Veterinary and Animal Science 25 (2024) 100381

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Veterinary and Animal Science

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Alternative protein sources in aquafeed: Current scenario and

future perspectives
Valentina Serra a,* , Grazia Pastorelli a , Doriana Eurosia Angela Tedesco b, Lauretta Turin a ,
Alessandro Guerrini b
a
Department of Veterinary Medicine and Animal Sciences, University of Milan, Via dell’Università 6, 26900 Lodi, Italy
b
Department of Environmental Science and Policy, University of Milan, Via Celoria 10, 20133 Milano, Italy

A R T I C L E I N F O A B S T R A C T

Keywords: Fish meal represents the main protein source for most commercially farmed aquatic species, as it is characterized
Aquaculture by high nutritional value and lack of anti-nutritional factors. However, its availability and the market price have
Novel protein sources been recognized as serious problems at least for over a decade, making it necessary to search for non-
Fishmeal replacement
conventional protein sources, as an alternative to fish meals. This review aims to comprehensively examine
Sustainability
and critically revise the use of fish meal and all alternative protein sources explored to date on the health,
Fresh-water fish
Salt-water fish welfare, and growth performance of the major aquatic species commercially interesting from a global scenario.
Animal health The investigation revealed that the inclusion levels of the different protein sources, plant- and animal-derived,
Fish nutrition ranged from 10 to 80 % and from 2 to 100 % respectively, in partial or complete replacement of fish meal,
and generated positive effects on health, welfare, growth performance, and fillet quality. However, the results
showed that above a certain level of inclusion, each protein source can negatively affect fish growth perfor­
mance, metabolic activities, and other biological parameters. Moreover, it is likely that by mixing different
protein sources, the combination of each ingredient causes a synergistic effect on the nutritional properties.
Therefore, the future of aquatic feed formulation is expected to be based on the blend of different protein sources.
Overall, the analysis highlighted the need for additional research in the field of replacing fish meals with new
protein sources, given that many knowledge gaps are still to be filled on aquatic species, which deserve to be
investigated.

1. Introduction calorie-protein ratios for human consumption (Melenchón et al., 2022).

Moreover, the increasing demand for seafood, recommended as healthy
Agricultural production will need to increase by 50 %, to satisfy the and sustainable, may be incompatible with ecological sustainability
growing demand for food according to the expected increase in the (Teixeira and Silva, 2024). Consumers play a key role, since based on
global population (9.7 billion people by 2050) (Hunter et al., 2017). their commercial choices they can promote sustainable fish farming
Moreover, the increasing consumption of animal-based foods, and the systems, which have now become essential to increase food production
improvement of the living standards in developing countries, will lead to as the global population increases.
increased global demand for sustainable animal proteins (Kim et al., Many fish reared for human consumption require high protein levels
2019). For these reasons, alternative feed protein sources will be to grow properly, and aquaculture has faced sustainability issues in
necessary to replace the current supply and satisfy the growing need. To recent decades. Fish meal (FM) is considered the ideal protein source in
address this need, research is exploring alternative protein sources for aquaculture, particularly for carnivorous species, because it is rich in
feed, as demonstrated by the increasing number of publications on such protein content, properly balanced with essential amino acid (AA)
topics in the monogastric, ruminant, and aquaculture species in the last profile, highly nutritive, and palatable. According to the FAO report
10 years (Fig. 1). (2022), 16 million tons of fish caught (9.03 % of the total) are used
Aquaculture represents one of the most important sources of animal directly for the production of FM and oil. The rapid growth of the
proteins for human nutrition. Fish grow rapidly and provide adequate aquaculture sector has significantly contributed to the increasing

* Corresponding author.
E-mail address: [Link]@[Link] (V. Serra).

[Link]

Available online 25 July 2024

2451-943X/© 2024 Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license ([Link]
V. Serra et al. Veterinary and Animal Science 25 (2024) 100381

demand for FM, which in turn has led to overfishing and subsequent Hermetia illucens, Tenebrio molitor, etc.); specific names of the macro­
destruction of aquatic ecosystems (Szczepanski et al., 2022). Total feed algae/microalgae, and single-cell protein were also searched in the da­
production for all fish species is estimated to increase by 75 %, from 49.7 tabases. The review was open to the inclusion of studies written in any
million tons in 2015 to 87.1 million tons in 2025 (Hua et al., 2019). The language (but with abstract written in English) in the last 10 years
shortage and the expensiveness of FM have made FM-based feed a reporting in vivo studies (on-farm field trials and experimental
limiting factor in the aquaculture industry, leading to the search for controlled trials) on the effects of different alternative protein sources on
alternative sources with high protein content and similar nutritional growth performance (improved growth, improved feed conversion ratio,
value (Irm et al., 2022). Ideal alternatives to FM should be characterized etc.), and studies that evaluated a mixture of other protein sources, also
by a suitable AA profile, high nutrient digestibility, and low fiber and in experimental trials with pathogens (challenge). The search delivered
carbohydrate content. Moreover, the price should be competitive, the a total of about 350 results. Having removed those results nonrelated to
environmental impact low, and the source should be fully available, and the topic, 205 articles were selected.
easy to use. Great efforts have been made to find alternatives to FM and
among them are terrestrial plant proteins, animal by-products, insect 3. Alternative protein sources to FM
meals, marine algae, and biomass, characterized by a valuable protein
content (Fig. 2) (Aragão et al., 2022). Most likely a combination of 3.1. Plant-protein sourced feedstuffs
different protein sources is better than a single protein source because
the mixture has a preferable AA profile, which results in better fish Plant protein sources are recognized as the main source to replace
growth performance. FM, due to their wide availability, reasonable cost (Kari et al., 2023),
The present review aims to comprehensively examine and discuss the and different AA compositions. A range of plant ingredients are used in
use of FM and all alternative protein sources explored to date on the the aquaculture industry including grains (wheat, corn etc.), oilseeds
health, welfare, and growth performance of major aquatic species of (soybean, sunflower, rapeseeds, cottonseed, etc.), and pulses (beans,
commercial interest from a global scenario. This work, evaluating the lupins, peas, etc.) (Obirikorang et al., 2020; Kaiser et al., 2022; Burducea
progress achieved in the last decade, and identifying the most sustain­ et al., 2022; Szczepański et al., 2022; Reis et al., 2019; Ogello et al.,
able alternative sources from both economic and environmental views, 2017).
will help the aquaculture sector to reduce the costs of feed. Finally, Despite these positive features, they show significant limitations;
possible future approaches based on innovative alternative protein Primarily, the presence of anti-nutritional factors (ANFs; phytate,
sources not authorized yet, are also suggested. trypsin inhibitors, and lectins for instance), generally affects palatability
and interferes with the efficient nutritional utilization of diets, thus
2. Research methodology leading to alteration of growth performance, immunity, and lead to
inflammation processes (Aragão et al., 2022). No less, it has been re­
The present review analyses the scientific papers reporting evidence ported that ANFs and carbohydrate fractions present in plant-based
of using alternative feed protein sources in the aquaculture sector. A proteins included in diets may alter the aquatic species’ digestion and
systematic search of the literature was performed in Minerva (access nutrient utilization (Murashita et al., 2019; Dossou et al., 2021). The use
point to the bibliographic resources available from the University of of these protein sources showed contradictory effects on aquatic species.
Milan), PubMed, Google Scholar, Scopus-Elsevier, Scifinder-n, and Some studies reported that high levels of dietary plant proteins tend to
ResearchGate to retrieve all available studies using the following search decrease feed intake (FI) and consequently a worsen growth perfor­
terms “alternative protein source”, and “protein feedstuff” followed by mance (Sharawy et al., 2016; Kari et al., 2022). Contrarily, several
the name of the animal species or zootechnical categories (i.e.: fish studies demonstrated that FM replacement with plant proteins did not
including Sparus aurata, larvae, juvenile, etc.), and “aquaculture”. Spe­ negatively affect the growth performance of animals (Valente et al.,
cific names of the alternative plant-protein sources (i.e. soybean meal, 2016), even reporting an improvement (Kari, 2023), reason why it
corn/wheat gluten meal, rapeseed, lupin, etc.); specific names of the would be desirable to combine different plant proteins to meet the
alternative animal-protein sources (i.e. blood meal, feather meal, nutritional needs of aquaculture species. In the following paragraphs,

Fig. 1. The number of publications on alternative protein sources in monogastric, ruminants, and aquaculture sectors since 2014.

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V. Serra et al. Veterinary and Animal Science 25 (2024) 100381

Fig. 2. Protein content (CP %, DM) of suitable alternative protein sources to replace fish meal (FM) in fish diets. FM: fishmeal; SBM: soybean meal; WGM: wheat
gluten meal; CGM: corn gluten meal; FBM: faba bean meal; LM: lupin meal; PBM: poultry by-products meal; FeM: feather meal; MBM: meat and bone meal; BM: blood
meal; HBP: haemoglobin powder.

the main effects of using different plant-proteins sources used in aqua­ process (Zulhisyam et al., 2020) (Fig. 3). Fermentation is a useful
culture nutrition will be illustrated and discussed. Table 2 summarizes a technique for removing compounds such as phenols, tannins, and phy­
selection of studies examining the effects of plant-proteins used as FM tates from plant-based feeds, and producing health-promoting biological
replacers on key aquaculture species. substances (Kari et al., 2023). Some authors suggest that the microbial
fermentation of plant ingredients could enhance the bioavailability of
3.1.1. Soybean and soybean by-products potential antioxidant compounds (e.g. glucosinolates and phenolics)
Soybean (Glycine max, L.) is an annual crop belonging to the Legu­ leading to improved anti-oxidative defense in fish (Zhang et al., 2023).
minosae family (Dei, 2011). Soybean, and particularly soybean meal In African catfish (Clarias gariepinus) fed with 50 % fermented soy
(SBM) are the source of plant proteins alternative to FM mostly used in pulp (FSP) in partial substitution of FM, an improvement in growth
aquafeed. SBM is an excellent source of balanced AAs (Table 1), rich in performance, associated with a significantly lower (desirable) feed
lysine (Lys), tryptophan (Trp), threonine (Thr), and isoleucine (Ile), conversion ratio (FCR) was observed (Kari et al., 2022). The authors
which are often scarce in cereal grains (Florou-Paneri et al., 2014). ascribed these results to the lactic acid fermentation that the soybean
Furthermore, soybean by-products (e.g. fermented SBM, soy pulp, soy­ by-product underwent, with consequent improvement in the nutritional
bean protein concentrate) represent a valuable replacement for FM, due value and elimination of feed allergens and ANFs (Kari et al., 2022).
to the lower amount of ANFs generated through the fermentation Similar beneficial effects were detected in Japanese seabass (Lateolabrax

Table 1
Amino acid profile (% DM) of different plant protein sources used as FM replacement in aquafeed summarized from references.
Amino acid SBM CGM CGM WGM PPI Fava bean RSM Untreated Fermented SFM CSF
L. albus L. albus

Arginine 3.86 2.01 2.52 2.73 6.3 9.46 2.21 3.29 - 2.24 5.87
Histidine 1.48 1.29 1.19 1.76 1.76 2.41 1.01 0.97 3.13 0.72 1.44
Isoleucine 2.04 2.54 2.35 3.67 3.34 3.94 1.53 1.31 2.44 1.18 1.44
Leucine 3.15 11.36 10.27 5.79 6.26 7.47 2.70 2.4 3.90 1.90 2.80
Lysine 3.19 0.93 1.18 1.38 5.12 7.08 1.95 1.54 5.98 1.07 2.15
Methionine 0.59 1.43 0.60 1.13 0.50 0.87 0.76 0.28 0.83 0.08 0.82
Phenylalanine 2.31 3.59 3.98 4.44 3.47 4.19 1.53 1.24 1.11 1.37 2.64
Threonine 1.76 2.17 2.5 2.13 2.64 3.40 1.76 1.25 6.92 1.10 1.50
Tryptophan - - 0.22 0.74 - 0.87 0.51 0.22 - - -
Valine 2.11 3.06 2.79 3.71 3.88 4.31 1.97 0.94 4.73 1.42 2.07
Alanine 2.11 5.76 5.80 2.11 2.97 4.15 1.71 1.06 7.85 1.30 1.59
Aspartic acid 5.36 3.83 4.71 - 8.55 10.74 2.83 3.42 5.88 3.12 4.85
Glutamic acid 10.12 19.23 14.22 - 16.73 16.51 6.03 7.05 21.84 6.09 13.75
Glycine 1.91 1.66 1.79 2.76 2.76 4.73 2.01 1.37 6.06 1.72 1.93
Proline 2.15 6.74 - 12.31 3.37 3.94 2.24 1.39 6.05 1.30 1.87
Serine 2.38 3.29 3.38 4.04 3.69 4.69 1.64 1.68 21.98 1.29 2.23
Tyrosine 1.66 3.42 3.40 2.95 2.34 2.78 - 0.915 1.32 0.65 1.44
Cystine - 1.05 0.62 1.71 0.63 1.33 0.91 0.64 - 0.16 0.94
Reference Li Wang Santizo-Taan Kar Wang Martineau-Côté Mosenthin Ritter Krunglevičiūtė Shi Wang
et al., et al., et al., 2020 et al., et al., et al., 2022 et al., 2016 et al., 2022 et al., 2016 et al., et al.,
2022 2020a 2016 2020a 2023 2020c

Abbreviations: CSF: cotton seed flour; CGM: corn gluten meal; PPI: pea protein isolate; RSM: rapeseed meal; SBM: soybean meal; SFM: sunflower meal; WGM: wheat
gluten meal.

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Table 2
Plant-protein sources as a substitute for FM in the diet of different aquatic species.
Alternative Aquatic species Inclusion level FM inclusion Time Effects Reference
protein source in the control (weeks)
diet

SBM; Nile tilapia 565 g/kg SBM; 355 g/kg 8 Performance: highest FBW in CGM+SBM+B; Ismail et al., 2020
CGM; (O. niloticus) 565 g/kg SBM + 2 lower FBW in SBM, CGM and CGM+SBM than
SBM + CGM, g/kg B (SBM + B); FM basal diet; Intestinal histomorphology: ↑
with or 359 g/kg CGM; intestinal villi length and number of goblet cells
without 359 g/kg CGM + 2 in SBM+B, CGM+B, SBM+CGM+B groups;
betaine (B) g/kg B (CGM + B); Blood haematology and biochemistry: ↑ HB,
106 g/kg CGM + blood total protein in CGM+B, SBM+CGM,
400 g/kg SBM SBM+CGM+B; highest blood RBCs, WBCs, and
(CGM + SBM); globulin in SBM+CGM+B; Gene expression: ↑
106 g/kg CGM + LPL and FAS in SBM, CGM, SBM+CGM; ↑ IGF-1
400 g/kg SBM + 2 in SBM+B, CGM+B, SBM+CGM+B than SBM or
g/kg B (CGM + CGM.
SBM + B)
PCM Nile tilapia 125 g/kg (PCM1); 29 % DM 5 Performance: ↓ in FBW in PCM3 and PCM4; no Mohammadi et al.,
(O. niloticus) 250 g/kg (PCM2); difference in FCR, FI and ADC of protein; 2020
375 g/kg (PCM3); Digestive enzymes activity: no difference in
500 g/kg (PCM4) lipase, alkaline protease and amylase activity; no
difference in mucosal LYS, ALPR and ALP
activities and total IG content; Liver
antioxidative status: no difference in CAT,
SOD, GPx and MDA; highest gene expression of
liver GPx and CAT in PCM4; highest expression
of SOD in PCM3; Histology: intensive intestinal
and hepatic mononuclear immune cell
infiltration, lamina propria expansion and
intestinal villus detachment and shortening in
PCM3 and PCM4.
CGM Rainbow trout 9 % CGM; 16 % DM 24 Performance: no difference in FBW, TCG and Saez et al., 2016
(O. mykiss) 18 % CGM FE; Muscle colour: ↓ Astaxanthin isomer, all-
trans astaxanthin and all-trans lutein in response
to increasing levels of CGM; ↓ Redness (a*) and
Chroma (C*ab).
LM Rainbow trout 150 g/kg LM 62 % DM 8 Performance: ↓ FBW in LM45 and LM60; ↓ FI in Acar et al., 2018
(O. mykiss) (LM15); LM60; Blood parameters: ↓ Hematocrit value in
300 g/kg LM LM30, LM45, LM60; no differences in HB, RBC
(LM30); and MCH rates; no differences in GLU, GOT, GPT;
450 g/kg LM ↓ ALP and LDH in all groups than the control.
(LM45);
600 g/kg LM
(LM60)
RL; Atlantic salmon 15 % RL (RL15); 562 g/kg 8 Performance: no differences in whole-body Rodríguez-Estrada
FL (S. salar) 15 % FL (FL15); composition; ↑ FBW, WG, SGR and PER in FL15; et al., 2020
30 % RL (RL30); Nutrient apparent digestibility: ↑ ADC of
30 % FL (FL30) protein and nitrogen-free extract in FL15;
Immune response: ↑ LYS activity and leucocyte
respiratory burst in FL15.
PPP Common carp 10 % PPP (T2); - 12 Performance: ↑ WG, ADG and SGR in T3; ↓ FCR Tewari et al., 2019
(C. carpio) 20 % PPP (T3); in T3
30 % PPP (T4)
CGM Common 5.4 % CGM 27 % DM 8 Performance: ↑ FBW in CGM100; ↓ FBW in Potki et al., 2018
carp (CGM20); CGM20; no difference in HSI; no difference in
(C. carpio) 10.8 % CGM LPV; ↑ PPV in CGM20 than the other groups;
(CGM40); Hematological parameters: No difference in
16.2 % CGM RBC number; ↑ CHO level in CGM80; no
(CGM60); difference in MCV, MCH, MCHC, GLU.
21.6 % CGM
(CGM80);
27 % CGM
(CGM100)
RM + Chlorella Crucian carp 99.6 g/kg RM + 520 g/kg 6 Performance: ↑ WGR, SGR, FI and PE with Shi et al., 2017
meal (CM) (C. auratus gibelio) 99.6 g/kg CM increasing RCM inclusion level; Intestinal
(RCM25); digestive enzymes: no difference in amylase
199.2 g/kg RM + activity; ↑ trypsin and lipase in RCM75 and
199.2 g/kg CM RCM100; ADCs: ↑ DM, CP, CL and ash with
(RCM50); increasing RCM inclusion level; ↓ ADC values of
298.8 g/kg RM + most AAs in control diet than RCM50, RCM75
298.8 g/kg CM and RCM100 diets; Histology of anterior
(RCM75); intestine: no significant difference (similar
398.4 g/kg RM + appearance, including intact intestinal mucosal
398.4 g/kg CM epithelium, well-organized villi, thickness of
(RCM100) tunica muscularis and length of villi).
(continued on next page)

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Table 2 (continued )
Alternative Aquatic species Inclusion level FM inclusion Time Effects Reference
protein source in the control (weeks)
diet

CGM Indian major carps (Catla 25 % CGM (CGM1); 45 % DM - Performance: mean monthly WG highest in Karim and Shoaib
catla, Labeo rohita, Cirhinus 35 % CGM (CGM2); CGM3; maximum ADG in Cattla cattla in all (2018)
mrigala) 45 % CGM (CGM3) treatments.
FBM “Crispy” grass carp 630 g/kg (FBM70); 3 % DM 14 Performance: ↓ FBW, WG, SGR and VSI in all Fu et al., 2022
(Ctenopharyngodon idella) 720 g/kg (FBM80); groups than control; Morphology of myofiber:
810 g/kg (FBM90); ↑ myofiber area and radius in all groups than
900 g/kg (FBM100) control; ↓ myofiber space in all groups than
control; mRNA expression: ↑ col1a1, col1a2,
fgf6a and fgf6b in FBM70 muscle.
CGM; Chinook salmon 59 % fish meal (FM) 59 % 56 Performance: no difference in FBW Doughty et al., 2019
PBM (Oncorhynchus (HighFM); (HighFM);
tshawytscha) 15 % FM + 16 % 15 %
PbM + 28 % CGM (LowFM)
(LowFM)
PPC Juvenile tench 285 g/kg PPC 645 g/kg 13 Performance: no difference in total length and Carral et al., 2021
(T. tinca L.) (PPC35); weight; no difference in survival rate; SGR and
366 g/kg PPC FCR significantly lower in PPC75 and PPC85.
(PPC45);
487 g/kg PPC
(PPC60);
608 g/kg PPC
(PPC75);
685.4 g/kg PPC
(PPC85)
CGM Turbot (Scophthalmus 212 g/kg (CGM20); 620 g/kg 8 Performance: dose-dependent ↓ in growth Bai et al., 2019
maximus) 318 g/kg CGM performance, nutrient digestibility, and feed
(CGM30); utilization; Intestinal cytokines: ↑ IL-1β, IL-8,
426 g/kg CGM TNF-α and TGF-β gene expression with the rise in
(CGM40) the CGM level; Electron microscopic structure
of the distal intestine: significantly shorter and
less dense microvilli in CGM40; ↑ infiltration of
leucocytes from the submucosa to the epithelium
layer in CGM40 compared to control; Oxidant
and antioxidant indices: ↑ MDA level with the
rise in the level of CGM; ↓ SOD, CAT, GPX, GR
and GSH levels with the rise in the level of CGM;
Intestinal immune parameters: ↓ ACP, C3 and
C4, IgM level with the increasing levels of CGM.
CGM; PPI Black sea bream 135 g/kg CGM 660 g/kg 8 Performance: ↓ WG of CGM40 than the other Wang et al., 2020a
(Acanthopagrus (CGM20); treatments; Feed utilization: no difference;
schlegelii) 120 g/kg PPI Haematological parameters: significantly
(PPI20); lower content of serum CHO in CGM40; ↑ liver
70 g/kg CGM + 60 ALT activity in CGM40 than PPI20.
g/kg PPI (CPP20);
270 g/kg CGM
(CGM40);
240 g/kg PPI
(PPI40);
130 g/kg CGM +
125 g/kg PPI
(CPP40)
FRM Sea bream (Pagrus major) 18.75 % (FRM1); 47 % DM 9 Performance: ↓ FBW, WG, SGR, FI in FRM4; Dossou et al., 2018
37.5 % (FRM2); Blood parameters: No difference in GLU, T-Pro,
56.25 % (FRM3); CHO, TG, BUN, T-Bill, GPT; ↓ d-ROMs in FRM1,
75 % (FRM4) FRM2 and FRM3; ↑ BAP values in FRM0, FRM1
and FRM2; ↓ CAT in FRM4; Immunological
parameters: no effect on serum LYS and total
peroxide.
LKM Whiteleg shrimp 100 g/kg LKM 250 g/kg 8 Performance: ↑ FBW in control and L10; ↓ FBW Weiss et al., 2020
(Litopenaeus vannamei) (L10); in L30; Haemolymph parameters: ↑ GLU in L10
200 g/kg LKM than L30; no difference in total haemolymph
(L20); protein; ↓ acylglyceride in L30; ↑ phenoloxidase
300 g/kg LKM activity in L10.
(L30)
PPC Sharpsnout 160 g/kg (PPC16); 550 g/kg 8 Performance: ↓ FBW with increasing PPC Nogales-Merida
sea bream 320 g/kg (PPC32); inclusion level; no difference in FCR, FI, PER et al., 2016
(Diplodus puntazzo) 487 g/kg (PPC48) across PPC levels;
↓ HSI in PPC48 compared to control; no
difference in PPV and EPV; no difference in AAs
composition of muscle; Liver histology: no
difference in liver nuclei, liver hepatocyte
cytoplasm, hepatocyte vacuolisation or
pancreatic acinar cells; Intestine histology:
longest villous length in PPC48 (posterior
(continued on next page)

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Table 2 (continued )
Alternative Aquatic species Inclusion level FM inclusion Time Effects Reference
protein source in the control (weeks)
diet

section); widest lamina propria and muscularis

thickness in PPC48 (anterior section); greatest
villus width in PPC32 (mid intestine).

Abbreviations: ↑: improvement; ↓: decrease; AAs: amino acids; ACP: acid phosphatase; ADC: apparent digestibility coefficient; ALPR: alkaline protease; BAP: bio­
logical antioxidant potential; C3: complement 3; C4: complement 4; CAT: catalase; CGM: Corn gluten meal; CHO: cholesterol; CL: crude lipid; CP: crude protein; d-
ROMs: Reactive oxygen metabolites; DM: dry matter; EPV: energy productive value; FAS: fatty acid synthase; FBW: final body weight; FCR: feed conversion ratio; FI:
feed intake; FL: fermented lupin; FM: fishmeal; FRM: fermented rapeseed meal; GLU: glucose; GOT: glutamic oxaloacetic transaminase; GPT: glutamic pyruvic
transaminase; GPx: glutathione peroxidase; GR: glutathione reductase; GSH: reduced glutathione; HB: haemoglobin; IG: immunoglobulin; IGF: insulin like growth
factor; IL-8: interleukin 8; Ile: isoleucine; LDH: lactate dehydrogenase; Leu: leucin; LM: lupin meal; LKM: lupin kernel meal; LPL: lipoprotein lipase; LPV: lipid pro­
ductive value; LYS: lysozyme; MCHC: mean corpuscular hemoglobin concentration; MCH; mean corpuscular haemoglobin; MCV: mean corpuscular volume; MDA:
malondialdehyde; PBM: poultry meal; PCM: processed canola meal; PER: protein efficiency ratio; PPC: pea protein concentrate; PPI: pea protein isolate; PPP: pea pod
powder; PPV: protein productive value; RBCs: red blood cells; RL: raw lupin; SBM: soybean meal; SBMIE: soybean meal-induced enteritis; SGR: specific growth rate;
SOD: superoxide dismutase; TCG: thermal growth coefficient; T-Bill: total bilirubin; T-Pro: total serum protein; TG: triglyceride; VSI: viscerosomatic index; VW: villous
width; WBCs: White blood cells; WG: weight gain; WGR: weight gain ratio.

Fig. 3. The fermentation process of soybean meal.

japonicus) fed 40 % fermented SBM, whilst worse growth performance improving growth rate (Howlader et al., 2023). Commonly, an amelio­
was observed when the percentage of inclusion exceeded 80 % ration in growth performance and positive effects on blood hematology
(Rahimnejad et al., 2019). The effects of fermented and un-fermented were correlated with an improvement in gut morphology. The
soybean by-products in the fish diet on growth performance have also above-mentioned study conducted by Howlader and colleagues (2023)
been correlated with changes in health parameters, such as immunity, demonstrated an increase in the intestinal shape (villi) of stinging catfish
stress, blood biochemical indices, bio-availability of micronutrients, gut by adding SBM up to 50 % in the diet and a decline by adding up to 75 %.
morphology, and finally fish fillet composition (Fig. 4). In particular, the intestinal villi were increased in length, width, area,
The partial replacement of FM with fermented SBM or pulp enhanced and thickness. Moreover, the partial (50 %) replacement of FM with FSP
the innate immunity, along with an increase of lysozyme activity, total caused positive pathomorphological changes in the African catfish gut,
antioxidant capacity (TAC), and specific antioxidant enzyme activity as an intact epithelial barrier with a very well-organized villus structure,
(superoxide dismutase-SOD and catalase-CAT) (Rahimnejad et al., 2019; tunica muscularis, and goblet cell arrangement (Kari et al., 2021). Other
Zhang et al., 2021). Reduced production of the pro-inflammatory cyto­ authors reported gut disturbances for salmonids (Nimalan et al., 2022),
kines (IL-1β, IL-6, IL-12, IL-32, and TNF-α) in the intestine and liver yellowtail (Viana et al., 2019), turbot (Liu et al., 2019), northern
(Zhang et al., 2021), and increased expression of genes regulating snakehead (Miao et al., 2018), and Japanese seabass (Zhang et al., 2018)
growth and immunity (TGF-β1, lyzg, NF-kβ, and hsp90α) were also re­ after the dietary inclusion of SBM at percentages above 10 %, probably
ported (Kari et al., 2022). due to the presence of ANFs, which cannot be completely removed by
The improvement of the antioxidant capacity and the reduction of the thermal processes. Studies also reported alterations in liver func­
inflammatory markers due to the use of soybean by-products can also tionality in fish fed soybean by-products, as evidenced by Yaghoubi and
affect directly the blood biochemical indices (Bonvini et al., 2018). For colleagues (2016). Silvery-black porgy juveniles (Sparidentex hasta) fed
example, at 75 % FM replacement with SBM, the glucose (Glu) was with different levels of SBM (0-340 g/kg diet) and isolated soy protein
significantly higher in stinging catfish (Heteropneustes fossilis) compared (0-210 g/kg diet), showed liver damage with a marked increase of
to other treatment groups fed with 0, 18, or 36 % of SBM; this was alkaline phosphatase (ALP) enzymes, but a reduction in plasma alanine
associated with an increase of BW due to the augmented hemoglobin aminotransferase (ALT) and aspartate aminotransferase (AST) levels
(Hb), which allowed a better transport of oxygen into the tissues, thus when fermented soybean replaced 20, 40 and 60 g/kg of SBM in the diets

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V. Serra et al. Veterinary and Animal Science 25 (2024) 100381

Fig. 4. Effects of FM alternative protein sources on fillet quality. CP: crude protein; CF: cride fibre; DM: dry matter; DHA: decosahexaenoic acid; EPA: eicosa­
pentaenoic acid; MUFA: monounsaturated fatty acids; PUFA: polyunsaturated fatty acids; SFA: saturated fatty acids.

of largemouth bass (Micropterus salmoides) (Jiang et al., 2018). the wheat gluten meal (WGM), obtained after starch extraction from
grains. Due to its low Lys content and high digestibility of the protein
3.1.2. Corn/wheat gluten meal fraction, it is suitable for use as a feed ingredient in aquatic species
Corn gluten meal (CGM), a corn starch by-product, represents the (Bonaldo et al., 2015), typically salmonids, whose diet can include WGM
main protein fraction obtained from the wet milling process for the in replacement of FM up to 35 % without adverse effects (Storebakken
separation of the starch, germ, protein, and fiber corn components. This et al., 2000). The replacement of FM up to 30 % with CGM and fer­
by-product is characterized by protein content of 67-71 %, low fiber mented SBM did not show differences in growth performance and feed
content, and absence of ANFs (Kopparapu et al., 2022); however, is poor utilization in olive flounder (Paralichthys olivaceus), with any effects on
in essential AAs such as Lys and Trp (Table 1). Due to its insolubility in the immune system (Seong et al., 2018). However, as reported for other
water, CGM can be subjected to various physical and chemical processes plant protein sources, a reduction of the growth rate and feed efficiency
aimed at increasing its solubility and digestibility and therefore was observed with a replacement higher than 80 % of FM with CGM in
expanding its applications in food and feed industries (Huang et al., juvenile spotted rose snapper (Lutjanus guttatus) (Hernández et al.,
2024) (Fig. 5). 2021). An increasing level of dietary CGM caused a significant reduction
Another by-product rich in protein content (75 %), is represented by in Hb and hematocrit value, with an increase in triacylglyceride levels.

Fig. 5. Different modifications of corn gluten meal (CGM).

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V. Serra et al. Veterinary and Animal Science 25 (2024) 100381

These results were explained by an up-regulation of genes involved in as Nile Tilapia (Oreochromis niloticus) (Chien and Chiu, 2003), and
the triacyl-glyceride synthesis, similar to the up-regulation of genes common carp (Anwar et al., 2020), showed no adverse effects on growth
involved in lipogenesis in rainbow trout fed gelatinized starch reported performance, physiological status, and gut integrity when white and
by Song and colleagues (2018). Another adverse effect was noticed in blue lupin were added in the diet.
Atlantic salmon fed with 30 % WGM, as symptoms similar to gluten
sensitivity in humans. This correlated with an up-regulation of chole­ 3.1.5. Faba bean (Vicia faba, L.)
cystokinin genes, which regulate FI and replacement, and might be Faba bean (FB) belongs to the Fabaceae family and is an annual crop
caused by a gluten-induced metabolic intestine disorder (Johny et al., cultivated worldwide, sown in autumn or in spring and, even though
2020). primarily grown for its edible seeds (beans), also used as a whole crop.
FB is an important food and feed legume due to the high nutritional
3.1.3. Rapeseed and rapeseed by-products value of its seeds, which are plentiful of proteins (25-33 % DM) and
Rapeseed (Brassica napus, L.) is one of the most important oil crops in starch (40-48 % DM), thus representing a valuable source of protein and
the world, ranking fifth after soy, cotton, peanuts, and sunflower energy for livestock (Guevara Oquendo et al., 2022)). Despite being rich
(Lafarga, 2021). It is commonly known as canola (Canadian rapeseed 00 in protein, carbohydrates, fats, and minerals, FB seeds contain a variety
variety) (Kaiser et al., 2022), primarily cultivated for oil extraction, and of ANFs, such as vicine and convicine, well-known to cause the favism
the meal that remains after this process is a rich source of protein syndrome (Rizzello et al., 2016).
(around 36-50 %) (Thiyam et al., 2004; Muranova et al., 2017). In aquaculture, FB diet inclusion at different percentages (40, 50, 60,
Therefore, it may be used either as a high protein feed supplement and 70 %) in Nile Tilapia revealed a decrease in BW proportional to the
especially in cattle, poultry, and aquatic animals, or as organic fertilizer. increase of FB inclusions (Li et al., 2023). However, FB was evaluated as
Rapeseed meal (RM) production has increased steadily over the last few a replacement for SBM. In juvenile grass carp (Ctenopharyngodon idella)
years, making it the second major oilseed meal produced worldwide was demonstrated that FB could be used as a partial substitute for SBM at
after SBM (Patrick and Andre, 2014). However, the presence of ANFs (e. inclusion levels up to 420 g/kg without affecting the growth perfor­
g. glucosinolates, erucic acid, tannins, sinnapine, phytic acid, and mance, whilst a higher inclusion level (560 g/kg) negatively impacted
indigestible carbohydrates) limits its inclusion level as FM replacer in (Gan et al., 2017).
diets usually not above 10-20 % (Sallam et al., 2021). Despite all
treatments applied to reduce ANFs and to increase CP content, rapeseed 3.1.6. Pea (Pisum sativum L.)
protein products were only sporadically used to replace FM in aquatic Pea belongs to the Fabaceae and Papilionoïdeae phylogenetic group
feeds without adverse effects on fish’s growth performance (Kaiser et al., like soybean (Fischer et al., 2020). Raw peas are relatively low in ANFs
2022). To overcome this problem, Kaiser and colleagues (2021) devel­ compared to dry edible beans, including protease inhibitors, tannins,
oped processing methods to reduce nitrogen-free extracts as well as lectins, and phytate (Iji et al., 2017). Compared to protein-rich soybeans,
ANFs of rapeseed, simultaneously increasing protein content. The peas are legumes with relatively lower protein content, which ranges
resulting highly purified rapeseed protein has been used in diets (66 % from 18 to 33 % (Walter et al., 2022). Nevertheless, with a lower content
replaced of FM) of rainbow trout, without negative effects on growth of sulfur amino acids and less protein digestibility, pea has a lower
performance. However, positive effects on growth performance and nutritional value than, for example, soybeans. Moreover, peas contain
antioxidant defense (increase in lysozyme, bactericidal, and peroxidase more AAs involved in off-flavor development, such as Leu (3.5 vs 6.6 g
enzymes activities), were evidenced in red sea bream (Pagrus major) amino acid/100 g protein for pea and soybean), Ser (2.5 vs 4.8 g/100 g
when fed with FM substituted up to 50 % with different percentages of protein for peas and soybean), and Thr (1.6 vs 3.6 g/100 g protein for
fermented RM (25, 50, 75, and 100 %), being best 25 % (Dossou et al., pea and soybean), making them a less appreciated product (Fischer
2018). et al., 2020) (Table 1).
Pea is a common FM replacement for marine and freshwater species.
3.1.4. Lupin (Lupinus L.) Aside from pea meal, a valuable alternative to FM is represented by pea
Lupin belongs to the Fabaceae family, and the genus Lupinus includes pods, a food waste of high interest as it is environmentally friendly and
267 botanical species; however, only four of these are cultivated in able to reduce production costs. Furthermore, pea protein concentrate
different pedo-climatic areas, namely white lupin (L. albus), blue lupin can be used as an FM protein replacer in fish feed formulation. It was
(L. angustifolius), yellow lupin (L. luteus), and pearl lupin (L. mutabilis) reported that the addition of 20 % pea pod powder in the common carp
(Abraham et al., 2019). The use of lupin in animal nutrition is not that diet determined higher WG, specific growth rate, and lower FCR, thus
frequent, due to its low palatability and the presence of ANFs, such as demonstrating the efficiency of this by-product in determining better
non-starch polysaccharides, oligosaccharides, hemicellulose, cellulose, growth performance (Tewari et al., 2019). Also in rainbow trout,
especially neutral detergent fiber (NDF), and acid detergent fiber (ADF) lumpfish (Cyclopterus lumpus), and tench (Tinca tinca), 25 %, 35 %, and
that affect the nutritional characteristics and reduce the nutrients di­ 50 % of FM replacement with a pea protein concentrate did not interfere
gestibility (Struti et al., 2020; Parrini et al., 2023). The protein value of with the fish growth (Demirci et al., 2021; Willora et al., 2020;
lupin is comparable to the ones of SBM, peas, or other legume grains González-Rodríguez et al., 2016a). However, also in these cases, a
(Sujak et al., 2006), especially after dehulling (De Vries et al., 2012). The higher pea protein inclusion caused harsh histopathological changes in
lupin’s hull represents about 15-30 % of the seed weight, and its me­ the liver of rainbow trout (Demirci et al., 2021), and affected the growth
chanical removal contributes to an increase in nutritional value in rate of juvenile tench when the percentage of inclusion was above 35 %
particular in the level of protein (31.1 and 54.4 % DM). Whole lupine probably due to the presence of ANFs (González-Rodríguez et al.,
seeds are characterized by a variable AA profile, rich in Leucine (Leu), 2016a).
Valine (Val), Thr, Ile, and Serine (Ser), but poor in Trp and sulfur AAs
such as Methionine (Met) and Cystine (Cys) (Table 1). 3.1.7. Other oilseeds used as fish meal replacer
In aquaculture, the use of lupin as an FM alternative is still under Sunflower meal (SFM) is a by-product that remains in large quanti­
investigation. The few studies available in literature report that a per­ ties after the oil is extracted from sunflower seeds. SFM is a rich source of
centage of 75 % of FM replaced with 51 % of lupin meal or a dose of 21 % protein (290-340 g/kg) for fishes, and, due to the price lower than that
of lupine kernel meal in Barramundi fish (Lates calcarifer) and juvenile of SBM and high palatability, it is primarily used as a low-cost protein
cobia (Rachycentron canadum) diet respectively, caused liver steatosis, and energy source for all classes of animals (Banjac et al., 2021; Shi
kidney necrosis and gut damage, resulting in worse growth performance et al., 2023). The content of sulfur-containing AAs in sunflower flour is
(Siddik et al., 2021; Pham et al., 2020). However, some fish species such lower than in SBM, but other AAs are more balanced, especially

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glutathione and aspartic acid (Table 1). Using SFM as an FM/SBM tested (19.7 and 39.5 %), as improved the final body weight (FBW) and
replacer has produced good results in different aquatic species. Chris­ SGR of fish, together with no adverse effect on serum parameters (i.e.
topher et al. (2020), obtained an improvement in the growth perfor­ white blood cells, glucose, total protein, and phosphorus) (Emre et al.,
mance of tilapia when different percentages of SFM (10, 20, and 30 %) 2018).
were included in the diet in partial substitution of SBM. In particular, Linseed (Linum uistatissimum L.) is a cold-season annual plant, pro­
optimum growth and feed utilization were observed when SFM was duced in southern Brazil. Linseed meal is obtained after oil extraction as
included up to 30 % (best results for FCR, feed efficiency ratio (FER), and a by-product which has a high protein content (300 g/kg on average). Its
specific growth rate (SGR)). In the same aquatic species, SFM was tested high fiber concentration limits its use in aquaculture nutrition since it
as an FM replacer for 210 days at diet inclusion levels from 64.75 to 259 can compromise the availability and utilization of food nutrients
g/kg (Ogello et al., 2017) for growth performance and meat quality of (Pianesso et al., 2020). The production of linseed protein concentrate
fish. The high growth performance was obtained with the supplemen­ (LPC) allows the obtainment of a product with higher protein content
tation of 64.75 g/kg SFM (25 % FM replacing), while the reduced and reduced ANFs, thus potentially increasing its inclusion in the diets.
growth found when SFM levels were higher could be related to imbal­ Given that most of the studies available from the literature on linseed
ances of dietary AAs such as phenylalanine and methionine and high address the use of its oil, considered an alternative lipid source to fish
levels of fiber that limit nutrient bioavailability (Ogello et al., 2017). oil, these will not be considered in the context of the present review. In a
Regarding the meat quality, the protein content decreased with study conducted on silver catfish, four diets containing different levels
increasing levels of SFM, probably because of changes in protein syn­ (45.8, 91.6, 137.4, and 183.2 g/kg diet) of LPC in partial substitution of
thesis, and different growth rates, while the higher fiber and ash con­ FM were tested (Pianesso et al., 2020). The results showed that LPC has
tents were observed in the group fed with the highest SFM level (Ogello FM-equivalent nutritional quality and can replace FM up to 400 g/kg
et al., 2017). FM could be replaced by SFM at 12.9 % of inclusion, with without causing metabolic and histological damage that affects the
no significant adverse effects on growth and feed utilization in juvenile growth and nutrient utilization of fish. The authors did not report dif­
turbot (Scophthal musmaximus L.), as well as without negative effects on ferences in the protein and fat body deposition of the LPC-fed fish, thus
antioxidant parameters (the lowest MDA level and highest TAC, SOD, demonstrating that this protein source did not interfere with energy
and CAT activities in fish fed 12.9 % SFM) (Zhou et al., 2016). Similarly, metabolism. Likewise, evaluation of the animals’ plasma revealed sim­
in grass carp (Ctenopharyngodon idellus) it was found that the substitu­ ilarities in total protein, albumin, and glucose content, indicating that
tion of > 50 % SBM with SFM had significant negative effects on the the nutrients were metabolized without compromising hepatic synthe­
weight gain ratio (WGR) and FCR of fish (Shi et al., 2023). The incom­ sis. Another linseed by-product is deoiled linseed oil cake (LOC), which
plete decortication of SFM and the high content of crude fiber and contains a high amount of crude protein (34 % dry weight) and for this
indigestible lignin can reduce the rate of utilization and the nutritional reason, is a good candidate as an FM substitute. Raw and fermented LOC
value of raw materials by delaying gastric emptying, so it is advisable to were tested at different concentrations replacing FM at 10, 20, 30, and
limit high percentages of SFM in diets. 40 % in the diet of rohu (Labeo rohita) for 70 days (Banerjee et al., 2023).
Cottonseed meal (CSM) has been studied as a potential alternative The results indicated that fermented LOC can replace up to 30 % of FM
ingredient to both FM and SBM due to its lower cost, and better palat­ in rohu diets without compromising the growth and nutrient utilization,
ability, although the protein content can be variable (23–53 %) as fish fed fermented LOC showed better performance in terms of higher
depending on how this product is processed (Hassaan et al., 2019). The mean WG, SGR, and PER compared with the fish fed diets with the same
imbalance of AAs (Table 1) and the presence of ANF represent the main level of raw LOC; the poor growth of fish fed raw LOC was probably due
factors that limit their incorporation into aquatic feed; it is recom­ to AA imbalance and reduced bioavailability of the nutrients as a
mended that low levels of CSM be included in the aquafeeds (Kumar consequence of ANFs. The carcass composition was influenced by LOC
et al., 2014). A trial of 90 days performed on South Asian carp (Catla supplementation, as the higher protein deposition was recorded in fish
catla) investigated the effects of the replacement of SBM with CSM at fed fermented LOC. The considerable increase in digestive enzyme ac­
different percentages (6.25, 12.50, 18.75, and 25 %) on different bio­ tivity in fish fed fermented LOC was most likely due to the more efficient
logical traits (Aslam et al., 2023). According to the results obtained, it utilization of the nutrients than the fish fed with raw LOC. The incor­
was recommended to use a maximum of 50 % CSM as SBM replacement poration of fermented LOC for partial replacement of FM in carp diets
in the diet of C. catla to maintain optimal growth performance and other should be considered, as it would be cost-effective (much cheaper than
biological parameters, such as antioxidant indices (reduction of MDA FM) and it involves a simple processing technique. Its use should also be
and SOD value), intestinal enzyme activity (decrease of amylase, pro­ evaluated in other aquatic species.
tease, and lipase activity), and intestinal morphology (reduction in the Among pumpkin (Cucurbita maxima) by-products is seed cake (PSC),
villus height/villus width ratio). Poor nutrient assimilation due to al­ which is produced after the extraction of oil from seeds and is charac­
terations in intestinal morphology may have caused the reduced growth terized by the richness in protein, fiber, and minerals (Mounes et al.,
performance observed with high levels of CSM (Aslam et al., 2023). 2024). PSC has proven to be a promising, and cost-effective alternative
Similarly, the same percentage of FM replacement (50 %) was suggested protein source to SBM for Nile tilapia, as its inclusion at different con­
in the study conducted by Wang et al. (2020c), where different per­ centrations (33.5, 67, 100.4, and 133.9 g/kg diet) significantly
centages of CSM (8.5, 17 and 25.5 %) were supplemented to red drum enhanced growth performance, feed conversion, antioxidant capacity,
(Sciaenops ocellatus) diet to partially replace FM and investigate the ef­ and immunity (Mounes et al., 2024). In particular, fish fed the diet with
fects on performance and body composition of fish (Wang et al., 2020c). the highest PSC inclusion level exhibited the greatest improvements in
Results demonstrated that CSF could replace up to 50 % of crude protein FBW, BWG, SGR, and FCR, as well as the lower concentration of total
provided by FM in diets without significantly affecting growth perfor­ cholesterol, triglyceride, ALT, AST, creatinine, and urea, thus demon­
mance or whole-body composition; conversely, higher dietary levels of strating a hepatoprotective and nephroprotective effect exerted by PSC.
CSM decreased weight gain and feed efficiency, probably because of the The active biomolecules present in PSC may have triggered the antiox­
reduced palatability typical of plant protein feedstuffs (i.e. presence of idant defense of fish, by increasing the activity of antioxidant enzymes
ANFs such as gossypol in the case of cotton seed) (Wang et al., 2020c). It (e.g. CAT, SOD, and GPx) and reducing the MDA lipid oxidation in all
is worth underlining that red drum appears to have lower sensitivity to PSC-supplemented groups (Mounes et al., 2024). Similar results were
the ANFs present in alternative protein sources when compared to other obtained from the study by Sezgin and Aydın (2021), who found that
carnivorous fish (Minjarez-Osorio et al., 2016). In Russian sturgeon increasing levels (126.5, 253, 380 g/kg diet) of PSC in the diets of mirror
(Acipenser gueldenstaedtii), the inclusion of CSM as FM replacement is carp (Cyprinus carpio) led to a decrease in both cholesterol and triglyc­
more efficient than the inclusion of SBM at both the inclusion rates eride levels, with a continued effect on cholesterol until 100 % inclusion

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V. Serra et al. Veterinary and Animal Science 25 (2024) 100381

was reached after 63 days of feeding trial. Additionally, fish fed 253 (ABPs) (Categories 1, 2, and 3), of which, under European law, only
g/kg of PCS in the diet exhibited higher FBW, WG, and SGR than fish fed Category 3 by-products may be used to produce processed animal pro­
the control diet (Sezgin and Aydın, 2021). The supplementation of teins (PAPs) for aquaculture and aquafeed purposes (Reg. EC 1774/2002
different concentrations (2, 4, 6 g/kg) of pumpkin seed meal (PSM) in (European Union Regulation, 2002).
Mozambique tilapia (Oreochromis mossambicus) for 28 days determined Poultry by-product meal (PBM), which was re-authorized for use by
a significant increase in FCR, SGR, FE, and PER (Musthafa et al., 2017). the European Union in 2013 (European Commission et al., 2013), and is
The PSM integration also enhanced the immune response of fish fed 4 obtained from rendered and clean by-products of the poultry processing
and 6 g/kg of C. mixta, as the complement activity was significantly industry, and may include head, neck, feet and undeveloped eggs,
increased, and the mortality caused by the pathogen Aeromonas hydro­ exclusive of feathers and intestines. The poultry production industry
phila was reduced in these fish groups than in the control group generates large quantities of these by-products, with an annual pro­
(Musthafa et al., 2017). Pumpkin seeds and pomace (50 and 100 g/kg duction of around 175,000 tons of feather meal in Europe (Campos et al.,
diet for both by-products) were included in the Pacific white shrimp diet 2017). Despite this, PBM is still sparsely used as a protein source in
for 60 days in the study conducted by Zancan et al. (2023). The seeds aquatic feed, although it presents favorable characteristics, such as good
exerted a negative effect on performance and decreased the antioxidant palatability and a well-balanced AA profile (Gaudioso et al., 2021).
activity of muscle (< DPPH value), while the pomace improved the Since most processed animal by-products are characterized by low
growth parameters (better FCR and PER), antioxidant activity, total content in arginine (Arg), Lys, Meth, and Trp, supplementation of these
carotenoid content, and shrimp body color. The improvement in shrimp AAs in diets according to fish nutritional requirements, is necessary for
color, associated with the total carotenoid content, is an important the formulation of balanced feeds with essential AAs (Table 3). For
factor in consumer acceptability, making this by-product a sustainable example, 30-60 % of diets of PBM in juvenile rainbow trout appeared to
and cost-effective resource for improving the color of this aquatic spe­ represent a valid protein source option in FM-free diets (Gaudioso et al.,
cies (Zancan et al., 2023). 2021). Black sea bass and Gilthead seabream fish fed 40-50 % of FM
replaced by PBM showed no adverse effects in the growth performance,
digestive protease activities (trypsin and chymotrypsin), and hemato­
3.2. Non-plant protein sources logical and biochemical indices (Dawson et al., 2018; Karapanagiotidis
et al., 2019). However, in black sea bass, when FM was replaced 100 %
3.2.1. Animal by-products with PBM, the growth was negatively affected. This effect may be due in
Animal-sourced feedstuffs for aquaculture derive from the by- part to the relatively low dietary levels of essential fatty acids, in
products of fish, poultry, pork, and beef, as they are made from particular, the long-chain n-3 PUFAs (Dawson et al., 2018). At the same
several organs or tissues, such as blood, intestinal mucosa, feathers, time, also in other species, such as turbot, negative effects on growth
meat, and bone (Jia et al., 2022) (Fig. 6). These animal by-product meals performance and poor FCR were evidenced when fed poultry
are considered valuable FM alternatives due to their nutritional quality, by-products at high levels (≥ 168 g/kg diet) (Hao et al., 2020). These
including an AAs profile more similar to the one present in the animal effects could be due to the accumulation of some toxic substances (e.g.
(Table 3), and low prices. Moreover, they display considerable advan­ aromatic AA derivatives in the intestinal tract) in poultry by-products,
tages over plant-derived proteins, such as lack of ANFs. Table 4 sum­ which disrupt digestion and nutrient absorption (Hao et al., 2020).
marizes a selection of studies examining the effects of animal-by Among more economically and environmentally sustainable alter­
products used as FM replacer on key aquaculture species. native protein sources to reduce production costs is feather meal (FEM),
The Regulation (EC) 1774/2002 (European Union Regulation, 2002) which is becoming attractive due to high supply options, low costs, high
established the definition of three categories of Animal By-products”

Fig. 6. Main animal by-products used in aquaculture feed formulation.

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V. Serra et al. Veterinary and Animal Science 25 (2024) 100381

Table 3
Amino acid profile ( % DM) of different animal by-products used as FM replacement summarized from references.
Amino acid FM PBM FEM MBM PMM BM

Arginine 3.75 8.24 5.92 3.44 4.55 4.2

Histidine 1.68 1.10 0.68 1.12 1.47 7.63
Isoleucine 3.13 2.92 4.17 1.76 2.03 0.40
Leucine 5.17 4.48 7.26 3.33 4.3 14.64
Lysine 4.95 3.9 1.85 3.33 3.76 8.75
Methionine 1.97 1.30 0.66 0.86 1.24 0.75
Phenylalanine 2.99 2.21 4.38 1.89 2.35 6.8
Threonine 2.80 2.85 4.01 1.77 2.3 3.14
Tryptophan - 0.46 - 0.44 - -
Valine 3.6 3.27 6.63 2.47 2.95 8.45
Alanine 4.14 3.78 3.91 3.93 5.22 8.43
Aspartic acid 6.22 5.30 5.64 3.99 5.12 13.84
Glutamic acid 8.36 5.52 8.86 6.39 8.78 8.34
Glycine 3.72 1.76 6.7 6.36 8.28 4.98
Proline 3.18 4.76 8.81 3.72 5.41 4.05
Serine 2.49 4.23 9.17 1.74 2.7 4.55
Tyrosine 2.20 1.54 2.42 1.39 1.76 2.42
Cystine 0.65 0.65 4.82 0.45 - -
Reference Poolsawat et al., 2021 González-Rodriguez et al., 2016b Poolsawat et al., 2021 Kerr et al., 2019 Huang et al., 2022 Takakuwa et al., 2022

Abbreviations: BM: blood meal; FEM: feather meal; FM: fish meal; MBM: meat bone meal; PBM: Poultry by-product meal; PMM: porcine meat meal

protein content (86 %) and essential AAs, and lack of ANFs (Jasour et al., seabream diet did not affect BWG or feed efficiency up to 61.5 %
2017). Using various rendered animal protein ingredients in combina­ (Moutinho et al., 2017), but the inclusion percentage of up to 30 % of
tion might be a way to formulate highly nutritive and cost-effective fish porcine meat meal (PMM) in juvenile golden pompano (Trachinotus
feed. This nutritional approach is based on the concept that the nutrient ovatus) diet, compromised the activity of plasma antioxidant enzymes,
balance and economic cost of a blend of rendered animal protein in­ without negative effects on the gut microbiota (Huang et al., 2022).
gredients are usually better than those of a single ingredient (Wu et al.,
2018). Based on this, it was observed that giant croaker (Nibea japonica) 3.2.2. Insects and invertebrates
fish fed a diet with a blend of PBM and FEM to replace FM (20, 40, 60, Insect farming for the feed industry has increased significantly
and 80 %), showed a better final BW, BWG, and FI at percentages of worldwide (Mulazzani et al., 2021). The European Regulation,
inclusion of 20 and 40 %, compared to the unsupplemented group. In 2015/2283 establishes rules for the release of novel foods and has been
general, it was observed that the FI decreased with the increase in the applied across all European countries since January 2018. Among the
percentage of FM replaced by PBM and FTH blend, probably due to the so-called novel foods are terrestrial invertebrates, including insects and
negative effect of FEM on palatability (Wu et al., 2018). However, hy­ earthworms. It should be noted that, to date, the use of earthworms as
drolyzed feather meal (HFM) has been demonstrated to successfully feed for monogastric animals and cattle is not permitted if the earth­
replace FM protein at 25 % without compromising the growth perfor­ worms are raised on waste (e.g. animal manure, organic fraction of solid
mance, and proximate composition of juvenile gilthead seabream fillet urban waste), despite some preliminary findings proving the safety of
(Psofakis et al., 2020). this procedure (Conti et al., 2019; Tedesco et al., 2020). In contrast,
Also in this case, as usual, negative effects were noticed with the use insect meal (IM) can be used in aquaculture nutrition (European
of animal blood meal (BM). BM is traditionally produced by heating the Parliament, 2017).
liquid blood to ~95 ◦ C to coagulate the blood proteins, which are then The insects are a feed ingredient with an interesting nutritional
separated from the liquid portion by centrifugation. The dietary addition profile, since they are rich in AAs (Table 5), lipids, vitamins, and min­
of cow BM over 7 % negatively affected growth performance, feed uti­ erals. Also, the insects are characterized by fast growth and reproduction
lization, and the activity of antioxidant enzymes (CAT, SOD, GPx), with rates and their requirement of water and land is minimal. For these
an increase in MDA concentration in African catfish (Ogunji and Ihea­ reasons, the use of insects in fish feed production is considered to be one
nacho, 2021), while in Nile tilapia the growth performance were of the most sustainable and economically viable alternatives (Fisher
negatively affected when BM was included over 50 % (Kirimi et al., et al., 2020; Auzins et al., 2024). The frass can also be used as a soil
2016). Differently, inclusion percentages (2.5, 5.0, 7.5 and 10 %) of ameliorant (Tedesco et al., 2020; Poveda, 2021; Aragão et al., 2022). For
other blood by-products such as dried bovine hemoglobin (DBH) these reasons, the use of insects as a protein source in fish nutrition
(Ibrahim et al., 2022) or spray-dried plasma (16.6, 33.2, 49.7, and 66.3 represents an attractive alternative to FM and has become one of the
g/kg) (De Araújo et al., 2017) used to replace FM in the diet of Nile main focuses of much research over the last years (Nogales-Merida et al.,
tilapia, showed a linear increase in the growth performance at the level 2019; Alfiko et al., 2022; Tran et al., 2022). Table 6 summarizes a se­
of 10 % of DBH and 51.83 g/kg of dried plasma, respectively. Moreover, lection of studies examining the effects of different insect species used as
an enhancement of the antioxidant hepatic capacity (higher TAC, GPx, FM replacers on key aquaculture species.
and SOD gene expression) was noticed (Ibrahim et al., 2022). The IM is extremely rich in proteins (60-80 %), essential AAs, vita­
Meat and bone meal (MBM) has high protein content (450-650 g/ mins, and minerals, and provides a good source of lipids, due to the lipid
kg), a well-balanced AA profile, and lacks ANFs (Hodar et al., 2020). content of the insects (31-43 %). It must be pointed out that some
MBM has been strictly banned in ruminant nutrition due to the risk of technological processes such as drying, fat extraction, or enzymatic
bovine spongiform encephalopathies. Moreover, it has been successfully hydrolysis, can improve the nutritional value of IMs (Mikołajczak et al.,
used for the replacement of FM in the diets of many aquatic animals 2020). Up to now, several studies have demonstrated the efficiency of
(Moutinho et al., 2017; Tang et al., 2018; Wang et al., 2020b). The IMs in different fish species as FM replacers.
extent of FM substitution by MBM differs markedly between aquatic Among insects, the black soldier flies (Hermetia illucens) are the most
species, varying for example between 20 and 40 % in olive flounder studied for nutrition purposes, followed by the yellow mealworm
(Paralichthys olivaceus) to 100 % in Nile Tilapia (Lee et al., 2012, Ribeiro (Tenebrio molitor). The inclusion of black soldier larvae meal in the diet
et al., 2016). Percentages of MBM of 40.9 or 61.5 % in the gilthead of several fish species has been evaluated at various inclusion levels

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Table 4
Animal by-products as a substitute for FM in the diet of different aquatic species.
Alternative Aquatic species Inclusion level FM inclusion in Time Effects Reference
protein source the control diet (weeks)

PBM; Crayfish (Cherax cainii) 22 % feather meal 30.15 % DM 8 Performance: no difference in % WG, SGR and FCR; ↑ Saputra
FEM; (FEM); % WG and SGR, lowest FCR (MBM group); survival et al., 2019
LM; 36.4 % lupin meal rate: ↑ in FEM > PBM; lowest survival rate in MbM
MBM (LM); group; Immune competence: ↑ THC in PBM,
29.5 % poultry by- differential haemocyte counts increased significantly
product meal (PBM); in FM, FEM, and LM; higher NRRT (FM group); higher
24.3 % meat and bone PR (FM and MBM groups); Bacterial loads: ↑ in LM.
meal (MBM)
HFM Pengze crucian carp 2 % (F15); 18 % DM 10 Performance: ↓ FBW, SGR in F60; FE in F30; ↑ HSI in Yu et al.,
(Carassius auratus var. 4 % (F30); F60; FBW, SGR, HSI of F15, F30 and F45 equal to 2020
Pengze) 6 % (F45); control group; no difference in FE among F15, F30 and
8 % (F60) F45; no difference in SR; Antioxidant status: ↓ CAT in
F15; ↑ GSH, LPO in F30, F45 and F60; no difference in
SOD and GPx; LPO, GSH in F15 equal to control group;
no difference in CAT among F30 and F45.
FEM; Tilapia (Oreochromis 23 g/kg FEM (FEM50); 60 g/kg 9 Performance: ↓ WG and ↑ FCR in FEM100 group than Poolsawat
EFEM niloticus × 46 g/kg FEM control; ↑ VSI in FEM50 and FEM100 than control; ↓ et al., 2021
O. aureus) (FEM100); HSI in EFEM50 and EFEM100 than FEM100.
23 g/kg EFEM
(EFEM50);
46 g/kg EFEM
(EFEM100)
SDBH Nile tilapia (Oreochromis 2.5 % SDBH 20 % 10 Performance: increase in FBW, ADWG, TWG, SGR, Amer et al.,
niloticus) (SDBH2.5); and PER by SDBH inclusion; Metabolic function 2022
5 % SDBH (SDBH5); indices: ↑ serum growth hormone levels and ↓ serum
7.5 % SDBH leptin hormone levels by increasing SDBH level; ↓
(SDBH7.5); serum GLU in SDBH7.5 and SDBH10 groups;
10 % SDBH (SDBH10) Digestive enzymes activity: ↑ amylase and protease
by increasing SDBH level; Expression of immune-
related genes: ↑ TGF-b, TLR2, and IL-10 (highest
expression in SDBH5); Expression of growth-related
genes in the muscle: ↑ peptide and AAs transporters,
IGF-1, ↓ myostatin in SDBH2.5 and SDBH7.5 groups;
Immunological parameters: LYS, NO and C3 levels
highest in SDBH5; Intestinal histology: ↑ VH, VW,
ratio VH: CD, MCT.
BM; Common carp (Cyprinus 6 % FM (control); 6 % DM 12 Performance: No significant difference in FBW, WGR, Gao et al.,
DPS carpio) 3 % BM (BM); CF and FCR; Intestinal morphometry: ↓ villus height 2020
3 % DPS (DPS); and fold depth in DPS than FM group; no difference in
2 % BM + 2 % DPS the muscular thickness.
(BM+DPS)
MBM Ussuri catfish 138 g/kg (MBM20); 450 g/kg DM 13 Performance: ↓ WG, SGR and FBW in MBM60, Tang et al.,
(Pseudobagrus ussuriensis) 276 g/kg (MBM40); MBM80, MBM100M; FCR of MBM80 and MBM100 2018
414 g/kg (MBM60); higher than control; ↓ FI in MBM80 and MBM100;
552 g/kg (MBM80); Enzyme activity: ↓ pepsin, intestinal protease and
690 g/kg (MBM100) liver protease in all groups; ↓ intestinal lipase with
increasing levels of dietary MBM.
MM; Ussuri catfish 91.3 g/kg MM; 180 g/kg DM 8 Performance: no difference in FI; ↓ SGR, FE, PER in Wang et al.,
MBM (Pseudobagrus ussuriensis) 84.9 MBM MBM than control (with FM); ↑ VSI in MM and MBM 2020b
than control; Digestive enzymes: ↑ lipase intestinal
activity in MM; ↓ TAC in MBM than control; ↓ hepatic
SOD and CAT than control; ↑ hepatic MDA in MM than
control; Expression of IGF-I: no difference.
MM Ussuri catfish 177.5 g/kg (MM1); 280 g/kg DM 8 Performance: ↓ FBW, WG, FI and SGR with increasing Luo et al.,
(Pseudobagrus ussuriensis) 355.1 g/kg (MM2) dietary MM; ↑ PER in MM diets; Apparent 2019
digestibility: No difference in ADC of CP; ↑ ADC of
DM, CL and gross energy of M2 than M1 and control;
Digestive enzymes: ↑ Pepsin and Alpha-amylase in
M2; ↓ Lipase activity with increasing dietary MM
levels; Hepatic antioxidant enzyme activity: ↓ TAC
and SOD with increasing dietary MM levels; no
difference in CAT; Expression of IGF-I: ↓ expression
of IGF-I in M2.
CPP Largemouth bass 38.3 g/kg (CPP50); 510 g/kg DM 12 Performance: ↓ SGR in CPP100 and CPP150; no Li et al., 2019
(Micropterus salmoides) 76.6 g/kg (CPP100); difference in HSI and CF; ↓ FI in CPP100 and CPP150;
115.0 g/kg (CPP150) ↑ FCR in CPP150; ↑ PER in CPP100; ↓ PRR in CPP150;
lowest LRR and ADC of lipid in CPP150; ↓ ADC of
essential AAs in CPP150; Immunological and
haematological parameters: ↓ serum LYS and
respiratory burst in CPP150; ↓ RBCs and HB in
CPP150; ↑ haematocrit in CPP50.
(continued on next page)

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V. Serra et al. Veterinary and Animal Science 25 (2024) 100381

Table 4 (continued )
Alternative Aquatic species Inclusion level FM inclusion in Time Effects Reference
protein source the control diet (weeks)

CHP Largemouth bass 3.83 % (CHP1); 51 % DM 12 Performance: ↓ FI in CHP2 and CHP3; ↓ FER and PER Ding et al.,
(Micropterus salmoides) 7.66 % (CHP2); in CHP3; ↑ PRR in CHP1; ↓ ADC of Thr, Met, Leu, Phe, 2020
11.50 % (CHP3) Lys and Arg with inclusion of CHP; Immunological
and haematological parameters: ↓ LYS in CHP3; ↓
RBCs and HB content in CHP2 and CHP3; ↓
haematocrit in all groups than control.
MBM Climbing perch (Anabas 26.35 % MBM (D2); 62 % DM 10 Performance: ↓ FBW and WG by FM replacement Hossain
testudineus) 31.99 % MBM (D3); levels; ↓ FI in D2 > D3 > D4; ↓ PER in D4; et al., 2017
37.64 % MBM (D4) Digestibility: ↑ ADC of DM, CP and CL in control diet
(with FM).
PBM Gilthead seabream 18 % - 16 Performance: ↑ FBW in control diet (with FM); no Sabbagh
(Sparus aurata) 36 % difference in HSI and VSI; Welfare parameters: No et al., 2019
difference in cortisol, protein levels, osmolality, ALT
and AST; no difference in liver alkaline phosphatase,
lipase and leucine amino peptidase.
PPH Gilthead seabream 5 % PPH 7 % DM 13 Performance: ↑ FBW, SGR, FI; no difference in FCR, Gisbert et al.,
(Sparus aurata) SR; Antioxidant status: no difference in TAC, SOD, 2021
CAT.
PBM; Giant croaker (Nibea 87 g/kg PBM + 37 g/kg 400 g/kg DM 8 Performance: ↑ FBW, WG and FI in control, B20 and Wu et al.,
FEM japonica) FEM (B20); B40 than B60 and B80; no difference in FCR and NRE; 2018
139 g/kg PBM + 59 g/ Waste outputs: No difference in nitrogen waste; ↑
kg FEM (B40); phosphorus waste in B20 and B40 than B60 and B80.
190 g/kg PBM + 82 g/
kg FEM (B60);
242 g/kg PBM + 104 g/
kg FEM (B80)
PBM; Hybrid grouper 60.4 g/kg PBM + 73.0 700 g/kg DM 8 Performance: no significant difference in FBW and Ye et al.,
SM; (Epinephelus fuscoguttatus g/kg SM + 10.0 g/kg WG; ↓ FE and PER in FM42, FM28 and FM14; ↑ HSI in 2019
BM x Epinephelus lanceolatus) BM (FM56); FM14; no difference in VSI and CF; Plasma
120.9 g/kg PBM + biochemical parameters: ↑ ALT in all diets compared
146.1 g/kg SM + 20.0 to control; ↑ AST in FM14; ↑ CHO and LDL-C with
g/kg BM (FM42); increasing level of APB; no difference in TG; Liver
181.3 g/kg PBM + histology: ↑ occurrence rate of nuclei shifting to the
219.1 g/kg SM + 30.0 cellular periphery cytoplasmic vacuolization in FM42,
g/kg BM (FM28); FM28 and FM14; Gene expression: ↑ expression of
241.8 g/kg PBM + lipid metabolism-related genes (PPARα, CPT1, FAS
292.1 g/kg SM + 40.0 and apolipoprotein Apo-AI); ↑ expression of apoptosis-
g/kg BM (FM14) related genes (caspase-3, caspase-8, caspase-9 and
p53) and inflammation-related genes (IL-8, IL-10 and
TGF-β1)
BM Red sea bream (Pagrus 4.3 % (BM10); 30 % DM 8 Performance: no difference in FBW, WG, SGR, DFR Takakuwa
major) 8.63 % (BM20); and SR; Apparent digestibility coefficients: ↓ et al., 2022
12.94 % (BM30) protein digestibility in BM20 and BM30 than control;
↓ fat digestibility in BM30; Serum analyses: ↑ TP in
BM30 than control; ↑ CHO in BM30 than control and
BM20; no difference in GLU, TG, GOT and GPT
MBM; Turbot (Scophthalmus 0 MBM + 45 g/kg SH 470 g/kg DM 8 Performance: ↑ SGR in MBM0SH; ↓ SGR in MBM50; ↑ Nguyen
SH maximus L.) (MBM0SH); FCR in MBM50; no difference in FCR among MBM0, et al., 2023
155.5 g/kg MBM + MBM0SH, MBM25, and MBM25SH; ↑ FI in fish fed SH;
0 SH (MBM25); Hematological parameters: ↓ TP in MBM50; ↓ AST in
155.5 MBM + 45 g/kg MBM25 and MBM50; ↓ ALT in MBM50.
SH (MBM25SH);
311 g/kg MBM + 0 SH
(MBM50);
311 g/kg MBM + 45 g/
kg SH (MBM50SH)
HFM European seabass 5 % (HFM5); 2.5 % FM Super 18 Performance: no difference in FBW, FCR and PER; no Campos
(Dicentrarchus labrax) 7.5 % (HFM7.5); Prime + 29 % difference in final whole-body composition; et al., 2017
12.5 % (HFM12.5) FM60 Digestibility: ↓ protein ADC in HF12.5; ↓ energy ADC
in HF12.5; ↑ Phosphorus digestibility concomitantly
with the inclusion of HF; no difference in metabolic
nitrogen losses; Immune parameters: No difference
in peroxidase, LYS, and alternative complement
pathway.

Abbreviations: ↑: improvement; ↓: decrease; AAs: amino acids; ADC: apparent digestibility coefficient; ADWG: average daily weight gain; Apo-AI: apolipoprotein AI;
Arg: arginine; AST: aspartate aminotransferase; BM: blood meal; C3: complement 3; CAT: catalase; CD: crypt depth; CF: condition factor; CHO: cholesterol; CHP:
chicken haemoglobin powder; CL: crude lipid; CP: crude protein; CPP: chicken plasma powder; CPT1: carnitine palmitoyltransferase 1; DFR: daily feeding rate; DM: dry
matter; DPS: dried porcine soluble; EFEM: enzymatic feather meal; FAS: fatty acid synthase; FBW: final body weight; FCR: feed conversion ratio; FE: feed efficiency;
FEM: feather meal; FER: feed efficiency ratio; FI: feed intake; FM: fishmeal; GLU: glucose; GOT: glutamic oxaloacetic transaminase; GPT: glutamic pyruvic trans­
aminase; GPx: glutathione peroxidase; GSH: reduced glutathione; HB: haemoglobin; HFM: hydrolysed feather meal; HSI: hepatosomatic index; IGF: insulin like growth
factor; IL-8: interleukin 8; IL-10: interleukin 10; LDL-C: low-density lipoprotein cholesterol; Leu: leucine; LM: lupin meal; LPO: lipid peroxidation; LRR: lipid retention
rate; LYS: lysozyme; Lys: lysine; MBM: meat and bone meal; MDA: malondialdehyde; Met: methionine; MM: mussel meal; NRE: nitrogen retention efficiency; NRRT:
neutral red time retention; PBM: poultry by-product meal; PER: protein efficiency ratio; Phe: phenylalanine; PPARα: peroxisome proliferator-activated receptor alpha;
PPH: porcine plasma hydrolysate; PR: phagocytic rate; PRR: protein retention; RBCs: red blood cells; SDBH: spray-dried bovine hemoglobin powder; SGR: specific

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V. Serra et al. Veterinary and Animal Science 25 (2024) 100381

growth rate; SH: shrimp hydrolysate; SM: shrimp meal; SOD: superoxide dismutase; SR: survival rate; TGF-b: transforming growth factor-beta; TLR2: Toll-like receptor
2; TWG: total body weight gain; Thr: threonine; VSI: viscerosomatic index; VW: villous width; WG: weight gain; WGR: weight gain ratio.

Table 5
Amino acid profile (% DM) of different insect meals used as fish meal replacement summarized from references.
Amino acid H. illucens H. illucens T. molitor T. molitor M. domestica G. sigillatus

Arginine 1.24 2.56 1.81 2.93 2.91 3.52

Histidine 1.07 1.50 1.77 1.71 1.63 1.35
Isoleucine 0.91 2.57 1.31 2.24 2.08 2.27
Leucine 1.86 4.12 2.96 3.98 3.41 4.25
Lysine 1.94 3.25 2.49 2.96 4.21 3.24
Methionine 0.47 0.91 0.57 0.68 1.40 0.97
Phenylalanine 2.16 2.03 3.07 1.78 3.81 1.90
Threonine 0.95 2.47 1.44 2.25 2.28 2.17
Tryptophan - - - - 0.71 -
Valine 1.42 3.53 2.32 3.08 2.80 3.16
Alanine 2.37 5.02 3.92 4.39 2.78 4.70
Aspartic acid 2.92 - 3.71 - 5.57 4.79
Glutamic acid 3.19 - 4.98 - 7.71 6.42
Glycine 1.84 2.98 2.87 - 2.33 2.68
Proline 1.58 3.81 3.04 4.05 2.27 2.92
Serine 1.43 2.73 2.49 2.74 2.18 2.87
Tyrosine 2.23 2.68 4.47 2.79 4.14 2.57
Cystine 0.13 - 0.24 0.21 0.53 0.53
Reference Melenchón et al., 2022 Mastoraki et al., 2020 Melenchón et al., 2022 Mastoraki et al., 2020 Hashizume et al., 2019 Józefiak et al., 2019

without negative effects on growth performance and other physiological acceptance, a necessary prerogative for successful IM supplementation
responses (Xiao et al., 2018; Wang et al., 2019; Abdel-Tawwab et al., into aquaculture. This acceptance could be accelerated by making in­
2020). When dried black soldier fly larvae meal replaced FM protein at formation available for product awareness, starting for example with
percentages up to 20-64 % no negative effects were observed on fish younger segments of the population, who are more willing to learn new
growth, feed utilization, and survival rate, neither the hematological concepts. The insect industry certainly needs to expand its production
indices affected (Magalhães et al., 2017; Wang et al., 2019; Abdel-­ scale so it can compete on the price of other more common protein
Tawwab et al., 2020; Adeoye et al., 2020). However, as reported with sources, as the production volume of SBM and FM is thousands of times
the use of some animal by-products, levels around 100 % negatively greater.
affected the growth performance, such as observed in catfish (Adeoye
et al., 2020). 4. Marine algae
The potential role of the yellow mealworm (T. molitor) as an FM
replacer is also increasingly being studied, due to its excellent nutri­ 4.1. Macroalgae
tional value, accompanied by a short life cycle (Rema et al., 2019). Its
inclusion at 25 % (corresponding to 33 % FM replacement) resulted in The Macroalgae, also called Seaweeds, are divided into three large
optimal WG, FCR, and PER in gilthead seabream (Piccolo et al., 2017), groups based on their color. Green seaweeds, including more than
while in European seabass, anti-inflammatory activity was exerted 13,000 species, owe their color to the presence of chlorophyll a and b,
(Henry et al., 2018) and in olive flounder immunostimulatory effect was which is used during the photosynthetic process. Red seaweeds (Rho­
observed in a range of inclusion from 13 to 52 % (Jeong et al., 2021). dophyta) comprise 6100 species and their color is due to phycoerythrin
Moreover, in the study conducted by Su and colleagues (2017), the in­ and phycocyanin pigments; they contain a higher amount of proteins
clusion percentages of 9, 18, or 27 % of yellow mealworm meal in a (up to 47 % of DM) compared to green and brown algae (Carpena et al.,
yellow catfish diet induced an up-regulation of the major histocompat­ 2021). Among macroalgae species, red algae appear to be the most
ibility complex (MHC) II, IL-1, CypA (cyclophilin), IgM and HE (hepci­ suitable source of animal feed due to their relatively high protein con­
din) genes, thus demonstrating an immunostimulatory effect. Useful tent and structurally diverse bioactive compounds with great pharma­
properties such as immunostimulant and against stress factors have been ceutical and biomedical potential (Younis et al., 2018). Brown seaweeds
attributed to IMs, possibly due to components of insect exoskeletons (e. (Ochrophyta, Phaeophyceae) include 1800 species and the color is
g., chitin and chitosan), which generally increase immunity by acti­ correlated with the content of carotenoid fucoxanthin. The protein
vating innate immune cells and inducing cytokines production through content of the latter is lower than the other two classes, ranging between
different cell surface receptor (Kamilya and Khan, 2020). It was 5 and 15 % (Mohammed et al., 2021). From a regulatory point of view,
observed that the use of 30 % of larval frass rich in chitin for the pres­ within Europe, seaweeds that have been subjected exclusively to drying
ence of insect moulting, improves the innate immune response and the and crushing are referred to as “seaweed meal” (European Union
resistance of fish against Flavobacterium columnare and Streptococcus Commission Regulation, 2022); otherwise, seaweeds subjected to other
iniae infection (Yildirim-Aksoy et al., 2020). Other insect species manufacturing processes are considered “novel feed ingredient”, regu­
approved by the European Commission for aquatic feeding (European lated by European Regulation (EC) No. 767/2009.
Parliament, 2017) include Musca domestica, Alphitobius diaperinus, Marine seaweeds represent a promising alternative to FM due to their
Acheta domesticus, Gryllodes sigillatus, and Gryllus assimilis. The studies low costs and relatively well-balanced essential AA composition
reporting the use of these insect species are listed in Table 6. (Table 7). Over 75 % of seaweed has higher proportions of total essential
It is worth considering that different fish species have different levels AAs than wheat flour, 50 % higher than soy flour, and also than rice and
of requirement for insects in their diet, which vary according to growth corn (Maehre et al., 2014). The inclusion of macroalgae could improve
stages and farming systems; to commercialize IM in the future, these fish growth performance, or in any case not negatively affect them
requirement levels must be known. One issue that certainly needs to be (Sotoudeh and Mardani, 2019; Zeynali et al., 2020). This was the case of
considered regarding the future perspectives of IM is consumer a red sea bream (Pagrosomus major) fed with a 3 % diet inclusion of

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Table 6
Insect-protein sources as a substitute for FM in the diet of different aquatic species.
Alternative Aquatic species Inclusion levels FM inclusion Time Effects Reference
protein source in the control (weeks)
diet

HIM Siberian 185 g/kg (HIM25); 70 % DM 16 HIM100 was excluded from the study as fish refused Caimi et al., 2020
sturgeon 375 g/kg (HIM50); the diet.
(A. baerii Brandt) 750 g/kg (HIM100) Performance: ↓ feed consumption in HIM25 and HIM50;
FBW in HIM50 than control; no difference in HSI and VSI;
Digestibility: no difference in ADC of DM; ↓ ADC of CP in
HIM25 and HIM50 than control.
HIM; Crayfish 39 % PBM; 41 % DM 8 Performance: no difference in WG and growth rate; Foysal et al., 2019
PBM (C. cainii) 32 % FM + 12 % HIM; ↑ haemolymph osmolality, LYS activity, total haemocyte
31 % PBM + 11 % HIM counts, and protein and energy contents in the tail muscle
(FM + HIM and PBM + HIM groups); Microbiota
analysis: ↑ bacterial activity and gene function correlated
to the biosynthesis of protein, energy and secondary
metabolites (PBM + HIM group); Proteobacteria dominant
in FM + HIM group, Firmicutes higher in PBM + HIM;
Gene expression: Up-regulation of cytokine genes in the
intestinal tissue (FM + HIM and PBM + HIM groups).
CM Nile Tilapia 20 % cricket meal - 6 Performance: ↓ FBW in CM1 than CM2; no difference in Cadena-Cadena
(O. niloticus) (CM1); length; ↓ feed conversion factor in CM1 than CM2. et al., 2023
30 % cricket meal
(CM2)
MD; Hybrid catfish 300 g/kg SBM (SBM); 15 % DM 6 Performance: no difference in FCR, FI, PPV, LPV; Fawole et al., 2023
SBM (C. gariepinus ♀ x 140 g/kg MD + 300 g/ ↑ FBW, WG, SGR, DGI of (SBM+MD21) than SBM and
H. kg SBM (SBM+MD14); control (FM diet); no difference in HSI and VSI;
longifilis ♂) 210 g/kg MD + 300 g/ Haematology parameters: no difference in Hb, RBCs,
kg SBM (SBM+MD21) Hct; ↑ white blood cell and lymphocyte counts in
(SBM+MD21); Immuno-physiological indicators: ↑
globulin value in (SBM+MD21); no difference in ALB, total
IG, ALP, ALT; ↑ AST in (SBM+MD14) and (SBM+MD21);
Antioxidant activity: ↑ SOD in (SBM+MD14); ↑ CAT in
(SBM+MD21).
MD Nile Tilapia 110 g/kg (MD1); 360 g/kg 10 Performance: No difference in SR, WGR and SGR of MD1, Wang et al., 2017
(O. niloticus) 220 g/kg (MD2); MD2 and MD3 than the control group (FM diet); ↓ SR, WGR
330 g/kg (MD3); and SGR in MD4; no difference in HSI and VSI; ↑ FCR of
430 g/kg (MD4) MD4 than the control group; Innate immunity: no
difference in serum LYS; ↓ macrophage phagocytic activity
in MD2, MD3, MD4 than control.
HIM Atlantic salmon 50 g/kg (HIM33); 10 % DM 16 Performance: no difference in FBW, WG, DGI, SGR, HSI, Belghit et al., 2019
(S. salar) 100 g/kg (HIM66); VSI, FI, FCR, CF, PPV and LPV; Digestibility: no difference
150 g/kg (HIM100) in ADC of CP, CL, amino acids and fatty acids.
HIM European 65 g/kg (HIM6.5); 32.4 % DM 9 Performance: no difference in FBW and feed utilization; Moutinho et al.,
seabass 130 g/kg (HIM13); Hepatic antioxidant enzymes: SOD and CAT activity 2021
(D. labrax) 195 g/kg (HIM19.5) highest in control; no difference in GR and GPX.
TM European sea 25 % TM; 70 % DM 6 Performance: no difference in FBW; HSI in all TM groups Henry et al., 2018
bass 25 % TM + proteases than control; Immunological analyses: ↓ activity of
(D. labrax) (TM-Prot); serum ceruloplasmin, myeloperoxidase and nitric oxide in
25 % TM + TM diets than control; no difference in antibacterial
carbohydrases (TM- activity of serum against Micrococcus luteus; ↓ bacteriolytic
Carb) activity against E. coli in TM-Carb than other groups; ↑ anti-
protease activity in TM and TM-Carb than TM-Prot and
control.
TM; European sea 19.5 % TM; 65 % DM 12 Performance: no difference in DFI; ↑ FBW in HIM than Mastoraki et al.,
HIM; bass 19.5 % HIM; TM; no difference in WG and SGR; ↑ FCR in TM than MD 2020
MD (D. labrax) 19.5 % MD and control; no difference in HSI, VSI and gut length;
Plasma metabolites: no difference in AST and ALT; ↓ GLU
in TM; ↑ CHO in HIM and control;
Liver enzyme activity: no difference in AST and ALT; ↑
GDH in HIM than MD
TM Red seabream 250 g/kg (25 % TM); 65 % DM 4 Performance: ↑ FBW in accordance with DMW inclusion; ↑ Ido et al., 2019
(P. major) 400 g/kg (40 % TM); FI in accordance with DMW inclusion; Challenge test
650 g/kg (65 % TM) with pathogenic Edwardsiella tarda bacteria: ↑ in 10 %
50 g/kg (5 % TM; MW.
challenge test for 8
weeks);
100 g/kg (10 % TM;
challenge test for 8
weeks)
MD Red seabream 70 % undefatted MD 70 % DM 4 Performance: no difference in BW and FI. Hashizume et al.,
(P. major) larvae (-MD); 2019
70 % defatted MD
larvae (+MD)
DTM Pacific white 52 g/kg (DTM25); 25 % DM 8 Performance: ↑ FBW in DTM50 and DTM75 than control; Motte et al., 2019
shrimp 103 g/kg (DTM50); ↑ SGR in DTM50 and DTM100 than control; ↓ 24 % FCR in
(continued on next page)

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Table 6 (continued )
Alternative Aquatic species Inclusion levels FM inclusion Time Effects Reference
protein source in the control (weeks)
diet

(Litopenaeus 154 g/kg (DTM75); DTM50 than control; Immunity: ↓ PO activity in all groups
vannamei) 205 g/kg (DTM100) after bacterial challenge with Vibrio parahaemolyticus.
TM Meagre 100 g/kg (TM10); 40 % DM 9 Performance: ↓ FBW, WG, FE, FI, PER with increasing TM Coutinho et al.,
(Argyrosomus 200 g/kg (TM20); inclusion; Digestibility: ADC of DM, CP and energy higher 2021
regius) 300 g/kg (TM30) in control than TM diets; Hepatic amino acid catabolism
enzymes: no difference in ALT, AST and GDH; Pancreatic
digestive enzymes: ↓ Trypsin and lipase activities with
increasing TM inclusion; no difference in α-amylase.
HIM; Rainbow trout 200 g/kg HIM; 34.8 % DM 10 Performance: FBW and SGR lower in GS than TM and Józefiak et al.,
TM; (O. mykiss) 200 g/kg TM; HIM; no difference in PER; Histology: ↓ villus height in TM 2019
GS 200 g/kg GS and GS; ↓ mucosa thickness in GS; Microbial community:
↑ total number of bacteria in HIM, TM and GS than control
(the highest value in TM); ↑ Enterobacteriaceae in TM than
other groups; ↑ Clostridium leptum subgroup in TM and GS
than HIM and control; ↑ Clostridium coccoides in HIM, TM
and GS than control; ↑ Lactobacillus sp./Enterococcus sp. in
all treatments (the highest value in TM).
HIM Rainbow trout 105 g/kg (HIM25); 42 % DM 14 Performance: no difference in FBW, WG, SGR and FCR; Cardinaletti et al.,
(O. mykiss) 210 g/kg (HIM50) Plasma metabolic parameters: no difference in CHO, TG, 2019
GLU, ALB and TP; Gene expression: no difference in igf1
and mstn1a (fish growth) and gr and hsp70 (stress response)
genes; up-regulation of hsp70 in HIM50; ↑ il-10, tnf-a, and
tlr-5 expression in intestine of HIM25 and HIM50;
Histology: ↑ liver lipid accumulation in HIM50; no
inflammation in intestine; significant shortening of the fold
length of medium intestine in fish fed diets containing
insects.
HIM Rainbow trout 100 g/kg (HIM10); 60 % DM 12 Performance: no difference in WG and SGR; Digestibility: Terova et al., 2019
(O. mykiss) 200 g/kg (HIM20); no difference in ADC of DM, CP and EE; Microbial
300 g/kg (HIM30) community: ↓ Proteobacteria in HIM20 and HIM30 than
control and HIM10; ↑ Actinomycetaceae, Brevibacteriaceae,
Corynebacteriaceae, and Microbacteriaceae in all HIM diets
than control; ↑ Lactobacillales in HIM diets than control; ↑
Facklamia, Enterococcus, Lactobacillus, and Pediococcus
genera in HIM diets.
HIM Rainbow trout 200 g/kg (HIM25); 60 % DM 11 Performance: no difference in FBW, WG, SGR and PER; Renna et al., 2017
(O. mykiss) 400 g/kg (HIM50) Digestibility: ↓ ADC of DM and CP in HIM50 than HIM25;
Morphometric investigations: no difference.
TM Rainbow trout 5 % (TM25); 20 % DM 22 Performance: no difference in FBW, WG, SGR, FCR, PER Chemello et al.,
(O. mykiss) 10 % (TM50); and FI; no difference in VSI; ↑ HSI in TM100 than control; 2020
20 % (TM100) Digestibility: ↓ ADC of CP with increasing TM level; no
difference in ADC of DM, EE and GE; Hepatic enzyme
activities: no difference in ALT, AST and GDH.
TM; Sea trout 100 g/kg TM; 25 % DM 8 Performance: no difference in FBW, BWG, SGR, FCR and Mikołajczak et al.,
ZM (Salmo trutta m. 100 g/kg ZM; PPV; ↓ PER in TM and ZM than control; ↑ HSI and VSI in ZM 2020
trutta) than TM and control; Blood serum immunology: ↑ AST in
ZM; ↓ ALP in ZM than TM and control; ↓ TG in TM than ZM
and control; ↑ ALB and CHO in TM and ZM than control; no
difference in ALT, T-Pro, LYS, GLU, IgM; Gut
histomorphology: no difference in villus height, villus
width, and villus area of anterior part of the intestine.
Microbial community: ↓ Aeromonas spp., Enterococcus
spp. and Carnobacterium spp. in ZM; ↓ Lactobacillus in TM;
no difference in Bacillus spp.
CM African catfish 75 g/kg (CM75); 300 g/kg DM 7 Performance: ↓ WG in CM75, CM150 and CM225; Taufek et al., 2018
(C. gariepinus) 150 g/kg (CM150); ↓ FCR in CM300.
225 g/kg (CM225);
300 g/kg (CM300)

Abbreviations: ↑: improvement; ↓: decrease; ADC: apparent digestibility coefficient; ALB: albumine; ALP: alkaline phosphatase; ALT: alanine aminotransferase; AST:
aspartate aminotransferase; BSF: black soldier fly meal; CAT: catalase; CF: condition factor; CHO: cholesterol; CL: crude lipid; CM: cricket meal; CP: crude protein; DFI:
daily feed intake; DGI: daily growth index; DM: dry matter; DTM: defatted Tenebrio molitor; FBW: final body weight; FCR: feed conversion ratio; FE: feed efficiency; FI:
feed intake; FM: fishmeal; GDH: glutamate dehydrogenase; GLU: glucose; GPx: glutathione peroxidase; GR: glutathione reductase; GS: Gryllodes sigillatus; Hb: hae­
moglobin; Hct: haematocrit; HIM: Hermetia illucens meal; HSI: hepatosomatic index; IG: immunoglobulin; IGF: insulin like growth factor; IL-10: interleukin 10; LPV:
lipid productive value; LYS: lysozyme; PER: protein efficiency ratio; PO: Phenoloxidase; PPV: protein productive value; SGR: specific growth rate; SOD: superoxide
dismutase; SR: survival rate; TM: Tenebrio molitor meal; T-Pro: total serum protein; TG: triglyceride; VSI: viscerosomatic index; WG: weight gain; WGR: weight gain
rate; ZM: Zophobas morio meal

Gracilaria lemaneiformis, which showed an enhancement of growth (L. calcarifer) (Morshedi et al., 2023), probably as a result of the
performance in terms of BWG and specific growth rate (Xuan et al., improvement of intestinal morphology and the stimulation of digestive
2019). The replacement of a small amount (6 %) of dietary FM with enzymes secretion. Good growth performance was also observed after
Padina australis and Sargassum ilicifolium improved the growth perfor­ the supplementation of 3 %, 6 %, and 9 % of S. ilicifolium in the Asian sea
mance and innate immune parameters in juvenile Asian sea bass bass diet (Zeynali et al., 2020), and 6 % of the red seaweed Gracilaria

16
V. Serra et al. Veterinary and Animal Science 25 (2024) 100381

Table 7
Amino acid profile ( % DM) of different macroalgae summarized from references.
Amino acid Gracilaria gracilis Ulva rigida Ascophyllum nodosum Undaria pinnatifida Sargassum muticum

Arginine 1.3 1.51 0.10 0.53 0.48

Histidine 0.2 0.23 - 0.15 0.19
Isoleucine 2.3 0.94 0.02 0.38 0.41
Leucine 1.9 1.45 0.07 0.71 0.79
Lysine 1.6 1.24 1.85 0.57 0.49
Methionine 0.2 0.27 - 0.20 0.15
Phenylalanine 1.7 1.23 - 0.40 0.43
Threonine 1.7 1.10 2.24 0.44 0.40
Tryptophan - - 0.29 - -
Valine 3.1 1.22 0.02 0.63 0.55
Alanine 1.9 1.78 1.67 5.29 0.80
Aspartic acid 2.6 2.87 0.88 1.24 0.99
Glutamic acid 2.4 2.32 1.20 1.71 1.17
Glycine 1.1 1.62 0.11 0.88 0.53
Proline 1.0 1.08 0.02 - -
Serine 1.6 1.30 0.13 0.47 0.38
Tyrosine 1.3 0.86 0.04 0.24 0.25
Cystine 0.4 0.07 - 0.06 0.02
Reference Batista et al., 2020 Ferreira et al., 2021 Vieira et al., 2018 Meng et al., 2022 Meng et al., 2022

pygmaea in rainbow trout (Sotoudeh and Mardani, 2019). The survival 4.2. Microalgae
rate, growth performance, PER, chemical fillet composition (protein,
lipid, and ash) (Fig. 4), and digestive enzymes (amylase and protease) Like macroalgae, microalgae could be useful as feed additives or
were significantly increased in Labeo rohita fish fed with 100 g/kg of the replacements to FM, due to their capacity to synthesize nutrients and
red seaweed Halymenia dilatata (Manikandan et al., 2022). However, therefore produce an added high-value biomass, useful in aquaculture
poor survival rate, FI, and growth indices were observed in fish fed a nutrition (Sagaram et al., 2021). As an interesting characteristic,
percentage over 10 % of this macroalga, associated with declines in AA microalgae can grow on some waste, including wastewater, converting
levels due to the replacement of FM in the diet with excessive amounts of organic components in eutrophic effluents into nutrients, including
this alga (Manikandan et al., 2022). It is already known that feeding fish proteins, with well-balanced AA profiles (Table 8), lipids, and carbo­
with excessive macroalgae interferes with nutrient utilization and hydrates. In particular, they can provide a high percentage of proteins
adversely affects growth performance because they have a limited ca­ (30-40 %), with a high level of Met, synthesized, for example, in large
pacity to degrade non-starch polysaccharides (NSP), which are pre­ amounts by the Chlorella, Chlamydomonas, Porphyridium, Isochrysis, and
dominant in algae. Nannochloropsis genera (Wan et al., 2019). In addition, their typical
The supplementation of NSP-degrading enzymes in macroalgae- feature of lack of lignin improves the digestibility in fish (Niccolai et al.,
based diets (Ulva prolifera, Gracilaria lemaneiformis, or Ulva pertusa) 2019).
has been demonstrated to improve the innate immunity of rabbitfish In aquaculture, numerous studies were conducted on different fish
(Siganus canaliculatus), as the activities of serum lysozyme, SOD, and species to test the effect of FM replacement with microalgae. The studies
acid phosphatase were significantly higher in fish fed diets with the and the reviews published in the last 10 years agree on the evidence that
addition of macroalgae (Xie et al., 2019). Concerning the immune sys­ using microalgae in fish diets supports health, survival rate, and growth
tem of fish, in a study conducted by Nur and colleagues. (2020), the performance. Particularly, they correlated with an improvement of FI,
supplementation of the H. musciformis red seaweed at different FM BW, FCR, and immune response, despite a percentage of inclusion too
replacement percentages (10, 20, and 30 %) in Tilapia fish diet high could negatively affect these growth performance parameters
demonstrated positive effects, with an improvement of Hb and hemat­ (Jiang et al., 2019; Nagappan et al., 2021). Moreover, due to the
ocrit levels, thus indicating a better immune response. In particular, nutritional value of microalgae, the fillet quality characteristics were
Gracilaria sp. by-products (ethanol extract and agar extract) were used improved (Nagappan et al., 2021; Ribeiro et al., 2017; Chen et al.,
as dietary supplements in gilthead seabream exposed to an acute 2019a) (Fig. 4). For example, the replacement of FM up to 15 % of CP
crowding event with successful results in terms of oxidative stress with Phaeodactylum tricornutum and Nanochloropsis salina mixture, as
mitigation and innate immunity improvement (Silva-Brito et al., 2020). well as mixtures of N. salina with Amphora sp. or Cylindrothecatheca sp.
Furthermore, Gracilaria by-products (2.5 % and 5 %) were able to reduce improved the hybrid striped bass performance, in particular the BW,
the stress levels of fish by lowering plasma cortisol, boosting the anti­ FCR and protein retention efficiency (de Cruz et al., 2018). Effects were
oxidant response and finally decreasing GPx and GR activities in the noted also in gilthead seabream and Nile Tilapia fed with microalga
liver. Nanochloropsis gaditana (2.5-5 % and 30 % of inclusion, respectively)
Macroalgae are rich also in natural components with antimicrobial (Ayala et al., 2020; Teuling et al., 2019) and in Nile Tilapia fed with
activity (e.g. polyphenols, terpenes, hydroquinones oligomeric phlor­ N. salina meal (820 g/kg diet) (Gbadamosi and Lupatsch, 2018).
otannins, halogenated alkanes, and alkenes), as shown in seabream fish, More recent studies report that diets supplemented with marine
where the supplementation with 5 % powder of G. gracilis resulted in the flagellated Chlorophyta Tetraselmis suecica provided to Pacific white
protection of the fish against Photobacterium damselae subsp. piscicida shrimp (Litopenaeus vannameiis) at a dose of 2.5, 5, and 7.5 g/kg showed
infection (Passos et al., 2021). Similarly, a 3 % of seaweed mixture an improvement in survival rate, BWG and FCR, with the up-regulation
(U. lactuca, Jania rubens, and Pterocladia capillacea) extract showed of the expression of antioxidant genes (SOD, GPx), lowest in the group
antimicrobial properties in striped catfish diet (Pangasianodon hypo­ fed the highest dose of microalgae (Sharawy et al., 2019). Contrarily,
phthalmus), increasing the infection resistance against Aeromonas T. suecica (10 % of inclusion) did not influence growth performance, and
hydrophila (Abdelhamid et al., 2021). nutrient retention in gilthead seabream juveniles (Pereira et al., 2020).
However, at a dose of 15 %, as evidenced and common in many studies,
was observed a decrease in the serum protein profile (TP, Alb, Glob, and
their ratio) and enhancement in serum lysozyme activity, nitric oxide,

17
V. Serra et al. Veterinary and Animal Science 25 (2024) 100381

Table 8
Amino acid profile ( % DM) of different microalgae summarized from references.
Amino acid N. oceanica C. vulgaris Spirulina sp. S. platensis Scenedesmus sp. A. maxima

Arginine 2.0 4.54 4.47 9.50 1.32 6.50

Histidine 0.6 1.04 - 2.20 0.52 1.80
Isoleucine 2.4 2.19 3.64 6.70 1.04 6.0
Leucine 3.1 4.25 6.17 9.80 2.12 8.0
Lysine 3.2 6.74 3.4 4.80 1.71 4.60
Methionine - 1.00 1.71 2.50 0.52 1.40
Phenylalanine 1.8 2.67 3.33 5.30 1.40 4.90
Threonine 1.9 2.92 3.31 6.20 1.21 4.60
Tryptophan - - 0.85 0.30 - 1.40
Valine 5.1 3.21 4.21 7.10 1.50 6.50
Alanine 2.1 3.94 5.02 9.50 1.95 6.80
Aspartic acid 2.9 5.40 6.31 7.30 2.50 8.60
Glutamic acid 3.9 6.76 8.47 10.30 2.85 12.60
Glycine 1.7 3.87 3.43 5.70 1.66 4.80
Proline 1.7 2.81 2.53 4.20 1.42 3.90
Serine 1.3 2.72 - 5.10 1.10 4.20
Tyrosine 1.1 2.39 3.07 5.30 1.22 3.9
Cystine - 0.2 0.64 0.90 - 0.40
Reference Batista et al., 2020 Ferreira et al., 2021 Bashir et al., 2016 Koyande et al., 2019 Noreen et al., 2021 Koyande et al., 2019

and nitroblue tetrazolium levels (Abdelghany et al., 2020). Phaffia rhodozyma, and Wickerhamomyces anomalus, which act as sources
Among the best-known common microalgae, spirulina by-products of proteins, lipids, pigments and enzymes (Glencross et al., 2020).
(3 % of inclusion) and defatted Haematococcus pluvialis (12 % and 24 The use of yeast as a source of dietary protein for farmed fish is not a
% of inclusion) administered to Nile Tilapia, showed an increase in BW, new concept, as studies have been investigating this feasibility since the
FCR, and protein efficiency at 12 % of inclusion but the 24 % of inclusion 1970s.
negatively affected the BW (Ju et al., 2017). Dietary supplementation Recently, a study by Hansen et al. (2019) reported that Atlantic
with spirulina (Arthrospira platensis) powder in juvenile gibel carp salmon parr fed diets containing C. utilis in combination with FM (20 %)
improved the growth performance and survival rate of fish fed 3.38 and or high levels of SMB (yeast percentages of 5, 10, 20 %) for 28 days had
6.76 g/100 g, and increased the plasma SOD and phagocyte activity of no negative effect on the intestinal structure, also showing high growth
blood leukocytes (Cao et al., 2018). performance. Similarly, Nile tilapia fed diets containing different per­
centages (3, 5, 7 %) of S. cerevisiae for 84 days, showed a better growth
5. Single-cell protein performance and higher stress tolerance to hypoxia and disease resis­
tance to Aeromonas compared to the control group proportionally to the
Single-cell protein (SCP) refers to proteins extracted from pure or inclusion level (Abass et al., 2018). S. cerevisiae supplemented with diet
mixed cultures of microorganisms, such as microalgae, yeast, fungi, or acts as an essential probiotic in Nile tilapia, as growth performance and
bacteria, and can be used as a substitute for conventional protein sources feed utilization indices were increased significantly in the fish fed with
intended for human and animal consumption (Pereira et al., 2022). the highest inclusion level (4 g/kg) compared to the control group (Islam
Other names it can refer to are bioprotein, microbial protein, or biomass et al., 2021). In addition, in the same group of fish an improvement in
(Sharif et al., 2021). Their numerous advantages compared to tradi­ the absorptive surface of the intestine occurred (e.g. increase of length,
tional protein sources (e.g. high crude protein content (60-80 %), width, and area of villi), consequently leading to improved absorption of
shorter production time, less use of land, ability to grow on a variety of essential nutrients and ultimately high growth performance of the fish
substrates, absence of ANFs) have made SCP of particular interest in the (Islam et al., 2021). However, it should be considered that the di­
aquaculture sector, especially as a valuable substitute for expensive gestibility of yeast is generally lower than that of FM and some plant
protein sources such as FM and SBM (Ruiz et al., 2023). To reduce the proteins, so high yeast inclusions usually result in lower feed utilization
production costs of SCP, several low-cost suitable substrates have been and fish growth. This was the case of rainbow trout fed with 35.5 % of
used so that the microorganisms can grow and produce tons of proteins. Wickerhamomyces anomalus + S. cerevisiae, which had a lower specific
Such substrates include waste products from agriculture and industry (e. growth rate than fish fed FM (Vidakovic et al., 2020). The authors
g. waste of fruit and vegetable processing, brewery wastewater) (Sharif explained this result as a combined effect of lower FI and poorer protein
et al., 2021). Although microalgae are part of the SCP group, for the quality. Similarly, a previous work conducted by Hauptman et al. (2014)
purposes of this review they have been considered together with mac­ reported that replacing more than 37.5 % (11.2 % dietary inclusion) of
roalgae in the previous paragraphs. FM with dried grain distillers yeast in rainbow trout diets reduced
Over the past 10 years, the use of SCP has been examined in a panel growth performance, probably because of alterations in the quality of
of studies involving the main commercial aquatic species and showed its the pellet, which may affect the trout’s ability to utilize nutrients.
potential to replace FM and terrestrial plant proteins, especially in the Table 9 summarizes a selection of studies examining the effects of
case of yeast, or unicellular fungi (Glencross et al., 2020; Agboola et al., yeast and fungi on key aquaculture species.
2021). Compared to filamentous fungi, yeasts are more important in Bacterial SCP generally carries the highest protein content (50-80 %
aquaculture research, so most of the studies in the literature focus on DM) compared to the other SCP resources, and a high proportion of
them. Yeast species normally used in aquaculture are considered the essential AAs, vitamins, and other valuable molecules. The most used
main protein-rich ingredient in aquatic feeds, due to their crude protein bacterial species to produce SCP are Methylobacterium extorquens,
content of 38-52 % DM (Pereira et al., 2022). Yeasts in particular can Methylococcus capsulatus, Rhodobacter sphaeroides, Afifella marina, and
convert low-value non-food biomass from the forestry and agricultural Corynebacterium ammoniagenes (Pereira et al., 2022). The bacteria are
industries into high-value feed with less dependence on arable land, very attractive as a source of SCP as they grow rapidly in different
water, and changes in climate conditions (Lapeña et al., 2020). Hun­ substrates as by-products from agroindustry and wastewater (Chumpol
dreds of yeast species exist while only a few are used in aquafeeds, such et al., 2018).
as Saccharomyces cerevisiae, Candida utilis, Kluyveromyces marxianus, Studies addressing the application of bacterial SCP in aquaculture

18
V. Serra et al. Veterinary and Animal Science 25 (2024) 100381

Table 9
Fungal single-cell protein as a substitute for FM in the diet of different aquatic species.
Alternative protein Aquatic species Inclusion levels FM Time Effects Reference
source inclusion in (weeks)
the control
diet

Saccaromyces pombe Pacific white shrimp 10 g/kg (D2); 60 g/kg 6 Performance: ↓ growth, feed utilization and Qiu and Davis.,
(L. vannamei) 20 g/kg (D3); PRE in D5; Proximate composition: no 2017
40 g/kg (D4); difference in protein, moisture, lipid, crude fiber
60 g/kg (D5) and ash content
Rhodotorula Nile tilapia 0.125 % (HY1) 2% 8 Performance: no difference in FBW, WG and Chen et al., 2019b
mucilaginosa (Oreochromis 0.25 % (HY2) survival rate; ↑ SGR and ↓ FCR in HY4 than
niloticus) 0.50 % (HY3) control; ↓ VSI than control; Proximate
1 % (HY4) composition: ↑ CP and ash in HY4 than control;
no difference in moisture and lipid;
Biochemical parameters: no difference in TP,
ALB, CHO, TG, HDL and LDL; no difference in
ALP among groups; Immunological and
antioxidant parameters: ↑ LYS in HY2, HY3,
HY4 than control; ↓ MPO in HY2, HY3, HY4
than control; ↑ TAC and SOD in HY2, HY3, HY4
than control; ↓ liver MDA in HY2, HY3, HY4
than control; no difference in liver TAC;
Intestine histology: ↑ villi height in all groups
than control; no difference in villi width;
Bacteria challenge: ↑ survival rate against
Streptococcus iniae in all groups than control
Aspergillus oryzae Nile tilapia 1 g/kg continuously 80 g/kg 9 Performance: ↑ in WG, SGR, FER in ASPC than Dawood et al.,
(O. niloticus) (ASPC); control; no difference in survival rate; 2019
1 g/kg for 1 day and Proximate composition: No difference for ash,
the next day with the moisture, lipid, CF, HSI and VSI; Digestive
basal diet (ASPF1); enzymes: ↑ lipase and protease in all groups
1 g/kg for 1 day and than control; ↑ amylase in ASPC than control;
the next two days Intestine histology: ↑ anterior, middle and
with the basal diet posterior villi lengths than control; Blood
(ASPF2) markers: ↑ Hb in ASPC than control; ↑ Hct in
ASPC and ASPF1 than control; ↑ RBC in ASPC
and ASPF1 than control; ↑ Heterophils and
lymphocyte in ASPC than control
Aspergillus niger Whiteleg shrimp 125 g/kg (FR50) 250 g/kg 6 Performance: no difference in WG and SGR in Dayal et al., 2020
(Penaeus vannamei) 150 g/kg (FR60) FR50, FR60 and FR70 than control; ↓ WG and
175 g/kg (FR70) SGR in FR80 and FR90 than control; ↓ FCR in
200 g/kg (FR80) FR50, FR60 and FR70 than other groups; no
225 g/kg (FR90) difference in survival;
Digestibility and digestive enzyme activity: ↑
ADC of DM in FR50; ↓ ADC of protein in FR80
and FR90; ↓ hepatopancreas protease with
increase FM substitution; ↑ amylase in FR60 and
FR70; Proximate composition: ↓ CL in control
than other groups; no difference in moisture,
CP, CF and ash
Candida utilis Shrimp 6.4 % (7T) 47.5 % 4 Performance: ↑ FBW in 15T than control; Gamboa-Delgado
(L. vannamei) 12.7 % (15T) lowest FBW in 100T et al., 2016
25.5 % (30T)
50.9 % (60T)
84.95 % (100T)
C. utilis (CU); Atlantic salmon 20 % (CU) 71 % 4 Performance: no difference in FBW; Intestine Grammes et al.,
Saccharomyces (Salmo salar L.) 20 % (SC) histopathology: examination of the distal 2013
cerevisiae (SC); 20 % (KM) intestine showed that all fish fed the SC diets
Kluyveromyces developed characteristic signs of SBM induced
marxianus (KM) enteropathy, while those fed the FM, CV or CU
diets showed a healthy intestine.
S. cerevisiae (SC) Rainbow trout 107 g/kg (SC20) 30 % 10 Performance: no difference in FCR; ↓ SGR in Huyben et al., 2017
Wickerhamomyces (Oncorhynchus 214 g/kg (SC40) WA60 than control; WA40 diet reduced
anomalus (WA) mykiss) 321 g/kg (SC60) bacterial diversity, whereas the WA60 diet
118 g/kg (WA20) increased the abundance of the pathogenic
239 g/kg (WA40) yeast Candida albicans and reduced lactic acid
355 g/kg (WA60) bacteria in the gut
S. cerevisiae Rainbow trout 21.4 % (SC) 30 % 6 Performance: ↓ WG and SGR than control; ↑ Huyben et al., 2019
(Oncorhynchus FCR than control; Blood biochemistry and
mykiss) haematology: no difference; Intestinal
histology: ↑ lamina propria inflammation than
control; Intestinal gene expression: ↓ TNFα,
IL1β, IL8 and CLD6
Brewer’s yeast (BY); Pacific white shrimp 1 % YH 25 % 8 Performance: ↑ WGR and SGR in YH than Jin et al., 2018
Yeast hydrolysate (L. vannamei) 1 % BY control; lowest FCR in YH; Proximate
(YH) composition: no difference in DM, CP, CL, and
(continued on next page)

19
V. Serra et al. Veterinary and Animal Science 25 (2024) 100381

Table 9 (continued )
Alternative protein Aquatic species Inclusion levels FM Time Effects Reference
source inclusion in (weeks)
the control
diet

ash; Expression of inflammation-related

genes: ↓ relative expression levels of tnf-α and
IL-1β genes in YH; no difference in alp gene
expression; highest expression of tnf-α and IL-1β
genes in control; Expression of immune-
related genes: highest expression of proPO in
the control intestine; ↑ dorsal and relish
expression in YH and BY than control; no
difference in lysozyme expression; ↑ penaeidin3a
and crustin expression in hepatopancreas of YH
Cyberlindnera jadinii Atlantic salmon 10 % (FM10) 676.8 g/kg 5 Performance: no difference in SGR; Gut Leeper et al., 2022
(S. salar) 20 % (FM20) microbiome: no difference in any of the alpha
diversity measures tested across the groups
Yarrowia lipolytica Nile tilapia 3 % (YL3) 28.5 % 5 Performance: ↑ WG in all groups than control; ↑ Neuls et al., 2021
(O. niloticus) 5 % (YL5) total and standard length of fish in YL7 than
7 % (YL7) other groups; Hematological parameters: no
difference in RBC, Hb, Hct, MCH, MCHC, MCV;
Immune response: no difference in total
leukocyte and thrombocyte counts; ↓
lymphocytes number in all groups than control;
↑ plasma LYS in all groups than control; no
difference in renal LYS; ↑ plasma nitrite/nitrate
levels in YL3 and YL5 than control; ↑ renal
myeloperoxidase in YL3
Brewer’s yeast Giant freshwater 78 g/kg (Y20) 26 % 6 Performance: ↓ growth in Y60; ↑ FCR in Y60 Nguyen et al., 2019
prawn 155 g/kg (Y40)
(Macrobrachium 232 g/kg (Y60)
rosenbergii)
Brewer’s yeast Thai Panga 90 g/kg (D30) 30 % 36 Performance: highest FBW, WG, SGR in D45; ↓ Pongpet et al.,
135 g/kg (D45) growth performance in D60 and D75 than D45; 2016
180 g/kg (D60) no difference in FCR, FE, PER and HSI; Blood
225 g/kg (D75) anaylses: no difference in RBC, Hb, Hct, MCV,
MCH, lymphocyte and platelet counts; no
difference in CHO and GLU; ↑ ACH50, LYS
activity and total immunoglobulin in all groups
than the control; Proximate composition: no
difference; ↑ redness and yellowness in the
control
Sporidiobolus Nile tilapia 5 g/kg (T2) - 13 Performance: ↑ FBW, WG, ADG in T3 and T4 Van Doan et al.,
pararoseus (O. niloticus) 10 g/kg (T3) than control; no difference in survival rate; 2023
20 g/kg (T4) Blood analyses: no difference in TP, globulin,
AST, ALT, CHO; ↑ ALB in T4; no difference in
RBC, WBC, Hb, Hct, MCV, MCH, MCHC;
Proximate composition: no difference in
moisture, CP, CL, ash; Total carotenoid: ↑ in
T4; Immunological parameters: ↑ LYS in T4; ↑
SOD in liver of T4 > T3 > T2; no difference in
MDA values; Gene expression: ↑ IL-1β and
TNF-α in spleen of T3 and T4; ↑ IL-1β in liver of
T4; Challenge test with Streptococcus
agalactiae: ↑ survival rate in T4
C. utilis Atlantic salmon 25 % 15 % 8 Performance: ↑ feed intake and higher growth Sahlmann et al.,
(S. salar L.) Two rate than control; Histology and Morphometry: 2019
periods: FW Immunohistochemistry: decreased length and
(0–28 days) number of CD3 labeled cells in the simple folds
and SW of fish fed control diet; Gene expression in DI
(28–56 and spleen: no difference in IL-8 expression in
days) DI; ↑ Mhc1in DI than control; ↓ mhc1 in the SW
period as compared to the FW period for both
control and yeast;
Protein levels of cytokines: ↓ IFNγ, TNFα, IL-
1β, IL-8 and in DI of fish fed yeast compared to
control
Intact S. cerevisiae Arctic charr 289 g/kg (ISC); 46.8 % 14 Performance: ↓ FBW, SGR and WG in ESC and Vidakovic et al.,
(ISC); (Salvelinus alpinus) 172.6 g/kg (ESC); RHO than control; no difference in FCR among 2016
Extracted 260.1 g/kg (RHO); groups; no difference in HSI and VSI;
S. cerevisiae (ESC); 220 g/kg (MYE) Apparent digestibility: ↓ ADC for DM in RHO;
Rhizopus oryzae ↑ ADC for CP in MYE and ESC than ISC and RHO
(RHO);
Blue mussels
(Mytilus edulis)
(MYE)
(continued on next page)

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V. Serra et al. Veterinary and Animal Science 25 (2024) 100381

Table 9 (continued )
Alternative protein Aquatic species Inclusion levels FM Time Effects Reference
source inclusion in (weeks)
the control
diet

Nucleotide Pacific white shrimp 1 % (NT10) 17 % 8 Performance: ↑ WG, SGR and PER in NT50 Xiong et al., 2018
(NT)-rich yeast (L. vannamei) 3 % (NT30) than control; no difference in survival;
5 % (NT50) Proximate composition: ↑ protein content in
whole body of NT50 than control; no difference
in DM, CL, ash of muscle; Serum biochemical
parameters: ↑ TP and TG in NT50 than others; ↓
AST and ALT in NT50 than control; no
difference in GLU and CHO; ↑ PO and LYS in
NT50; Intestinal morphology: ↑ fold height
and fold width in NT30; ↓ microvillus height in
the control; Expression of immune-related
genes: no difference in acp; ↑ alp and lzm in
NT30
Yeast extract (YE) Pacific white shrimp 4 % (D15) 25 % 6 Performance: No difference in WGR, SGR; ↑ Zhao et al., 2017
(L. vannamei) 8.5 % (D30) FCR with increasing level of YE; Digestive
13 % (D45) enzymes in hepatopancreas: ↑ trypsinase with
18 % (D60) increasing level of YE; ↓ lipase activity than
25 % (D100) control; Proximate muscle composition: no
difference

Abbreviations: ↑: improvement; ↓: decrease; ACH50: Alternative complement activity; acp: acid phosphatase; ADC: apparent digestibility coefficient; ADG: average
daily gain; ALB: albumine; ALP: alkaline phosphatase; alp: alkaline phosphatase; CHO: cholesterol; CL: crude lipid; CLD6: claudin-6; CORT: cortisol; CP: crude protein;
DI: distal intestine; FBW: final body weight; FCR: feed conversion ratio; FDY: flash dried yeast; FE: feed efficiency; FER: feed efficiency ratio; FO: fish oil; FW:
freshwater; GLU: glucose; Hb: haemoglobin; Hct: haematocrit; HDL: high density lipoprotein; HSI: hepatosomatic index; IL-1β: interleukin-1β; IL-8: interleukin-8; IFNγ:
interferon-γ; LDL: low density lipoprotein; LYS: lysozyme; lzm: lysozyme; MCH: Mean corpuscular hemoglobin; MCHC: Mean Corpuscular hemoglobin concentration;
MCV: Mean corpuscular volume; MDA: Malondialdehyde; mhc1: major histocompatibility complex 1; MPO: Myeloperoxidase; PER: protein efficiency ratio; PO:
phenoloxidase; RBC: erythrocytes; SGR: specific growth rate; SOD: superoxide dismutase; SW: seawater; TAC: Total antioxidant capacity; TG: triglyceride; TGC:
Thermal growth coefficient; TNFα: tumor necrosis factor α; TP: total protein; VSI: viscerosomatic index; WG: weight gain

nutrition are relatively few compared to those using yeasts, although commercial SCP concentrate obtained from the bacteria Corynebacte­
their effectiveness has been repeatedly proven. The utilization of SCP rium ammoniagenes (named PROTIDE) through a specific fermentation
produced from M. extorquens bacteria, known for the ability to consume process, has been tested in whiteleg shrimp, demonstrating the suit­
methanol, was evaluated in rainbow trout to replace a portion of SBM ability of this FM substitute at percentages higher than 10 and lower
(5–10 %) for 12 weeks. Results showed that an inclusion of up to 10 % than 20 (Hamidoghli et al., 2019). Significant improvement in growth
improved fish survival, despite the slightly lower weight gain in fish fed and feed utilization has been observed in barramundi fed diets supple­
the 10 % SCP diet, partly due to lower FI, resulting in a lower palatability mented with SCP derived from Methylococcus capsulatus at different
of the diet (Hardy et al., 2018). Therefore, incorporating components percentages of inclusion (10, 20, and 30 %). This SCP proved to be
that may increase palatability could further improve the results ob­ highly palatable for barramundi, and healthy for the liver as indicated
tained. In white shrimp, the addition of R. sphaeroides and A. marina by HSI, triglyceride, and histopathology results (Woolley et al., 2023).
bacteria at different concentrations (1, 3, and 5 %) has been shown to Despite the numerous studies mentioned above have demonstrated
provide some immunostimulant effect, promote growth, and increase beneficial effects in several aquaculture species of fish and shrimp fed
survival of animals (Chumpol et al., 2018). Indeed, shrimps fed with the SCP-based diets (i.e. improvements in survival and growth performance,
lowest concentration of bacteria (1 %) showed a higher growth perfor­ modulation of the intestinal microbiota, enhancement of innate immu­
mance and survival rate (85 %); shrimps fed the diet with 3 % bacterial nity, and increased resistance to stress), there are still challenges to face
SCP showed the highest total hemocyte count (THC) value, an indicator in the increase of production, processing, and economics of SCP. Since
of health, while activities of phenoloxidase and SOD were significantly the main industrial limitation of SCP is economic, it is necessary to
higher in all the groups compared to the control (Chumpol et al., 2018). develop strategies to reduce production costs and increase productivity,
Chen et al. (2020) tested the use of the protein of Clostridium autoetha­ for example by developing more efficient fermentation systems.
nogenum (CAP), a natural non-pathogenic strain used in the gas
fermentation processes for biofuel production, as FM replacer in black 6. New proposals for alternative protein sources to fishmeal
sea bream diet for 70 days at six different inclusion percentages (4.85,
9.70, 14.55, 19.40, 38.80 and 58.20 %). Results showed that CAP could Like the animal by-products derived from poultry or livestock used in
be added to the black sea bream diet to replace up to 58.20 % of FM fish nutrition, crustacean processing discards contain valuable products
protein without any negative effects on the growth performance of an­ including proteins, lipids, astaxanthin, organic acids, essential amino
imals, and did not markedly affect the antioxidant capacity, measured as acids, chitin, and calcium (Prakash et al., 2012). For example, snow crab
activity of hepatic SOD, CAT, and MDA (Chen et al., 2020). These results processing discards can potentially be recovered from processing in­
suggest that higher inclusion levels of CAP than these may also be tested dustries, and converted into by-products such as crab meal with a higher
in the same aquatic species. Another study demonstrated that CAP can content of CP and lipids (~51 % and ~16–25 %, respectively) or
be used in the largemouth bass diet at a level of inclusion up to 152 g/kg recovered for their high content of astaxanthin (33.8–39.6 µg/g) (Burke
(150 g/kg FM replacing) without negative effects on growth, feed uti­ and Kerton, 2023). Other crustaceous species have returned to the media
lization, and intestinal histology (Yang et al., 2023). In another fish spotlight for their national interest as invasive species for aquatic eco­
species, grass carp, the replacement of SBM with 50 g/kg CAP signifi­ systems. This is the case of the blue crabs Callinectes sapidus (Rathbun,
cantly improved the feed efficiency and WG, while higher CAP inclusion 1896), Portunus segnis (Forskål, 1775), and Procambarus clarkii (Girard
(100 g/kg) reduced the survival of fish and led to liver damage, which 1852), known as Louisiana crayfish.
may be ascribed to the low arginine content in CAP (Wei et al., 2018). A The blue crabs, native to the American coast and Indo-Pacific Ocean,

21
V. Serra et al. Veterinary and Animal Science 25 (2024) 100381

respectively, have established themselves in the Mediterranean Sea 7. Conclusions

(Mancinelli et al., 2021; Marchessaux et al., 2022; Shaiek et al., 2021)
and neighboring waters, where they are currently considered an inva­ The most relevant result emerging from this study consists in high­
sive alien species (Zenetos et al., 2005). Furthermore, the areas of lighting that the alternative ingredients used up-to-date to fully or
expansion include also the Adriatic Sea and the Black Sea. Their bio­ partially replace FM may affect several health parameters of aquatic
logical characteristics such as early sexual maturity, rapid growth rates, species. In general, the inclusion levels of the different protein sources,
opportunist diet, high reproductive rates, generalist habitat use, plant- and animal-derived, ranged from 10 to 80 % and from 2 to 100 %
long-range larval dispersal, and effective physical and aggressive respectively, in full or partial replacement of FM. The parameters posi­
behavior (Castriota et al., 2022; Mancinelli et al., 2017), make blue crab tively affected are the growth performance, followed by the improve­
species efficiently invasive and with high potential of successful spread ment of the immune status and antioxidant defense, and consequently a
across sea areas. Additionally, their biological traits imply that they better general health, welfare, and fillet quality. Studies have shown a
have the potential to impact benthic communities at multiple trophic high variability of the inclusion levels, which could vary depending on
levels. With similar biological characteristics to blue crabs, the Louisiana the species and time of administration, as well as on the protein source
crayfish, which originated in North America, is an invasive exotic spe­ production process. However, results clearly demonstrated that above a
cies of European importance (Black List), European Union Commission certain amount, the different protein sources can exert negative effects
Implementing Regulation (2017), now widely spread in national and on fish growth performance, body composition, metabolic activities, and
European internal sea waters. For the species included in this list, the other biological parameters due to their ANFs (especially in the case of
same Regulation allows all eradication measures, including capture and plant-protein sources). Although replacing FM with plant-based in­
subsequent disposal. However, today, the blue crabs are not yet included gredients is considered environmentally sustainable, it should be
in this list. considered that such a substitution would shift the demand for resources
Some studies have emphasized the high nutritional qualities of from oceans to land, potentially adding pressure to terrestrial food
Mediterranean blue crab meat (Küçükgülmez and Çelik, 2008; Zotti production systems, and impacting the environment, biodiversity,
et al., 2016) and Lousiana crayfish (Shahidi et al., 1998; Zaglol and availability, and prices of crops.
Eltadawy, 2009). It is evidenced that in C. sapidus blue crab, protein, fat, New aquatic food resources to be commercially attractive should be
ash, and moisture of the breast, claw meat and hepatopancreas can be available in large quantities, and competitively priced. At present,
averaged of 19.05, 0.59, 2.10 and 76.85 g/100 g, respectively, with low availability and low cost remain the major limitations for the use of
differences of the protein contents in claw meat (19.55 g/100 g) than several new alternatives in aquaculture feed.
both breast meat and hepatopancreas (18.81 g/100 g) (Küçükgülmez Not all the new protein sources discussed in this review are available
et al., 2006). Similar results of the proximal compositions of C. sapidus for the aquaculture feed industry and their direct use for aquatic feeding
blue crabs belonging to different sexes were observed by Tufan (2023). may be limited by several factors, including an unbalanced AA profile, a
The average protein content in male and female blue crabs was 18.79 % low protein quantity, or the presence of ANFs.
and 19.11 %, respectively. The fat content in male crabs ranged from Plant-based by-products are commercially available, but their
0.46 to 0.69 %, whereas the amount in females ranged from 0.63 to 0.92 nutritional value is often too low to meet the nutritional requirements of
%, with a moisture and ash content in all of the body parts of both sexes some aquatic species, making necessary additional processing steps,
varying between 78.62 and 76.73 % in males, and between 2.29 and which would also increase production costs.
2.39 % in females, respectively. Animal by-products are commercially available in large quantities
Less data are available in the literature about the nutritional and are commonly used as aquatic feed ingredients. In some European
composition of Lousiana crayfish. The most recent data, relating to the countries, consumer acceptance is limited, due to general misinforma­
whole product or meal, record a protein content varying between 40 and tion, or for food safety reasons.
75 % DM, a balanced AA profile, a high ash content, and a rather low Furthermore, it should be considered that it is unlikely that a single
lipid content in fat. Specifically, the chemical composition and nutritive protein source can satisfy the nutritional needs of a certain aquatic
value of crayfish showed mean values of TP, fat, ash, and cholesterol species, therefore, it is advisable to mix different protein sources to
contents of 13.88 %, 1.76 %, 1.52 % and 13.575 mg/100 g respectively. exploit the nutritional properties of each ingredient, observing syner­
Moreover, crayfish showed a higher content of PUFA (73.6 %) with 56.5 gistic or antagonistic effects. It follows that the future of aquatic feed
% and 15.08 % mono-ionic and poly-ionic fatty acids. Minerals con­ formulations will probably be based on the blend of different protein
centration levels were 1.32 %, 506.33, and 415.63 ug/g for phospho­ sources, both of vegetable and animal origin. However, future research
rous, iron, and magnesium respectively (Zaglol and Eltadawy, 2009). is necessary to determine which alternative proteins are the most suit­
Overall, the crayfish meal is characterized by a high content of chitin (8 able, in what proportions they should be included in diets, and how their
%) and carotenoids (119 mg/kg), of which approximately 90 % is made nutritive value could increase, considering also their environmental
up of astaxanthin (Shahidi et al., 1998), which makes this ingredient impact.
very interesting for the diets of fish species of commercial interest in The other main global issue that aquaculture is expected to face in
which coloring has added value, such as sea bream and rainbow trout. the future is the progressive growth of the sector, which will have to
However, the typical color of blue crab claws is due to a natural pigment. satisfy the increasing demand for protein from an expanding global
These species are commonly consumed by human as food, but due to population. The aquaculture industry is large and complex and can
their nutritional characteristic, their processing waste could be used as include the possible farming of more than 650 species of fish, shellfish,
valid feed ingredients or replacers to the FM. However, today its use is aquatic plants, and algae grown in a variety of marine, brackish, and
still little investigated and poorly considered. No less, it must be freshwater systems.
considered that, in addition to being intended for food production, these The global aquaculture policy priorities and outcomes do differ
species are included in the list of (European Union Regulation, 2024) among countries (e.g. Europe, USA, Asia, etc.) for degree of success as
Reg. (EU) 1143/2014, which allows all eradication measures, including measured by growth in fish supply and export, value chain development,
capture and subsequent disposal. Considering the emergency resulting environmental and spreading disease consequences, and distribution of
from the high proliferation of invasive species such as the blue crab and benefits. The agro-climatic conditions, the economic policies, and the
the Louisiana crayfish, their usefulness as a new alternative source of cultural orientation of a given country definitely affect the integration of
animal proteins for aquaculture could be considered, after fishing and aquaculture into food policies.
subsequent processing, safeguarding the feed safety aspects. However, to consider these sources cost-effective and above all sus­
tainable for their use in the future, other factors should be taken into

22
V. Serra et al. Veterinary and Animal Science 25 (2024) 100381

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