuoles (hepatic steatosis or fatty liver), vascular swelling, and the deposition of extra-hepatic cells—conditions that may be due to a disturbance in fatty acid metabolism [322]. In accordance with poorer growth being accompanied by hepatomegaly, Ref. [263] observed an almost 50% increase in the HSI in trout fed a diet comprising a mix of PBM and FEM. Studies with feeds incorporating BSFL/PBM [212], YMW larvae meal [284], and various species of earthworm [311] report similar findings, and [323] observed hepatomegaly attended with abnormal nuclei, bile duct proliferation, and damage to parenchymal cells following 126 d feeding with a casein-gelatin diet. Chemello and co-workers [284] suggested that the hepatomegaly associated with feeding YMW larvae meal potentially indicated disorders in glucose and lipid metabolism, but the authors failed to detect any disturbance in hepatic lipogenic or amino acid catabolic activities. Others have measured no effect of feeding alternative animal proteins on HSI. These include investigations with BSF meal [286] following feeding with live house crickets and/or superworms [255], with darkling beetle larvae meal [279], with poultry-based diets [264,300,307], and with mixed protein meals [145,299]. In contrast to the preceding, however, [124] reported a decreased HSI after feeding trout with earthworm (Eisenia foetida)- and mealworm-based feeds, while [256] recorded lower values (p < 0.05) for HSI in trout fed an IM–pork viscera meal and Moghaddam et al. [292] recorded lower values in fish fed PBM. The histological examination of the liver in the latter study revealed a reduced hepatocyte diameter and, correlating with this, smaller hepatic nuclei, suggesting karyopyknosis, which generally signals the irreversible onset of apoptosis. The microscopic evaluation of the liver of steelhead trout fed with PBM-BLM-based feeds revealed decreased hepatocyte vacuolization [288], which the authors considered might reflect a divergence in crude fat digestibility between the FM and PBM-BLM feeds. However, in other studies, no differences in hepatic architecture were described for trout fed a PBM-based feed [296] or 50:50 mixes of PBM and BLM [265].

The replacement of FM by PBM-BLM caused mild hypertrophy of the kidney and hyperplasia of the nephron tubular epithelia in steelhead trout [288], while FM’s substitution with defatted mealworm [279] caused renal tubules to be replaced by a mineralized amorphous material which led to a higher pathological score (p < 0.001). However, the latter did not negatively impact gill or renal functionality as suggested by the lack of changes in blood gases, the acid–base balance or electrolyte levels, except for Na⁺ [279]. More obvious changes in architecture with FM replacement have been visualized in the trout gut.

Alternative animal proteins have been reported to affect the architectural integrity of all parts of the trout gastrointestinal tract (GIT). For example, the anterior intestinal fold height increases in trout fed with poultry products [324,325], and this is also the case when IMs substitute FM [213,274,278,324]. However, some studies [286,300] have failed to recognize any changes, including those in which mixed animal protein sources [254], BSF [279], and YMW [274] were deployed. Dumas et al. [212] reported that PBM/BSF larvae meal decreased (p < 0.05) the length of the anterior intestine, but not the width, while [321] found that a BSF meal thickened the foregut, which also expressed a dull whitish coloration. However, Refs. [254,325] revealed that the replacement of FM with mixtures of animal proteins had no effect on lamina propria thickness in any part of the GIT. Tefal et al. [256] found that a mix of pork viscera/IM feed increased the submucous layer in the proximal intestine and the serous layer in the distal intestinal segments (p < 0.05), while [325], using an alternative protein mix, saw an increased submucosal width in the posterior gut (p < 0.0001).

Enterocyte dimensions and cell infiltration along the intestine’s entirety did not differ when fish were fed mixed alternative protein feeds [254]. However, increased goblet cell abundance has been observed in the anterior gut of trout fed PBM and IM [296,324], and this observation was confirmed by the significant increases in mucin synthesis and the increased goblet cell numbers in both the distal and proximate intestine of trout fed BSF prepupae meal [271]. Increased goblet cell numbers, accompanied by augmented mucus production, is indicative of inflammation. Despite that, Ref. [286] did not record any differences in the inflammatory responses in the gut, liver and spleen of fish fed BSF meal, which Miebach et al. [321] discussed in relation to the possibility of BSF meal dampening GIT inflammatory responses. Indeed, chitin has been demonstrated to possess immunological benefits [94,275] and may adjust or modify the severity of inflammatory irritations.

Trout maintained in seawater and fed a feed comprising mainly poultry meal exhibited increased vacuolization of pyloric caeca apical enterocytes as well as increased abundance in relation to goblet cell numbers [288]. Miebach and associates [321] likewise report increased vacuolization in the lamina epithelialis mucosae of fish nourished with BSF meal. As suggested by Matulić et al. [326], it is possible that alternative protein-driven modifications to the trout liver and GIT may offer prospective biomarkers to predict the practicality and adequacy of specific ingredient mixes prior to widespread adoption. Production length studies to evaluate ultimate responses would nonetheless be needed to establish the validity of such a method.

5.3. Gut Physiology and Microbiome

Not surprisingly, changes in morphology and histology are often associated with alterations to trout physiology. For example, Ref. [256] measured lower trypsin and chymotrypsin levels in the pyloric cecum (p < 0.05) of trout following being feed a diet comprising pork viscera and IM. Taken together, the reduced protease activity, changes in hepatic and intestinal architecture, and decreased protein and lipid retention efficiencies of pork–IMh-fed trout provide explanation for their poorer growth and FCR (Table 1). Jalili et al. [297] examined alkaline protease, lipase, and amylase activity in the pyloric cecum in fish reared either on a PBM or PBM-BLM feed but found no differences in activity when compared against controls.

The fish gut hosts a complex microbiome composed of resident and transient microbes that support digestion, nutrient production, immune function, and gut barrier integrity [327]. A stable core microbiome develops early, diversifies after first feeding, and continues to change with age and nutrition. Different intestinal segments harbor distinct microbial communities, with microbial density increasing from the proximal to distal gut. Changes to gut microbial population structures and abundance can alter apparent nutrient digestibility via the excretion of enzymes that contribute to digestion [328,329]. Although there have been a reasonable number of studies of dietary-driven changes in the gut microbiome of fish, especially those that consider alternative plant proteins [57], studies on the impact of animal proteins supplanting FM have, for whatever reason, focused mainly on Ims, and few publications exist for other animal protein sources.

To achieve the potential for manipulating the gut microbiome for production benefit, in its broadest sense, in the future, a wider research net needs to be cast. This could include developing a deeper understanding of those mechanisms that align the gut microbiota to enhance FE, and which optimize health and overall production efficiency. This will require production-length studies to ascertain how the gut’s microbiota is regulated with feed, age, rearing conditions, and genetic background. This is needed to develop effective management strategies, avoid dysbiosis and better understand how the microbial ecology of the GIT impacts the physical integrity of the gut and its secretions. Syn-, pre-, pro-, para- and post-biotics all provide potential benefits (i.e., short-chain fatty acids, enzymes and cell fragments, and immunomodulatory and anti-inflammatories), and expose the rewards that might be anticipated with a thorough familiarity of the functionality of the gut’s microbial consortia and species therein, and how these interplay with feed formulations and ingredients.

A meta-analysis of trout fed BSF meal at different dietary levels and ages indicated that Actinobacteria and Firmicutes abundance was heightened mainly due to the increased presence of Actinomyces, Bacillus, Enterococcus and Lactobacillus [330]. Similar responses in biodiversity were measured by [275], especially for Firmicutes, Actinobacteria and Proteobacteria taxa, with the replacement of FM with BSF meal, which increased the abundance of Cetobacterium sp. and Achromobacter sp. Nonetheless, in a study by Biasato et al. [286] the gut exhibited differences in relation to the relative abundance of bacterial genera, particularly for Staphylococcus, Enterococcus, Actinomyces and Oceanobacillus, which were more copious in the posterior gut segment of fish fed BSF meal. A concern regarding the presence of Oceanobacillus was that these are more regularly associated with marine crustacea and mollusks, thereby suggesting a potential for the tainting of BSF feedstock. Feeding a diet with YMW meal to trout, Terova et al. [285] observed a reduction in the number of taxa assigned to the Ruminococcaceae and Neisseriaceae (p < 0.03). Others (e.g., [94,275]) suggest that the modulation of gut microbial genera might be attributed to presence of chitin in the feed, acting as a prebiotic and supporting the growth of genera that express chitinolytic activity (e.g., Actinomyces, Bacillus, and Staphylococcus). In an interesting study (Figure 3), Bruno and colleagues [331] examined the microbiota of feeds, water and gut mucus. They discovered that feeds in which FM was replaced by YMW did not alter the core microbiome of the tank biofilm or water column, with Proteobacteria, Firmicutes and Bacteroidota representing the predominant phyla across all samples (Figure 3). However, differential abundance analysis uncovered enhancements and impoverishments in specific taxa, with the control samples illustrating a higher number of genera. The intestine of the FM-free trout had a reduced presence of potentially harmful Citrobacter, Kluyvera, Acinetobacter and Flavobacterium. Other animal protein alternatives to FM have been shown to increase Firmicutes, Spirochaetota and Proteobacteria, as seen after feeding trout with pork viscera–IM-based feeds [256].

It is important to remember that there are some questions when examining the published material on trout gut microbiota that remain unanswered. The microbiome comprises viruses, bacteria, archaea, and eukaryotic microbes, but most studies focus on bacteria. Knowledge of the gut’s mycobiome is not substantive, yet fungi are known to establish and associate with the rainbow trout GIT (e.g., [332,333,334]), produce enzymes that undoubtedly participate in digestive processes, and yeasts produce β-glucans, nucleic acids, and mannan oligosaccharides that have antimicrobial properties. Scarcely anything is known of how feed types influence the gut mycobiome, let alone its interactions with the intestinal bacteriome, with the potential to cause dysbioses. Although viruses significantly outnumber gut bacteria, the awareness of the trout gut virome, its interactions with other microbiota, and whether feed ingredients affect its character is virgin ground for research. Clearly, as parasites of bacteria, phages influence the structure of the gut’s bacteriome and bacterial metabolism, and the virome is known to be engaged in the development and functioning of the immune system, both positively and negatively. The application of metagenomic and bioinformatic technologies will certainly broaden our understanding in this field and reveal whether an unbalanced trout gut virome is the result of changes in nutrition. An additional impediment to trout gut microbiome research, like that with gene expression studies (vide infra), is their short-term nature. Production-length trials are needed to determine how the gut’s microbiota changes with age, rearing conditions, and genetic background, inter alia, to develop management schemes to retain or beneficially modify gut ecologies, avoid dysbiosis, maintain gut patency and promote production efficiency.

5.4. Hematology, Health and Immunity

Yardimci and associates [335] examined the effect of supplanting FM with whey protein and feeding 70 g trout over a 21 d period. At the end of the trial, they reported no differences in red blood cell or leukocyte counts, oxidative radical production, hemoglobin (Hgb) value or hematocrit (Hct). However, serum levels of complement (C3) increased (p < 0.05) following 14 d feeding. Hct, plasma glucose, protein and cholesterol (CHOL) did not differ in the fish fed PBM [244], while [293] found no differences in plasma Hgb, Hct or glutamic pyruvic transaminase (GPT). A PBM/IM- [212] or MBM- [309] based feed and trout fed PBM had lower (p < 0.05) serum total protein (TPROT) and α1-antiprotease activity [292]. Feeding a mixed YMW/BSF meal, Ref. [253] recorded no change in plasma values for Hct, Hgb, TPROT, albumin, glucose (GLU), CHOL and triglycerides. However, Ref. [273] detected declines (p < 0.05) in white blood cells, Hgb and Hct with full replacement of FM using YMW meal. This was attended by a lack of effect on plasma GLU, triglycerides, complement activity, cortisol and IgM levels. The feeding of a diet with high levels of egg flour reduced serum GLU, Mg, Na, K, and P, but increased (p < 0.05) TPROT, uric acid, creatinin, urea, triglycerides, and VLDL [336,337]. When replacing FM with a PBM/BM mix fed to steelhead trout, the feed had no effect on plasma levels of lactic acid, osmolality or TPROT but decreased (p < 0.05) Hgb and Hct [288]. The Hct and erythrocyte fragility in juvenile trout fed freeze-dried ground red wrigglers were unchanged [119].

The substitution of FM with PBM, chicken concentrate, or a chicken and egg concentrate had no effect on the ability of trout to survive injection challenge with Flavobacterium psychrophilum [92]. However, the 100% substitution of FM with BSF meal increased survival by 50% in trout injection challenged with Lactococcus petauri, a causal agent of hemorrhagic septicemia in fish [275], and potentially a foodborne zoonotic agent of clinical significance in humans. The protective effect of BSF meal may be the result of the presence of antibacterial peptides such as cecropin [338], which lyse bacterial cell walls and inhibit proline uptake, causing leaky membranes. Additionally, Sayramoğlu et al. [275] point out that dietary chitin provides a protective effect in fish by inducing the innate immune system, while eumelanin, responsible for the black color of BSF, possesses antibacterial and antifungal activity. The enzymatic cleavage of chitin by endogenous and extrinsic chitinases results in the production of various oligosaccharides, including N-acetyl-glucosamine, which has anti-inflammatory activity and modulates gut microbiota. Also produced is chitobiose, which expresses immune-enhancing, prebiotic, and anti-oxidant properties that may also partly explain BSF’s apparent protective effects. Mohamed et al. [339] describe extracts from BSF larvae fat as being protective against A. salmonicida and A. hydrophila. However, refs. [340,341], using skin mucus and in vitro (fins, gill, and scale) cell culture methods, discerned no differences in trout’s susceptibility to viral haemorrhagic septicaemia virus (VHSV) or Yersinia ruckeri, the causative agent of enteric redmouth disease, following the replacement of FM with BSF meal. The latter observations were confirmed for VHSV by [332], who also reported that BSF-fed trout had, nevertheless, an elevated expression of inflammatory markers and antimicrobial peptides.

Köse et al. [308] used an intraperitoneal injection challenge to examine the survival of fish fed egg flour-based feeds exposed to Lactococcus garvieae, a causal agent of lactococcosis, and Y. ruckeri. After 10 d, the egg flour-fed fish experienced 90% mortality versus 53.3% of the controls following a challenge with Lactococcus, and 97% versus 77% for Yersinia. However, the differences in susceptibility, rather than being a consequence of the feed’s ingredients, may simply reflect the size at challenge. The egg flour-fed fry were only 45% the weight of the controls, and size is known to influence outcomes to Y. ruckeri challenge in trout [342].

5.5. Gene Expression

Gene expression studies help reveal how organisms respond to their environment and clarify the molecular mechanisms underlying physiological processes. In rainbow trout, examining how novel diets, especially those replacing fish meal (FM), alter gene expression has improved the understanding of various physiological control processes and, because most of these depend on the coordinated action of many genes, large-scale array technologies are especially informative. Nevertheless, while gene expression technologies provide the means to explore thousands of genes, this, in general, is for only one moment in time. Gene expression profiles alone have limited practical applications, but their value is multiplied when combined with histological and biochemical methods. This amalgam of techniques enables the confirmation of the functional significance of differentially expressed genes. Like microbiome studies, gene expression analyses have been more frequently applied to IM-based research.

Several studies have evaluated the response of FM substitution with IMs from inflammatory and immunity aspects. Thus, in trout, the substitution of fishmeal with BSF meal decreased (p < 0.05) the relative mRNA abundance of IL-1β, IL-10, TNF-α, NFKβ, and MYD88, while increasing TLR-1 expression in the distal gut [324]. Miebach et al. [321] observed no changes in the transcription of CD8α, β-defensin 3 and 4, IL-1β, TNF-α, or in cathelicidin in fingerling trout fed BSF meal, although occludin expression was elevated in one genetic line. Following a L. petauri challenge, trout fry fed BSF meal for 21 days exhibited an elevated expression of the cytokines TGF, IL-10, IL-1β, TNF-α, and IL-8 (p < 0.05; [275]). In the same study, fold changes in IgM and IgT expression were reduced (p < 0.05), TLR5 expression increased, and MHC-II remained unchanged, collectively suggesting an improvement in immune reactivity. Reductions in hepatic and muscle gene expression for GH, IGF-I, TNF-α, IL-8, and IL-1β were reported in fish fed a mixed BSF/YMW meal [253]. Together with histological findings, it may be concluded that BSF meal does not have a significant impact from an inflammatory or immune perspective and may even be assistive as a feed ingredient.

Chemello et al. [213] examined YMW larvae meal in trout diet and found a significant upregulation (p < 0.05) of MyoD mRNA, with no differences in Myf5, Myf6, Myog, or fMHC expression. Although the authors could not identify the cause of the MyoD increase, its role as a key regulatory factor in muscle initiation, specification, and repair would typically suggest an association with improved growth—an effect that was not observed in their study (Table 2). Although plasma IGF-1 and cortisol concentrations were unaffected by PBM inclusion, both the parameters were influenced by the temperature [296].

6. Body Composition and Quality

Frequently, the exchange of FM with alternative animal proteins modifies whole-body and filets’ proximate composition in some way, most often impacting protein and lipid levels and, more rarely, moisture and ash (Table 5). For example, PBM and mixes thereof have been shown to decrease protein and increase whole-body lipid concentrations (e.g., [212,263,279,307]; Table 5) or to affect whole-body protein [300] and moisture [247,264,306]. A meal comprising the red wriggler earthworm, Dendrodrilus subrubicundus, resulted in increased body moisture and lowered lipid levels when compared to trout fed an FM-based feed [120,311]. A lack of effect has been observed with trout fed whey protein concentrates and MBM [145,292,309]. Obviously, dietary formulation has a major influence on nutrient deposition, and this is especially the case when examining fatty acid profiles. Thus, Parés-Sierra et al. [148] measured higher levels of 18:1n-9 and 18:2n-6 and lower HUFA n-3 in fish fed a diet void of FM and replaced by PBM. However, the PBM-based feed incorporated only poultry oil (3.5%), whereas the control feed contained only FO (7.2%). Similar shifts in filets’ fatty acid profiles were recorded by [255] who fed fish with live crickets A. domestica, superworm Z. morio larvae, and live white worms Enchytraeus albidus [125]. Changes in filets’ protein and lipid levels, which decreased and increased respectively (p < 0.05), were also seen by Acar et al. [253] following feeding fish a mixed BSF-YMW diet.

Changes to filets’ composition are particularly important since organoleptic quality, including texture, flavor, and aroma, can be modified by the prevailing ratios of protein, lipid and moisture. These characteristics, together with shape, color, and others, can all impact products’ desirability and consumers’ purchasing decisions (vide infra). Generally, although dispositions for specific product traits may be dependent on culinary heritage, ethnicity, educational attainment, age and gender, a firmer, flaky texture is preferred. Additionally, trout fed on live insects over 60 d [255] expressed harder filets than controls when evaluated instrumentally and by sensory analysis, while consumers described filets from fish fed BSFL meal as being more fibrous and less juicy [343]. The taste panel of [124] documented a firmer texture in fish fed earthworms (E. foetida) when compared against dried mealworm- and FM-fed rainbow trout. On the other hand, a taste panel evaluation of boiled filets derived from trout fed PBM/FEM/BLM feeds [302] recorded a less firm flesh and fishy odor, although the latter is more dependent on feed lipids and their origin. Reporting on the effects of feeding trout with earthworm or mealworm, Marjanović et al. [124] determined differences for saltiness and sweetness, which were lower, and umami flavor, which was elevated (p < 0.05), with trout derived from a YMW-fed group being described as having superior flavor scores [124] compared with controls. In contrast, Magnani et al. [344] reported that the complete replacement of dietary FM with mealworm larvae meal was without effect on filets’ sensory profile or flavor. However, consumer perception was lower (p < 0.002) when considering the safety of insect-fed fish but higher (p < 0.04) when taking environmental friendliness into account. An important quality factor is flesh color, and the 60 d feeding of a mixture of live insects impacted (p < 0.05) filets’ whiteness (L*) but did not affect their redness (a*) or yellowness (b*) [255,343], and the authors indicated that this, together with changes in sensory attributes, may decrease consumers’ acceptance of such products. Lesiow et al. [295] reported on the sensory effects of storing filets on ice for 1 or 6 d, for trout fed a mixed protein (MBM, BLM, PBM, and FEM) feed. Ostensibly, there were no differences in composition between filets, and the sensory panel was unable to detect deviations for palatability, tenderness, juiciness, or texture, although variations were found in relation to flavor and color at the 24 h time point. Flavor was stronger in the FM-fed trout, but their color was lighter. However, a further 120 h storage resulted in changes (p < 0.05) in filets’ color only, which were lighter in the fish fed the mixed protein feed. Further studies on the impact of alternative proteins and the lipids associated with these meals on filets’ storage characteristics and processing manipulations (e.g., smoking) warrant future investigation.

7. Consumer Acceptance and Anxieties

An important issue influencing the adoption of alternative proteins by both feed and production sectors is how consumers feel about fish reared using alternative feeds. In this regard, customers’ knowledge has been recognized as critical to their acceptance and willingness to pay (WTP). For example, Arru et al. [345] reported that subject knowledge was the most significant factor in purchasing decisions by Italian consumers when confronted with insect-fed fish, followed by dietary recommendations and guidelines, and packaging label information. Word of mouth, on the other hand, had little, if any influence on WTP [345]. An awareness of sustainability issues and understanding the environmental value of using alternative proteins in aquafeeds was found to influence an individual’s WTP more for such products [345,346,347,348]. In contrast, Ankamah-Yeboah et al. [349], who modeled German consumers’ preference for trout fed insect-based feed, reported that fish attributes were more important and that most purchasers were insensitive to the use of insect meals. This finding suggests that switching feed ingredients, at least in Germany, would have limited impact on market demand. Similar acceptability was observed by [346] in Spain, by Ref. [350] for Scottish consumers, by Ref. [351] for Greeks, and by Bazoche and Poret [352] for French markets. Some studies have highlighted negative aspects of IMs to consumers’ acceptance, and these include dietary habits, age, gender and food neophobia (e.g., [352,353,354]). Most researchers have underscored the importance of providing consumers with more information relating to the use of alternate animal-derived ingredients to ease their perception and acceptance.

An additional factor to consider when thinking of alternate proteins is end-user anxieties based on cultural and religious grounds. For example, many western cultures consider insect larvae, such as maggots, as disgusting and unclean [355,356] and this may explain consumers’ reticence to purchase fish reared on IMs (e.g., [353,354]). Noordin et al. [357] highlight the importance of the Islamic consumer and halal foods when considering the use of alternative proteins. Similar exclusions exist for Judaism under kashrut—the laws that deal with kosher products—and include winged insects, rodents, reptiles, amphibians, swine, and all shellfish. Of importance is the feedstock used for insect production, since this may incorporate prohibited, treyf, or haram ingredients. The exploitation of brewery by-products as a feedstock, such as DDGS, for example, is prohibited under Islamic law as are animal blood and products from improperly slaughtered animals. Grape products made by non-Jews, improperly slaughtered animals, blood products and the unacceptable handling of carcasses are likewise considered treyf. There is discussion as to whether the use of IMs as feed ingredients might result in fish being considered as haram [358,359] or whether it is possible for BSFL, for example, to be considered istihalah—the transformation of an impure or al-khabith substance into a pure or at-taiyib one—under Islamic law [360]. These sacred customs thus place severe restrictions on the use of animal by-products as FM alternatives.

8. Summary and Conclusions

Inconsistent growth was observed across the 106 tabulated studies that replaced FM. This was mainly due to differences in ingredient quality, AA balance, digestibility, and FI. It is possible that the presence of plant proteins, which were widely used as components of FM-free feeds, may have exerted an influence on the overall responsiveness of the experimental animals. It is notable that mixtures of alternative proteins tended to perform better than single sources. Even so, under conditions of precise diet formulation and appropriate nutritional supplementation, FM in rainbow trout diets can be completely replaced by terrestrial and aerial animal proteins. Alternative proteins influence organ and gut structure, filet composition, and sensory traits. The gut’s microbiome, too, is often modified, sometimes positively, but the long-term effects and impacts on and of the mycobiome/virome are poorly understood. Gene expression studies indicate some IMs, especially BSF, are supportive of the trout immune system but, again, contradictions exist and longer-term trials are needed to authenticate these claims. The consumer acceptance of trout reared on alternative proteins depends more on fish quality and sustainability messaging than on specific feed ingredients, though religious dietary rules may limit the use of some animal by-products. Consumer education is thus essential and requires more activity across the board.

Models suggest that industrial fisheries’ catches will decline by 4.5–19.4% over the next decade [34,361] which, together with the projected growth in fed aquaculture production, would result in a 1.8 Mt shortfall in feeds, further emphasizing the need for alternatives to FM. Even with the use of non-conventional ingredients, however, eliminating or substantially reducing FM from aquafeeds may offer only limited long-term benefits because global aquaculture growth and competing industries would quickly absorb current and forecast FM supplies, sustaining pressure on already depleted and collapsing stocks. Some alternative animal proteins may also carry higher ecological footprints, depending on production practices. Although more farmers are moving away from marine-based ingredients, substantial research is still needed in relation to precision feeding, advanced diet formulation, ingredient processing, and nutrient optimization to reduce costs and maintain performance, while achieving modern expectations for sustainability, animal welfare, and circular economy practices.

Author Contributions

Conceptualization, E.M. and F.T.B.; methodology E.M. and S.S.; data collection, curation and analysis, S.S. and E.M.; writing—original draft preparation, E.M.; writing—review and editing, F.T.B., F.B. and S.S.; and project administration, F.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The original contributions presented in this study are included in the article. Further inquiries can be directed to the corresponding author.

Acknowledgments

The authors are indebted to the Anthropocene Institute, Palo Alto, CA94301, USA, for their sustained, ardent support (see: anthropoceneinstitute.com).

Conflicts of Interest

Author Frederic T. Barrows was employed by the company Aquatic Feed Technologies LLC, Islamorada, FL 33036. Ewen McLean was employed by Aqua Cognoscenti LLC, West Columbia, SC 29170. All authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Abbreviations

AA = amino acids; Arg = arginine; BLM = blood meal; BSE = bovine spongiform encephalitis; BSF(L) = black soldier fly (larvae); Cys = cystine; CP = crude protein; d = days; EAA = essential amino acids; FCE = feed conversion efficiency; FCR = feed conversion ratio; FE = feed efficiency; FEM = feather meal; FI = feed intake; FM = fishmeal; FO = fish oil; g = grams; GIT = gastrointestinal tract; Hct = hematocrit; Hgb = hemoglobin; His = histidine; HSI = hepatosomatic index; Ile = isoleucine; IM = insect meal; kg = kilogram; LMW = lesser mealworm; Leu = leucine; Lys = lysine; MBM = meat and bone meal; Met = methionine; MM = meat meal; Mt = million tons; PBM = poultry by-product meal; PER = protein efficiency ratio; Phe = phenylalanine; S = survival; SGR = specific growth rate; Thr = threonine; Trp = tryptophan; wt = weight; WTP = willingness to pay; Val = valine; VSI = viscerosomatic index; and YMW = yellow mealworm.

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Figure 3. Relative richness, in percent, of the 25 most abundant families of bacteria from the feed, water column, and gut mucus of rainbow trout fed either an FM- or YMW-based diet over a 22-week period. Columns to the left are FM and those to the left are YMW, and each column represents an individual sample. The figure illustrates the distinctness and variability of the aquaculture system microbiome. The image’s presentation form, but not dataset, is slightly modified from Bruno et al. [331] and is used under the article’s Creative Commons License (http://creativecommons.org/licences/by/4.0/).

Table 5. Proximate whole-body composition of trout, varying in size/age, from 20 trials, fed either FM- or PBM-based diets, and average percent change for each component. Superscript letters denote differences (p < 0.02).

% Difference	PBM	FM
1.2	72.81 ± 3.82	72.01 ± 3.98	moisture
−3.93	15.86 ± 1.74 ^b	16.51 ± 1.67 ^a	protein
8.86	10.57 ± 4.95 ^a	9.74 ± 4.14 ^b	lipid
−2.44	2.12 ± 0.44	2.16 ± 0.45	ash

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McLean, E.; Smith, S.; Brodeur, F.; Barrows, F.T. Responses of Rainbow Trout to Fishmeal Replacement with Terrestrial/Aerial Animal Proteins. Fishes 2026, 11, 198. https://doi.org/10.3390/fishes11040198

AMA Style

McLean E, Smith S, Brodeur F, Barrows FT. Responses of Rainbow Trout to Fishmeal Replacement with Terrestrial/Aerial Animal Proteins. Fishes. 2026; 11(4):198. https://doi.org/10.3390/fishes11040198

Chicago/Turabian Style

McLean, Ewen, Sofea Smith, Ford Brodeur, and Frederic T. Barrows. 2026. "Responses of Rainbow Trout to Fishmeal Replacement with Terrestrial/Aerial Animal Proteins" Fishes 11, no. 4: 198. https://doi.org/10.3390/fishes11040198

APA Style

McLean, E., Smith, S., Brodeur, F., & Barrows, F. T. (2026). Responses of Rainbow Trout to Fishmeal Replacement with Terrestrial/Aerial Animal Proteins. Fishes, 11(4), 198. https://doi.org/10.3390/fishes11040198

Article Menu

Responses of Rainbow Trout to Fishmeal Replacement with Terrestrial/Aerial Animal Proteins

Abstract

1. Introduction

2. Methodology

3. Candidate Proteins

3.1. Insect Meals

3.2. Annelids

3.3. Rendered Animal Meals

3.3.1. Poultry By-Products

3.3.2. Feather/Hoof/Bristle/Hair Meals

3.3.3. Meat and Bone Meals

3.3.4. Blood Meals

3.3.5. Dairy By-Products

4. Technical Features of Animal Proteins

4.1. Composition

4.2. Digestibility

4.3. Palatability

4.4. Pelletability

4.5. Safety Concerns

4.6. Ingredient Costs

5. Effects of Dietary FM Replacement on Rainbow Trout

5.1. Growth

5.2. Morphology and Histology

5.3. Gut Physiology and Microbiome

5.4. Hematology, Health and Immunity

5.5. Gene Expression

6. Body Composition and Quality

7. Consumer Acceptance and Anxieties

8. Summary and Conclusions

Author Contributions

Funding

Institutional Review Board Statement

Data Availability Statement

Acknowledgments

Conflicts of Interest

Abbreviations

References

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