1. Introduction
Fish meal (FM) is generally made from wild-caught, small marine pelagic fish and it has been utilized as a key protein source in aquafeeds because of its high protein content, balanced amino acid (AA) profile, and excellent palatability and digestibility [
1,
2,
3]. However, the declining wild fisheries stock commonly used as an FM source and increasing FM price have severely restricted the use of FM in aquafeeds. Therefore, employing an alternative protein source that is not only economically inexpensive but also environmentally friendly for FM in fish feeds will help to minimize FM dependence and improve the economic return for farmers. The alternative sources of FM mainly come from plant protein, animal protein, and single-cell protein sources [
4]. Animal protein sources with high protein and lipid content, balanced AA profiles, and excellent protein digestibility have generally been considered more suitable alternative for FM in formulated aquafeeds compared to plant protein sources [
4,
5].
Chicken by-product, produced from chicken processing plants is an environmentally friendly and inexpensive source of animal protein to replace FM in aquafeeds [
6,
7]. Chicken by-product contains viscera, heads, bones, blood, and feathers, while viscera and feather account for about 30% and 10% of this waste, respectively [
8]. Improper disposal of chicken by-product could cause environmental pollution, diseases, and the loss of useful biological resources, such as protein, lipid, and enzymes [
8]. Replacements of FM with chicken by-product meal (CBM), chicken waste meal, chicken intestine, and chicken plasma powder have been reported in the feeds of olive flounder (
Paralichthys olivaceus) and abalone (
Haliotis discus hannai) [
6,
7], Asian sea bass (
Lates calcarifer) [
9], grass carp (
Ctenopharyngodon idella) [
10], and largemouth bass (
Micropterus salmoides) [
11], respectively. In particular, Ha et al. [
7] demonstrated that 50% FM replacement with CBM in the 65% FM-based diet of olive flounder could be made without inducing any unfavorable effects on growth and feed availability. Furthermore, up to 10% FM protein in a 35% FM-based diet could be substituted with chicken waste meal without producing any negative impact on the growth and feed availability of Asian seabass [
9].
The palatability and attractiveness of feeds are the critical factors to determine the success of feed manufacture as good palatability can promote fish’s ingestion of available nutrients [
12]. However, increased replacement levels of FM with the alternatives in aquafeeds commonly leads to deteriorated palatability of feed, and eventually brings about reduced feed consumption and growth [
2,
5,
13]. The manipulation of ingredients with excellent palatability in low-FM feeds is an effective method to address this problem [
13]. Some synthetic chemicals, such as betaine, taurine, inosine, nucleotides, and nucleosides are normally considered to improve the palatability of feeds for various fish species [
14,
15,
16]. However, their attractiveness to fish varies greatly depending on fish species, feeding patterns, and the type and dosage of attractants [
14,
17].
Some feed ingredients in formulated fish feeds, such as tuna viscera hydrolysates and jack mackerel (
Trachurus japonicas) meal (JMM), could improve feed intake [
13,
17,
18,
19]. In particular, Chotikachinda et al. [
13] unveiled that the inclusion of 3–4% tuna viscera hydrolysates in the 54% poultry by-product meal-based diet enhanced feed palatability and increased the feed consumption and growth of Asian sea bass. Furthermore, JMM containing AA, inosine-5′-monophosphate (IMP), and nucleotides as palatability enhancers have been explored in some fish species [
18,
20,
21,
22]. Takakuwa et al. [
23] also found that IMP in the muscle extracts of jack mackerel showed the strongest feeding stimulating response to greater amberjack (
Seriola dumerili). Furthermore, JMM exhibited the strongest attractiveness to olive flounder among 15 ingredients [
18], and manipulation of 5% JMM in extruded pellets produced the greatest attractiveness to olive flounder and led to the highest feed consumption and greatest growth. Choi et al. [
24] also demonstrated that incorporation of JMM as the main protein source in the feeds of grower walleye pollock (
Gadus chalcogrammus) resulted in statistical improvements in growth and daily feed consumption compared to walleye pollock fed diets with anchovy meal or pollock meal as the main protein source. Thus, the application of JMM in low FM diets, commonly resulting in deteriorated feed intake and reduced growth performance, can resolve their disadvantages in fish culture.
Rockfish is a viviparous marine teleost belonging to the
Sebastidae family [
25] and are widely dispersed over the Northwest Pacific coast [
26]. However, the natural stock of rockfish has dramatically decreased in recent years, primarily due to habitat deterioration caused by overfishing and pollution [
26]. Meanwhile, rockfish aquaculture industry has rapidly expanded since 1987 [
25]. As the second-highest cultured marine fish species, its aquaculture production reached 16,189 metric tons in Korea in 2022 [
27]. With the widespread cultivation of rockfish in the Eastern Asia, many nutritionists are paying attention to development of the rockfish feeds [
19,
22,
28,
29,
30,
31,
32,
33,
34]. The growth and feed intake of rockfish improved with increased incorporation levels of JMM from 0% to 40% at the expense of FM in diets, and optimum inclusion levels of JMM in diets were estimated to be 39.7 and 40.3% of FM based on weight gain and feed intake, respectively [
19]. The highest feeding attractant response of rockfish was also noticed in JMM among 16 crude protein sources [
29].
Application of low FM diets in practical feeding is unavoidable for sustainable fish culture [
35]. Our earlier study [
36] also proved that the replacement of FM with up to 20% CBM could be made without deteriorating the growth and feed intake of rockfish. Based on the substitutability of CBM for FM and the strong attractiveness of JMM to rockfish, this study was designed to elucidate the impact on the growth performance and feed availability of rockfish from including JMM in diets which otherwise substitute 20% FM with CBM.
4. Discussion
Our earlier study [
36] found that up to 20% of fish meal (FM) could be replaceable by chicken by-product meal (CBM) without deteriorating growth and feed utilization of rockfish when juvenile rockfish were supplied with a 55% FM-based feed or one of the feeds which replace 10, 20, 30, 40, and 50% FM with CBM. Kim et al. [
29] unveiled that jack mackerel meal (JMM) showed the strongest attractiveness to rockfish among 16 crude protein sources. That is why, in this study, we included the graded levels (0–80%) of JMM in low-FM diets which replace 20% FM with CBM. That is also why we tried to figure out the impact on growth and feed availability of rockfish from manipulating the graded levels (0–80%) of JMM in low-FM diets which replace 20% FM with CBM. No statistical differences in weight gain, SGR, and feed intake of the rockfish fed the Con and C20J0 diets supported our early finding [
36].
Linear improvement relationships in weight gain, SGR and feed intake of rockfish vs. incorporated JMM levels in low-FM diets which substitute 20% FM with CBM in this experiment indicated that JMM effectively improved feed intake of rockfish which were fed the low FM diets, eventually resulting in improved growth performance. However, no statistical differences in growth, SGR, and feed intake of rockfish which were fed the C20J60 and C20J80 diets implied that the C20J60 diet appeared to be the most recommended dietary treatment in this experiment. However, incorporated JMM levels up to 40% in the 55% FM-based diet improved weight gain, SGR, and feed intake of rockfish; however, JMM inclusion levels higher than 40% (60% and 100%) did not improve further when juvenile rockfish were fed with a 55% FM-based diet or one of the diets which include 1, 3, 5, 10, 20, 40, 60, and 100% JMM at the cost of FM in the 56-day feeding experiment [
19]. They also concluded that optimum inclusion levels of JMM were estimated to be 39.7 and 40.3% based on weight gain and feed consumption, respectively. Similarly, rockfish fed an extruded pellet incorporating 5% JMM as a feed enhancer instead of anchovy meal brought out the best weight gain and highest feed intake [
22].
Feed ingredients from marine animal origins, such as FM, fish hydrolysates, fish oil, shrimp meal, and krill meal in diets are commonly known to have positive palatability for several fish species [
43]. Wei et al. [
44] revealed that substituting up to 75% FM with Antarctic krill (
Euphausia superba) meal in diets could be made without inhibiting growth performance when large yellow croaker (
Larimichthys crocea) was provided with a 40% FM-based diet or one of the diets which replace 15, 30, 45, 60, and 75% FM with Antarctic meal for 9 weeks. They also stressed that dietary FM replacement with Antarctic meal resulted in improved feed intake and good skin color in muscle of large yellow croakers, and they explained that the improved feed intake might have been due to the excellent palatability of krill meal or leaching of smell-releasing chemical compounds from krill meal into the water, which stimulated feed searching behavior in fish. Similarly, the tissue of jack mackerel contains feeding attractants, such as AA, IMP, and nucleotides [
21], which might trigger the ingestion of rockfish fed the C20J60 and C20J80 diets, resulting in improved growth performance in this experiment. Furthermore, IMP derived from mackerel muscle extracts promoted feeding activity of the yellowtail (
Seriola quinqueradiata) [
20], Pacific bluefin tuna (
Trachrus japonicus) [
45], and greater amberjack (
Seriola dumerili) [
23]. Ikeda et al. [
46] also found that among the components of the synthetic muscle extracts of jack mackerel, AA, especially histidine, exhibited the highest feeding stimulant activity to olive flounder. Likewise, Kim and Cho [
22] revealed that AA, such as alanine, glycine, and histidine, and free histidine content in diets, showed correlations with the growth performance of rockfish. Therefore, increased alanine, glycine, and, in particular, histidine content in diets which replace 20% FM with CBM with incorporated levels of JMM could improve the palatability and eventually the feed intake and growth of rockfish in this experiment.
Except for arginine, all EAA content in CBM were relatively lower than those in FM. However, all EAA profiles of JMM were similar to those of FM (anchovy meal), except for the high content of histidine and the low content of leucine and tryptophan in the former. Several factors including feed intake, water temperature, fish size (age), and fish sex may influence the requirements of AA in diets [
47]. Nevertheless, the content of arginine (2.97–3.12% of the diet) and lysine (3.43–3.73% of the diet) in all the experimental feeds fulfilled the requirements (2.78 and 2.99% of the diet, respectively) for rockfish [
41,
42]. Furthermore, marine fish species require EPA, DHA, and ARA for their appropriate growth and development since they are likely to lack the ability to synthesize long-chain polyunsaturated FA (PUFA) from their 18-carbon precursor FA [
48]. The requirement of ∑n-3 HUFA (5.88% of total FA) for rockfish [
30] was also met in all the experimental feeds (6.68–7.51% of total FA).
No remarkable differences were found in the FCR, PER, and PR of rockfish in the present experiment, perhaps demonstrating that the elevated growth performance of rockfish was the result of the improved feed intake. Additionally, the biometric indices of the rockfish were not changed by the dietary treatments, consistent with the result of our previous study [
19] showing that the inclusion of JMM in rockfish feeds did not influence feed utilization and biometric indices. Similarly, feed utilization and biometric indices of olive flounder were not changed when 25 and 50% of FM were substituted with various animal proteins (tuna by-product meal, CBM, and meat meal) and 12% JMM inclusion as feed stimulants [
49]. Additionally, the FCR of Atlantic salmon (
Salmo salar) and Atlantic halibut (
Hippoglossus hippoglossus) were not influenced when fish were fed with a 61% FM-based diets or one of the diets which incorporate 20, 40, and 60% of krill meal or 40% amphipods meal at the expense of FM [
50].
No remarkable differences in the proximate composition and AA profiles of rockfish were found in this experiment, consistent with other studies in which incorporation of JMM in feeds did not affect the proximate composition and AA profiles of whole-body rockfish [
19] and olive flounder [
17], and the chemical composition of the muscle and liver of walleye pollock [
24]. Similarly, the incorporation of feed ingredients in diets did not alter the whole-body chemical composition and AA profiles of the large yellow croaker [
44], and chemical composition of the red sea bream (
Pagrus major) [
51,
52], olive flounder [
53], and Atlantic salmon [
50].
The n-3 HUFA are non-dispensable FAs for all vertebrates including fish and humans [
54]. Like all other vertebrates, fish require n-3 HUFA for normal growth and development including reproduction to maintain the normal structure and function of cell membranes [
55]. The low content of ∑n-3 HUFA in diets might lead to a decrease in the content of these non-dispensable FAs in fish, which could have adverse impact on consumer health [
56]. Because of the negligible amount of EPA, DHA, and ∑n-3 HUFA in CBM, the C20J0 diet exhibited the lowest ∑n-3 HUFA content. However, elevated JMM inclusion levels in low FM diets substituting 20% FM by CBM resulted to decreased ∑SFA and ∑n-3 HUFA, but increased ∑MUFA, eventually bringing about decreased ∑SFA and ∑n-3 HUFA, but increased ∑MUFA of the whole-body rockfish at the end of the 8-week feeding experiment. Likewise, FA profiles of the whole-body fish were well reflected from dietary FA profiles [
2,
48,
57]. The dorsal muscle FA profiles of large yellow croakers were also influenced by FM substitution with krill meal in diets [
44]. Suontama et al. [
50] demonstrated that the EPA content of the muscle of Atlantic salmon was changed by incorporating krill meal and amphipods meal in diets, while the ∑SFA, ∑MUFA, and total content of PUFA were unaffected by dietary treatments. Unlike this experiment, the FA profiles of olive flounder were not influenced by dietary treatments when 12% JMM was included in diets which replace 25 and 50% FM with animal proteins [
49].
In numerous pathological and ecotoxicological studies, plasma and serum parameters have been employed as the typical indicators of fish health status [
32]. AST and ALT can be detected in the blood, liver, and spleen of fish. When fish are healthy, they maintain modest activity; however, when there is tissue necrosis or disease, they are released, resulting in higher activity [
58]. In addition, SOD and lysozyme activity are reliable indicators for determining the effect of nutrition on the health status of fish [
59]. However, none of the plasma and serum measurements of rockfish were changed by the dietary treatments in this experiment, agreeing with our early study [
49] showing that the incorporation of JMM in low-FM diets which replace 25 and 50% FM with various animal proteins did not influence the plasma and serum parameters of olive flounder. However, the serum T-BIL, TP, and lysozyme activity of the Asian sea bass were changed when Asian sea bass were fed with the 72.6% FM-based diet or one of the diets which replace 80, 85, and 90% FM with poultry by-product meal with supplementation of 3.5–7% tuna hydrolysate and 5–10% black soldier fly (
Hermetia illucens) larvae meal [
60]. Additionally, the plasma ALT and AST of Atlantic salmon were altered when fish were provided with diets incorporating krill meal or amphipod meal [
50].
In regard to the economic analysis of this study, the C20J60 diet produced a slightly but not significantly higher EPI when compared to the C20J80 diet. This also well supported by the growth of the rockfish fed the C20J60 diet. Thus, when compared with the previous studies, the results obtained in this innovative study suggested that the manipulation of JMM in the low-FM diets is a good strategy to improve the palatability of diets and feed consumption for rockfish. Furthermore, the C20J60 diet appears to be the most recommendable dietary treatment as farmers can receive a high economic return in practical aquaculture.