Abstract
A six-treatment study in a 3 × 2 factorial design was conducted to investigate whether dietary supplementation of shrimp hydrolysate (SH) improves the efficacy of meat and bone meal (MBM) replacing fishmeal protein in juvenile giant trevally Caranx ignobilis. A fishmeal-based diet (MBM0) was used as a control; two low fishmeal diets were prepared by replacing 25% (MBM25) and 50% (MBM50) of fishmeal protein with MBM; and another three treatments by supplementing MBM0, MBM25, and MBM50 with 45-g/kg SH supplementation (MBM0SH, MBM25SH, MBM50SH) were produced. The results showed that fish fed MBM25 and MBM50 caused lower growth and feed utilization than MBM0, whereas no differences were observed among fish fed MBM25SH, MBM50SH, and MBM0. Increasing dietary MBM levels resulted in decreased lipids in fish muscles and increased ash contents, while SH supplementation improved the muscle lipid levels. Substituting fishmeal with MBM increased monounsaturated fatty acids (MUFA) and decreased polyunsaturated fatty acids (PUFA), n-3 polyunsaturated fatty acid (n-3 PUFA), n-3 highly unsaturated fatty acids (n-3 HUFA), and n-3/n-6 HUFA, whereas SH supplementation enhanced n-3 PUFA, n-3 HUFA, and n-3/n-6 HUFA. The goblet cell density in the intestine increased in fish fed diets supplemented with SH. The study suggested that dietary supplementation of 45-g/kg SH increased the efficacy of substituting MBM protein for 50% of fishmeal protein without compromising the growth of juvenile giant trevally.
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Introduction
Fishmeal is currently used as the primary protein source in aqua-feed production (Watanabe 2002). However, the increasing requirement and high price of fishmeal with expansion of aquaculture have put pressure on its supply (Zheng et al. 2014; Khosravi et al. 2015b; Tacon and Metian 2015). Feed cost normally accounts for up to 60% of the total aquaculture operational cost; therefore, reduced fishmeal level in diets will increase the profitability of the operation (Hernandez et al. 2016). Therefore, efficient use of the less expensive and more sustainable alternative protein source(s), which contain equal or even better quality than fishmeal protein, is crucial for the sustainability of aquaculture.
Meat and bone meal (MBM) is one of the promising alternative protein sources; it has been popularly used in poultry feed due to its high protein level and more beneficial effect on the growth performance of poultry (Ai et al. 2006). In aquaculture, MBM has been reported to partially replace the fishmeal without compromising the growth and feed utilization in spotted rose snapper Lutjanus guttatus fed 252-g/kg MBM (Hernandez et al. 2016), Florida pompano Trachinotus carolinus fed 100-g/kg MBM (Rossi Jr and Davis 2014), Korean rockfish Sebastes schlegeli fed 123-g/kg MBM (Yan et al. 2014), rainbow trout Oncorhynchus mykiss fed 120-g/kg MBM (Bureau et al. 2000). However, reduced growth performance was observed in white yellowtail Seriola quinqueradiata fed 192-g/kg MBM in diet, large yellow croaker Pseudosciaena crocea fed more than 325-g/kg MBM (Ai et al. 2006), and turbot Scophthalmus maximus fed 342-g/kg MBM (Song et al. 2016). Lower digestibility and unbalanced essential amino acids may attribute to the adverse responses in fish fed high MBM (Ai et al. 2006). Therefore, there is a need to investigate the effect of supplementing the selected ingredients to improve digestibility and overall desirable characteristics of the diet including MBM as partial replacement of fishmeal protein.
One of the potential supplements such as fish protein hydrolysate (FPH) can increase the efficacy of poultry by-product protein in aqua-diets as its positive effect on the growth performance of barramundi Lates calcarifer (Siddik et al. 2019) and pompano Trachinotus blochii (Pham et al. 2021) was proven. FPH has also shown to improve the growth and protein retention of Japanese flounder Paralichthys olivaceus (Zheng et al. 2014) and turbot Scophthalmus maximus (Xu et al. 2017) fed high plant protein–based diets. Further, FPH inclusion has shown to improve the growth and innate immunity of European seabass Dicentrarchus labrax (Costa et al. 2020) and restored the intestinal inflammation of Florida pompano Trachinotus carolinus (Novriadi et al. 2017) fed plant-based diets. Supplementation of FPH may provide essential amino acids which are normally limited in alternative protein sources, thereby improving the efficacy of the diets (Siddik et al. 2019). FPH also acts as an attractant and thus enhances the palatability of feed (Chotikachinda et al. 2013). High digestibility of FPH due to the availability of low molecular weight peptides and free amino acids (Refstie et al. 2004; Ospina-Salazar et al. 2016; Siddik et al. 2018b) is also documented (Kader et al. 2012; Khosravi et al. 2015b). Furthermore, bioactive properties of FPH stimulate the immune function and disease resistance in red sea bream Pagrus major (Khosravi et al. 2015a), Japanese seabass Lateolabrax japonicus (Liang et al. 2006), and coho salmon Oncorhynchus kisutch (Murray et al. 2003).
Giant trevally Caranx ignobilis is one of the commercially farmed species and has been widely cultured in Vietnam since the success of seed production, in which trash fish has been using as major feed for grow-out culture of this species. As carnivorous species, giant trevally generally requires high dietary protein and our previous study on this species has reported that the 52% protein and 10% lipid in a fishmeal-based diet provide desirable growth and feed utilization (Nguyen et al. 2022). Up to date, there is very few available information on nutritional requirements and diets for this species. In order to evaluate feed ingredient and nutritional responses of giant trevally fed formulated diets, the present was carried out to investigate whether SH supplementation in the diets of juvenile giant trevally has any positive effects when fishmeal protein is partially replaced by MBM.
Materials and methods
Diet preparation
The fishmeal-based diet with 52% protein and 10% lipid was formulated as a control diet (MBM0), and two other diets were prepared by replacing 25% (MBM25) and 50% (MBM50) fishmeal protein with MBM protein. Another three diets with the same MBM inclusion levels as above were prepared with 45-g/kg SH supplementation (MBM0SH, MBM25SH, and MBM50SH, respectively). All diets were made isonitrogenous and had the same energy values. All the dietary ingredients were finely ground, weighed, and well homogenized. The mixture was then mixed with fish oil and water before pelletizing through a 1–2-mm die. The pellets were dried at 60 °C in the oven for 12 h and stored at – 0 °C until use. The composition of feed ingredients and experimental diets is presented in Tables 1 and 2, respectively.
Experimental procedure
Juveniles of giant trevally were supplied by a commercial marine fish hatchery in Nha Trang (Khanh Hoa, Vietnam). The fish were acclimatized to the experimental condition for 2 weeks before feeding trial. During acclimation, fish were fed a commercial diet for marine fish with 52 protein and 10% lipid. After acclimation, the uniform-size and healthy fish were selected and randomly distributed into eighteen 250-L fiberglass tanks in triplicate with 30 individuals/tank. Fish (initially mean weight of 5.11 ± 0.04 g) were fed in six dietary groups for 8 weeks. Fish were hand-fed at 8 am and 4 pm until they achieved apparent satiation. Uneaten feed was collected 30 min after feeding and stored in a freezer to determine feed intake. The water in tanks was managed under a flow-through system with a flow rate of approximately 5 L/min. Water quality parameters, including temperature, salinity, pH, dissolved oxygen, and total ammonia, were maintained in suitable ranges of 29.5 ± 2 °C, 31 ± 1 ppt, 7.8 ± 0.2, 6.5 ± 0.3 mg/L, and < 0.5 mg/L, respectively.
Sample collection and chemical analyses
At the beginning of the experiment, fifteen fish were sampled to analyze initial proximate composition. At the end of the experiment, fish were starved for 24 h before anesthetizing them with MS-222 at 100 mg/L, then individually weighed, and length was measured using a technical scale (FHB 1000, Ningbo Company, China). Six fish per tank were anesthetized for blood collection; then, those fish were euthanized with an overdose of MS-222 at > 200 mg/L before dissecting the intestine, liver, viscera, and muscle to calculate the hepatosomatic and viscera-somatic indexes and take histological examination. Other three fish in each tank were euthanized for tissue proximate composition. Proximate compositions of feed and fish were determined following AOAC (1995). The protein and lipid were analyzed using Kjeldahl and Soxhlet methods, respectively. Moisture level was determined by drying in an oven (Thermotec 2000, Contherm Scientific, New Zealand) at 105 °C. Ash was analyzed by combustion at 550 °C for 24 h in an electric muffle furnace (Carbolite, Sheffield, UK). Amino acids in the diets were determined after acid hydrolysis by gas chromatography with GC 2010 Plus (Shimadzu, Kyoto, Japan). The muscle fatty acid composition was analyzed following the method described by O’Fallon et al. (2007).
Hematological parameters
As mentioned in the section above, six fish in each tank were anaesthetized for blood collection by puncturing their caudal vein with a 25-gauge needle, as the method described by Pham et al. (2019). The blood was centrifuged at 5000 g for 10 min at 4 °C; then, separated serum was analyzed for total cholesterol, triglyceride, protein, and glucose using an automated blood analyzer (Beckman Coulter AU680, USA).
Histological examination
After collecting blood, those six fish were euthanized to dissect the intestines and livers. The intestines and livers were put into a 10% buffer formalin solution. The livers were dehydrated in ethanol, equilibrated in xylene, and then embedded in paraffin wax following standard histological techniques. The 5–6-µm sections were cut and stained with hematoxylin–eosin solution and examined under light microscopy (Labomed CXR3, USA) and imaged with 10 M camera. The number of goblet cells was counted in the highest 10 mucosal folds with the numbers expressed as average number of goblet cells per fold as described by Ramos et al. (2017).
Calculations
Various parameters were calculated using the following equations:
Statistical analysis
All data were presented as mean ± SE. SPSS for Windows version 22 (IBM, New York, USA) was used to perform statistical analysis of all the data sets. The effects of dietary MBM inclusion levels, SH supplementation, and their interaction on all test parameters of juvenile giant trevally were examined following two-way ANOVA. When a significant interaction between dietary treatments occurred, one-way ANOVA with post hoc Tukey’s HSD multiple comparison test was applied to determine differences among six dietary groups, but not for means of main effects. When no interaction and a significant main effect were detected, a Tukey in two-way ANOVA was applied to determine the differences among substituted MBM groups. The statistical significance was examined at P < 0.05.
Results
Growth performance and feed utilization
The fish was fed slowly until satiation, and very few residual feeds at the tank’s bottom indicated the fish accepted experimental diets. No pathological signs were observed during the feeding trial. After 8 weeks, dietary MBM inclusion levels, SH supplementation, and their interaction significantly influenced the specific growth rate (SGR). The highest (P < 0.05) SGR was observed in fish fed MBM0SH, followed by MBM0, MBM25SH, and MBM50SH while fish fed MBM25 and MBM50 had the lowest SGR (Table 3).
Similarly, feed conversion ratio (FCR) was affected by dietary MBM, SH supplementation, and their interaction (P < 0.05). MBM50 showed higher FCR than MBM0, while no difference in FCR was seen among MBM0, MBM0SH, MBM25, and MBM25SH. Replacing 50% of fishmeal with MBM showed lower FI than fishmeal-based diet while no change in FI was seen among the substitution level of 25% and fishmeal-based diet. Fish fed SH-supplemented diets achieved higher FI than fish fed non-SH diets. The highest (P < 0.05) survival rate was observed in fish fed MBM0 and MBM0SH, followed by MBM25, MBM25SH, and MBM50SH, while fish fed MBM50 obtained the lowest survival rate (Table 3).
Proximate composition in muscle and somatic index
Protein and moisture levels in muscle were not different among fish fed any diets. In contrast, lipid content significantly decreased (P < 0,05) with increasing dietary MBM levels; it was higher in fish fed diets with SH than groups fed diets without SH. Dietary MBM affected ash level in muscle as higher ash was recorded in fish fed MBM diets than non-MBM diets (Table 4).
Dietary MBM significantly affected visceral somatic index (VSI) (P < 0.05), wherein diets with 50% of fishmeal replaced by MBM showed higher VSI in fish than other feeding diets. The interaction between dietary MBM inclusion and SH supplementation affected hepatosomatic index (HSI). Higher HSI was achieved in fish fed MBM0, MBM0SH, and MBM25SH compared to fish fed MBM25, MBM50, and MBM50SH. CF was not affected by dietary MBM, SH supplementation, and their interaction (Table 4).
SFA and MUFA were affected by MBM levels, supplemented SH, and their interaction (P < 0.05). The lowest SFA and MUFA were obtained in fish fed MBM25SH, whereas no difference was seen among other treatments (Table 5). Replacing fishmeal with MBM decreased PUFA, n-3 PUFA, n-3/n-6 HUFA, and n-3 HUFA. On the contrary, SH supplementation improved n-3 PUFA, n-3/n-6 HUFA, and n-3 HUFA (Table 6).
Histological examination
Histological examination showed normal hepatocytes in all feeding groups (Supplementary 1). The MBM and SH interaction significantly affected the number of goblet cells (GCs) in the distal intestine of giant trevally (P < 0.05). Fish fed MBM25 and MBM50 had the lowest GCs compared to other dietary groups. The highest GCs were observed in fish fed the MBM0, MBMSH and MBM25SH diets. At each replacement level, the SH supplementation significantly increased GCs compared to those fed MBM without SH supplementation (Fig. 1).
Hematological parameters
SH supplementation did not influence the blood biochemical parameters, whereas dietary MBM significantly affected (P < 0.05) total protein (TP), aspartate (AST), and alanine aminotransferase (ALT). Fish fed 311-g/kg MBM had significantly lower TP than those fed the control diet, while the AST was significantly reduced as increasing dietary MBM more than 155.5-g/kg diet. There was no difference on TP and AST of the fish fed the control and 155.5-g/kg MBM diets. ALT was affected by the interaction between dietary MBM level and SH supplementation, as lower ALT was seen in fish fed MBM50 than other remaining diets (Table 7).
Discussion
MBM has been used as a potential alternative protein source to fishmeal in diets of aquatic animals. However, the results also revealed negative effects in marine fish fed high MBM inclusion diets. Song et al. (2016) reported the reductions in growth and feed efficiency of turbot fed 342-g/kg MBM, while these threshold MBM levels in rainbow trout (Bureau et al. 2000; Esmaeili et al. 2017), large yellow croaker (Ai et al. 2006), and Japanese flounder (Kikuchi et al. 1997) were 381.6, 434.4, and 360-g/kg diets. These findings were consistent with the present study wherein 25% and 50% of dietary fishmeal protein replaced by MBM protein without SH supplementation caused lower growth and feed intake and higher FCR in giant trevally. Unbalanced amino acid profile and lower digestibility of MBM can contribute the reduced growth and feed utilization in fish (Ai et al. 2006). High level of poorly digested ash in MBM may also result in low digestibility (Bureau et al. 1999). Robaina et al. (1997) showed that diets containing more than 12.5% ash had negative effects on protein digestibility. Therefore, dietary ash increased from 10 to 17.97% as increasing dietary MBM up to 311-g/kg diet could negatively affect nutrient digestibility, resulting in growth reduction of giant trevally fed high MBM diets in this study. Less palatability and the abundance of SFA and MUFA acids in MBM may be responsible for the reduction of feed intake, thereby decreasing the growth of fish (Xue and Cui 2001; Turchini et al. 2009). The supplementation of essential nutrients, especially derived from marine by-product including FPH, may deal with the adverse effects presented by feeding a diet in high non-fishmeal protein source (Kader et al. 2012; Khosravi et al. 2015b). The previous studies reported that the FPH effectively reduced the negative impacts on the growth and welfare of fish, which were caused by inclusion of plant meal (Gisbert et al. 2018; Khosravi et al. 2018; Costa et al. 2020) and poultry by-product meal (Siddik et al. 2019; Chaklader et al. 2021; Pham et al. 2021). The reason for this could be high levels of free amino acid, available peptide fractions, digestibility, excellent viscosity (Saidi et al. 2014; Swanepoel and Goosen 2018), well palatability (Refstie et al. 2004), and bioactive properties (Costa et al. 2020) in FPH, which are suitable for intestinal assimilation, nutrient digestion, and absorption in aquatic animals. In this study, giant trevally fed 311-g/kg MBM diet supplemented with SH had no differences on growth and feed efficiency with those fed the control diet, indicating that SH supplementation could be an approach pathway to increase fishmeal replacement levels in giant trevally diets. However, the fish fed the highest MBM inclusion diets also had significantly lower survival rate than those fed the control, regardless with SH supplementation. This was consistent with observations on Pseudobagrus ussuriensis and large yellow croaker fed high MBM inclusion diets (Ai et al. 2006; Tang et al. 2018). In this study, no pathological signs were observed in fish during the feeding period and the liver tissues did not show any histopathological lesions among treatments; however, reduced survival rate in fish fed high MBM diets could be attributed to the imbalance of essential amino acids and deficient PUFA in high-MBM diets. In this study, most essential amino acids, especially methionine and lysine, reduced as increasing dietary MBM levels (Table 2), which could prevent the liver metabolism and induce liver lesions, resulting in reduced growth and survival as reported in Pseudobagrus ussuriensis (Tang et al. 2016).
The published literature has provided a mixed response of using dietary MBM as a fishmeal protein replacement on proximate composition. For example, no differences were observed in body composition of hybrid striped bass Morone chrysops × Morone saxatilis (Bharadwaj et al. 2002), gilthead seabream (Robaina et al. 1997), and rainbow trout (Bureau et al. 2000) fed up to 450, 280, and 240-g/kg MBM inclusion diets, respectively, whereas Pseudobagrus ussuriensis showed reduced protein and lipid contents in the whole body and muscles as increasing dietary MBM more than 200-g/kg diets (Tang et al. 2018). Ai et al. (2006) also reported the increased moisture and reduced lipid levels in the body of large yellow croaker fed more than 434.4-g/kg MBM diets. In the present study, dietary inclusion of MBM did affect ash and lipid levels in the muscles, although no change was observed in protein and moisture levels. Ash content increased while lipid decreased with increased dietary MBM levels, as seen in large yellow croaker (Ai et al. 2006) and Pseudobagrus ussuriensis (Tang et al. 2018). High ash deposition in the muscle of giant trevally was directly related to high ash level in MBM-based diets. Lower muscle lipid in fish fed MBM diets may be associated with low lipid digestibility of MBM diets and lipid metabolism in fish. Watanabe (1982) stated that the high SFA level in MBM reduced lipid digestibility in rainbow trout. Declined n-3 HUFA in fish with increased dietary MBM levels in the present study confirm the findings of Ai et al. (2006) that high-MBM diets inhibit the lipid metabolism. High dietary FPH can reduce the fatty acid synthesis, but promotes the lipid oxidation and energy utilization, leading to low lipid accumulation (Liaset et al. 2009; Bjørndal et al. 2013; Xu et al. 2016). However, a low FPH level elevated body lipid as seen in Japanese flounder fed 45-g/kg FPH (Zheng et al. 2014), rainbow trout at 16–32% FPH inclusions. The present result found that 45-g/kg SH enhanced the muscle lipid levels and the synthesis of HUFA (Table 6) and might compensate for lipid and unsaturated fatty acid deficiency caused by replacing 25% fishmeal with MBM, resulting in similar HSI between fish fed MBM25SH and fishmeal-based diet.
Hematological analysis showed lower total serum protein in fish fed diets replacing 50% fishmeal with MBM compared to fish fed non-MBM diets while there was no difference in serum glucose, cholesterol, and triglyceride among any feeding treatments. Siwicki et al. (1994) stated that improved total protein links to the stronger innate immunity of fish. High total protein and a low ratio of albumin/globulin indicate good health (Siwicki et al. 1994; Pham et al. 2021). Declined total protein may impact the welfare of giant trevally fed diets substituting 50% fishmeal with MBM. Plasma ALT and AST reflect liver health; they leak into the blood at abnormal levels if the hepatic cells are impaired due to any stress (Ye et al. 2019). The use of dietary non-fishmeal protein resources has been reported to negatively affect ALT and AST of fish (Ye et al. 2019; Chaklader et al. 2020b). Increased plasma ALT and AST were observed in hybrid grouper (Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂) fed dietary animal protein blend replacing fishmeal levels at 20–80% and 80% respectively, leading to suppress the immune competence (Ye et al. 2019). Similarly, the serum AST in barramundi increased when they were fed poultry by-product, causing liver injury (Chaklader et al. 2020b). On the contrary, no changes in AST and ALT caused by poultry by-product inclusions in diets were recorded in barramundi (Siddik et al. 2019; Chaklader et al. 2021). In the present study, plasma AST and ALT even decreased in fish fed diets substituting MBM for 50% of fishmeal, indicating that replacing 50% fishmeal with MBM did not damage the hepatic cells in giant trevally. Besides, the histological observation showed no alteration in the livers of all fish fed any diets, additionally proving that replacing up to 50% fishmeal with MBM did not impair the liver of juvenile giant trevally.
The intestine is a crucial immune organ in fish; improved intestinal health enhances the mucosal epithelium preventing microbial infections (Siddik et al. 2019). The intestine epithelium is significantly affected by nutrition intake, and insufficient nutrition can change the intestine micromorphology such as fold height and goblet cell density (Siddik et al. 2018a). Goblet cells generate mucus that contains several defensive substrates, influencing the innate immunity of the host species (Chaklader et al. 2021). The present result showed that higher goblet cell density in the intestine of fish fed diets with SH supplementation than fish fed diets without SH (Fig. 1), indicating that SH supplementation improved intestine health of giant trevally fed MBM replacing up to 50% fishmeal protein. The result was consistent with the finding in pompano, wherein adding 10% viscera hydrolysate protein increased the goblet cell number and fold heights of the intestine (Pham et al. 2022). Chaklader et al. (2020a) reported that the supplementation of various hydrolysates with poultry by-product elevated the goblet cell number in barramundi and increased the goblet cell densities enhancing the innate immunity against microorganisms (Siddik et al. 2018b). Hydrolysate supplementation also healed the intestine inflammation of Florida pompano fed high plant-based diets (Novriadi et al. 2017).
Fatty acids in the muscle of giant trevally were affected by substituted MBM levels and supplemented SH. Regardless of SH supplementation, fish fed dietary MBM replacing 50% fishmeal had the highest MUFA, as elevated fillet MUFA with increasing dietary MBM levels in rainbow trout (Esmaeili et al. 2017) and large yellow croaker (Ai et al. 2006). The fatty acid composition in muscle mirrors the dietary fatty acids, which involved the abundance of MUFA and SFA and the deficiency of PUFA and HUFA in high-MBM-based diets (Watanabe 1982). Giant trevally fed MBM diets also showed poorer DHA, EPA, PUFA, and n-3 HUFA than fish fed fishmeal-based diet, as seen in large yellow croaker (Ai et al. 2006) and rainbow trout (Esmaeili et al. 2017). Besides, the lack of PUFA, HUFA in dietary MBM, and increased oxidation may cause the reduction of PUFA and HUFA in fish fed dietary MBM (Esmaeili et al. 2017). However, lower muscle SFA was obtained in giant trevally fed dietary MBM, inconsistent with the finding in rainbow trout (Esmaeili et al. 2017), which may be due to the use of these fatty acids for energy production. Besides, the present result showed lower SFA and MUFA and higher DHA, EPA, PUFA, n-3 PUFA, n-3/n-6 HUFA, and n-3HUFA in fish fed SH supplemented diets compared to fish fed SH non-supplemented diets. The result agreed with Pham et al. (2022), who stated that PUFA and n-3PUFA increase with increasing FPH substitution to fishmeal from 5 to 20%. Likewise, the significantly elevated levels of PUFA, n-3HUFA, n-6HUFA, and n-3/n-6HUFA in muscle were noticed in barramundi fed diets containing high poultry by-product level with FPH supplementation (Chaklader et al. 2020a). The change in PUFA and HUFA in fish fed FPH may be due to the modulatory effects of FPH on lipid and fatty acid metabolism–related genes, which were noted in turbot (Xu et al. 2016), barramundi (Chaklader et al. 2021), pompano (Pham et al. 2022), and mice (Bjørndal et al. 2013). Chaklader et al. (2021) reported that total fishmeal replacement by poultry by-product with the supplementation of FPH and black soldier fly Hermetia illucens larvae improved PUFA and MUFA in muscle.
Conclusion
The study demonstrated that supplementing 45 g/kg of SH negated the depressed growth effects caused by partially substituting fishmeal with MBM. Supplementing SH improved the growth performance, feed utilization, and essential fatty acid synthesis in giant trevally fed 50% of the dietary MBM protein and fishmeal-based diet. The intestinal health of the juvenile trevally also improved by adding 45-g/kg SH in MBM diet.
Data availability
The data used to generate the results in the paper are available from the corresponding author upon reasonable request.
Abbreviations
- FPH:
-
Fish protein hydrolysate
- GCs:
-
Goblet cell number
- MBM:
-
Meat and bone meal
- SH:
-
Shrimp hydrolysate
- TH:
-
Tuna hydrolysate
- SFA:
-
Saturated fatty acids
- MUFA:
-
Monounsaturated fatty acids
- PUFA:
-
Polyunsaturated fatty acids
- HUFA:
-
Highly unsaturated fatty acids
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Acknowledgements
We would like to thank the marine fishery hatchery in Nha Trang, Vietnam, that provided a culture system, giant trevally juvenile, and equipment for our research.
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Open Access funding enabled and organized by CAUL and its Member Institutions This work was supported by a PhD program of Curtin Malaysia Postgraduate Research Studentship (CMPRS).
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All authors contributed to the study conception and design. Diet preparation, experimental execution, data collection, and analysis were performed by Minh Chau Nguyen. Fish rearing and experimental work were supported by Duc Hung Pham. Ravi Fotedar supervised the experiment. The first draft of the manuscript was written by Minh Chau Nguyen and all authors commented on the previous version of the manuscript. All authors read and approved the final manuscript.
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An experiment was performed according to the Australian Code of Practice for the care and use of animals for scientific purposes, as approved by the Animal Ethics Committee of the Curtin University, Bentley, Australia (Permit Number: ARE2022-15).
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Nguyen, M.C., Fotedar, R. & Pham, H.D. Can shrimp hydrolysate improve the efficacy of meat and bone meal diet in juvenile giant trevally Caranx ignobilis?. Aquacult Int 32, 1909–1926 (2024). https://doi.org/10.1007/s10499-023-01250-0
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DOI: https://doi.org/10.1007/s10499-023-01250-0