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Review

Fish Viscera Hydrolysates and Their Use as Biostimulants for Plants as an Approach towards a Circular Economy in Europe: A Review

by
Haizea Domínguez
1,
Bruno Iñarra
1,*,
Jalel Labidi
2 and
Carlos Bald
1
1
AZTI, Food Research, Basque Research and Technology Alliance (BRTA), Parque Tecnológico de Bizkaia, Astondo Bidea, Edificio 609, 48160 Derio-Bizkaia, Spain
2
Biorefinery and Processes Research Group, University of the Basque Country UPV/EHU, Plaza Europa 1, 20018 Donostia-San Sebastián, Spain
*
Author to whom correspondence should be addressed.
Sustainability 2024, 16(20), 8779; https://doi.org/10.3390/su16208779
Submission received: 19 July 2024 / Revised: 1 October 2024 / Accepted: 4 October 2024 / Published: 11 October 2024
(This article belongs to the Section Sustainable Food)
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Abstract

:
Crop production has become a priority issue in recent years because of the exponential growth of the world’s population and the need to find substitutes for chemical fertilizers. The latter is under the spotlight in order to achieve a more sustainable approach in a cost-effective way. Biostimulants have gained attention as an alternative to chemical fertilizers. Although they are not considered fertilizers as inputs of nutrients, they stimulate plants’ nutrition and tolerance to stress, among other characteristics. In the literature, amino acid-based biostimulants have been found to be effective. This review focuses on the effectiveness of biostimulants, their presence in the global market, and their production with fish by-products as a source, using enzymatic hydrolysis and autolysis, with a particular focus on fish viscera, their possibilities in the agricultural sector, and their availability in Europe for possible opportunities. Fish viscera protein hydrolysates for biostimulant production seem a feasible alternative to fishmeal production in Europe, especially in areas located far from fishmeal plants.

Graphical Abstract

1. Introduction

Fisheries can be the most economically important sector in many countries. Among them we can find China, Chile, Norway, Egypt, and Nigeria [1]. According to FAO [1], worldwide fishing and aquaculture production increased in 2020, reaching 90.3 million tonnes and 87.5 million tonnes, respectively. In parallel with fish, the volume of fish by-products also increases. Fish by-products (head, skin, scales, bones, and viscera) constitute between 60% and 70% of the weight of whole fish [2]. By-products can be disposed of or used for other purposes, such as the production of fishmeal or fish protein hydrolysates with bioactive peptides, due to their high protein and oil contents. If not used, they may cause environmental, health, and economic problems [3]. Therefore, the valorization of fish by-products, especially viscera, must be fully implemented to meet societal needs. As another example, transformed by-products can be used as ingredients for the formulation of bio-based fertilizers or biostimulants. This alternative may be interesting in areas where there are no fishmeal production plants nearby. Thus, some fertilizers produced from fish by-products are currently on the market, some of which are even authorized for organic agriculture [4]. Additionally, the combination of hydroponics and biostimulants presents a promising environmentally friendly production strategy for the next decades for vegetable growth, which requires further research [5]. Previously published reviews about fertilizers from fish by-products do not focus specifically on the use of viscera, whereas those focusing on fish viscera hydrolysates present only the food, nutraceutical, and feed applications. Thus, the aim of the present review is to highlight the possibilities of the production of fish viscera protein hydrolysates and their use as bio-based fertilizers and plant biostimulants for the European bioeconomy, as well as the need to carry out more research in this field.

2. Bio-Based Fertilizers for Plants

Owing to the exponential growth of the human population, the exploitation of natural resources is increasing. These resources are, in most cases, non-renewable and perishable. Therefore, the use of alternative sources for food production should be focused on maintaining the stability of food availability [6].
Most fertilizers require phosphate rock to be produced. Approximately 90% of the phosphate rock is imported into Europe, which makes it very vulnerable to the rising prices of raw materials. The demand for phosphorus and nitrogen is expected to increase in the next few years, which could lead to geopolitical problems [6,7]. Additionally, the use of phosphorus and nitrates in fertilizers provokes leaky losses in soil, and nutrients can run off into surface waters, polluting the environment and causing harm to aquatic ecosystems [6]. To reduce the number of toxic nitrates in the soil, the EU Council Directive of 12 December 1991 concerning the protection of waters against pollution caused by nitrates from agricultural sources (91/676/EEC) called for a significant reduction in the number of nitrogen-containing fertilizers used in agriculture and horticulture. Therefore, it is necessary to find new alternatives to minerals, like recycled organic matter, and to improve the efficiency of fertilization, reducing its environmental impact. There is also a need to recirculate nutrients, close the loop, and prevent their dissipation into the environment. For fertilizers, which are typically composed of minerals, some of the raw materials can be substituted with residual biomass from animals [8].
In this way, animal by-products that might otherwise end up in landfill could be revalued and repurposed, increasing resource efficiency. In fact, the availability of raw materials to produce bio-based fertilizers (BBFs) is high, and farmers from different countries within Europe have common preferences for BBFs with similar nutrient contents but lower prices than chemical fertilizers [9]. BBFs are promising alternatives to traditional synthetic fertilizers and can help to promote sustainable agricultural practices.
However, several disadvantages and barriers associated with bio-based fertilizers have been identified. These include unpleasant odors, time-consuming processing, variable compositions, and the slow mineralization and release of nutrients [6,10]. Additionally, BBFs face challenges related to the presence of antibiotic and microplastic residues, the toxicity of heavy metals, pathogen exposure, and the accumulation of salts. Despite these issues, BBFs offer opportunities to improve crop quality, increase micronutrient uptake in plants, promote soil biodiversity, and aid in soil remediation [6].

2.1. EU Fertilizer Product Regulation

In fertilizer product regulation, Regulation 2019/1009 of the European Commission [11], a wider range of products is covered apart from fertilizers. Additionally, end-of-waste status is established, with which materials that constitute waste can cease to be waste if they are contained in a compliant EU fertilizing product.
According to Regulation 2019/1009 [11] and as shown in Table 1, products are categorized into seven Product Function Categories (PFCs). Fertilizers are products whose function is to provide nutrients to plants or mushrooms, and they can be organic, organo-mineral, or inorganic. A liming material’s function is to correct soil acidity. Soil improvers (inorganic or organic) improve or protect the physical or chemical properties, structure, or biological activity of the soil to which they are added. The function of the growing medium is to maintain, improve, and protect the physical or chemical properties, structure, or biological activity of the soil to which it is added. Inhibitors may improve the nutrient release of a product that provides plants with nutrients by delaying or stopping the activity of specific groups of microorganisms or enzymes related to nitrification, denitrification, or urease activity. The function of plant biostimulants is to stimulate plant nutrition processes without considering the nutrient content of a product, with the objective of improving one or more characteristics of the plant or plant rhizosphere (nutrient use efficiency, tolerance to abiotic stress, quality traits, and availability of confined nutrients in soil or rhizosphere). They can be microbial or non-microbial. Fertilizing product blends are made of two or more fertilizing products that are already CE-marked.
An EU fertilizing product will be characterized by its component materials that shall comply with the requirements for one or more of the Component Material Categories (CMCs) listed in Table 2. Products are composed of at least one CMC or might contain more than one CMC. CMCs 3, 4, 5, 12, 13, 14, and 15 must undergo a defined recovery operation, and the resulting recovered materials must comply with relevant requirements.
With respect to the safety of plant biostimulants, according to Regulation 2019/1009 of the European Commission [11], contaminants must not exceed the limit values established for certain elements (Table 3), as they can pose a risk to human, animal, and plant health, and they can also accumulate in the environment and enter the food chain. The information provided by the producer must be the physical form of the biostimulant, the production and expiration date, the application method, relevant instructions related to the efficacy, and the effect claimed in the target plants. Regulation 2019/1009 of the European Commission requires demonstrating the effects claimed on the label of the biostimulant with evidence, and such evidence can be evidence that was published in the literature or that comes from experimental data from field trials [12].

2.2. Biostimulants

As an alternative to chemical fertilizers, we can find biostimulants, which are formulated products of biological origin that can be used to stimulate plant growth and increase yields [12]. Unlike bio-based fertilizers, they act as nutrient sources for plants, but they stimulate their metabolism, improving nutrient uptake. Biostimulants act on the metabolic and enzymatic pathways of plants, improving productivity and crop quality [13]. Hydrolysates of by-products are usually animal sources for biostimulants, which are normally produced via alkaline or enzymatic hydrolysis [13], and food waste streams are considered important precursors for biostimulant development.
Depending on the composition and the expected results, biostimulants can be applied to soil or leaves, and their effects are species- and product-specific [14]. To address this specificity, information and data that enable farmers to discriminate among products with different levels of effectiveness are needed [15]. Leaf permeability is a crucial factor, and the penetration of biostimulants into plant tissue is a necessary condition for reliable efficiency [16]. Additionally, foliar application increases amino acid and peptide availability for their uptake by plants by reducing competition with soil microorganisms compared with soil application [17].
The largest consumer and producer of biostimulants worldwide is the United States [18]. Farmers, investors, regulators, consumers, and scientists are still learning about biostimulants and their role in agriculture [19]. Among the most important barriers to introducing bio-based fertilizers and biostimulants in Europe are the low level of technological readiness, the biological waste collection system (to ensure the availability of secondary raw materials), and legislation [8].

2.3. Amino Acid-Based Biostimulants

Studies have shown that organic compounds such as amino acids promote the growth of several horticultural plants [20,21,22,23]. The synthesis of amino acids demands a high energy consumption in plants, so their foliar application in agriculture is a usual practice, as it allows plants to save energy on amino acid synthesis by regulating nitrogen acquisition in roots to increase the pace of their reconstruction, especially during critical times such as transplantation or climatic stress [24,25]. Amino acids are also used as chelators of metal ions. The combination of essential micronutrients with amino acids in the form of aminochelate fertilizers can accelerate their absorption and transport within the plant and thus increase plant growth [26,27].
Glutamic acid plays an important role in the biosynthesis of proline and other nitrogen-containing compounds, in addition to having a positive effect on the photosynthetic activity and major production of fruits in plants [22,28]. In the literature, glutamic acid is the most abundant amino acid in fish protein hydrolysates produced from both enzymatic hydrolysis and silage [29,30,31].
In addition to glutamic acid, other amino acids have beneficial effects in crops. According to the work of Ashraf et al. [32], proline stimulates plant defenses against biotic and abiotic stress. In fact, several studies have shown that proline accumulation is high in cells adapted to high concentrations of salt [33] because it mitigates the effect of sodium chloride on cell membrane disruption [34] and that proline neutralizes increased ethylene production in stressed plants suffering from drought [35]. Flores et al. [36] reported that arginine plays an important role in nitrogen storage and transport in plants during both biotic and abiotic stress. However, tyrosine, methionine, and lysine are the amino acids usually applied in biostimulants [23].
Some examples of commercially available amino acid-based plant biostimulants include Radifarm produced by Valagro (Atessa, Italy), which stimulates root growth; Megafol produced by Valagro (Atessa, Italy), which stimulates plant growth during abiotic stress; and SeaActiv, produced by Timac AGRO (Navarra, Spain) and derived from algae, which reduces abiotic stress and maintains the yield of crops.

3. Fish Protein Hydrolysates

After the production of fishmeal, the production of fish protein hydrolysates (FPHs) is the most common valorization route for fish by-products. Fish protein hydrolysates are rich in soluble proteins, highly digestible, and sometimes even antioxidant and antimicrobial properties [37], among others. FPHs contain mainly free amino acids and low-molecular-weight peptides, and hydrolysis can be alkaline, acidic, or enzymatic.

3.1. Chemical Hydrolysis

Alkaline and acidic hydrolysis require strong experimental conditions and extreme precautions [38,39], and such conditions attack all peptide bonds, resulting in a very high degree of hydrolysis and the release of free amino acids. However, it also destroys several amino acids: tryptophan is usually destroyed with acidic hydrolysis, cysteine, serine, and threonine are partially lost, and asparagine and glutamine are converted into their acidic forms [17]. The large use of acids and alkalis can also lead to an increase in salinity in the FPH. In addition, racemization occurs during chemical hydrolysis. This means that there is a conversion of the free amino acids from the L-form to the D-form, which may cause some problems in terms of the effectiveness of the FPHs, for example, as biostimulants, as plants cannot directly use D-form amino acids in their metabolism [17].

3.2. Enzymatic Hydrolysis

Given the disadvantages associated with chemical hydrolysis, enzymatic hydrolysis is the most widely used method because of its mildness, ease of control, and lack of residual organic solvents [40]. Compared with chemicals, enzymes hydrolyze proteins more gently, allowing the production of low-molecular-weight peptides, dipeptides, or even free amino acids depending on the experimental conditions. A schematic flowchart of the production of fish protein hydrolysates using enzymes is shown in Figure 1.
The enzymes used in hydrolysis can be classified into two types on the basis of their origin. Exogenous enzymes, which are commercially available, are added to the sample to be hydrolyzed, and they are typically extracted from plants, animals, and microbes. Among these, Alcalase is the most referenced in the literature [41,42,43,44,45], but others such as Protamex [41,46], Flavourzyme [29,46], and Protana Prime [30] are also used. Some examples of published works on the enzymatic hydrolysis of fish with commercial enzymes are shown in Table 4.

3.3. Endogenous Enzymes of Fish

Enzymes can also be naturally present in fish, known as endogenous enzymes. The largest group of enzymes in fish are proteases, which catalyze the hydrolysis of peptide bonds via different mechanisms [47]. Proteases are classified into two groups depending on their substrate specificity. Exoproteases or peptidases cleave the peptide bond of the terminal amino acid (amino/carboxyl end) of the polypeptide chain, whereas endoproteases or proteinases cleave the internal bonds of the chain [47,48].
As explained by Vannabun et al. [49] and Sriket [50], fish viscera contain different types of digestive proteases: serine, aspartic/acid, cysteine/thiol, and metallo-proteases. Inside the serine type, trypsin can be found, which is stable and active at pH values between 7.5 and 8.5 and is present in the pyloric caeca of fish [51]. Trypsin not only cleaves ingested proteins but is also involved in the activation of precursor forms of several other digestive proteases, such as chymotrypsin [52]. Moreover, pepsin, which is secreted in the stomach of a fish, is present in the aspartic/acid group, and its peak activity occurs under acidic conditions [52].
The use of fish proteases can reduce the economic cost of the process, as the price of commercial enzymes is high. The use of trypsin has increased because of its unique features: stability and activity over a wide range of pH values (8–11) and temperatures (38–70 °C) [47].
The process of hydrolysis using endogenous enzymes is known as autolysis, and it can be performed in two ways. The most common method is silage or acid autolysis, very often used in areas with high fishing density but where there are no fishmeal processing plants nearby or where they are not economically feasible [53]. For example, in 2014, more than 250,000 tonnes of fish by-products were preserved by silage only in Norway, representing 41% of the total fish by-products generated in the country [54]. Silage consists of the liquefaction and stabilization of minced fish at room temperature (see flowchart of the process in Figure 2). Typically, formic acid is added to achieve a pH range of 3.5–4.5 to prevent microbial growth [55]. Protein hydrolysis occurs owing to the aspartic endoproteases present in the fish viscera, particularly pepsin [52], which has been reported to be highly stable at pH values between 1 and 5 [49]. Pepsin provokes the breakdown of proteins and makes it possible to obtain low-molecular-weight peptides [56]. Acid-preserved fish silage can completely or partially replace fishmeal in feed for fish with a high digestibility; in fact, a 6-day-old silage can contain a protein content similar to that of good-quality fishmeal [57]. However, due to chemical reactions between α amino and aldehyde groups present in amino acids, the concentration of some amino acids can decrease over time [3].
The other alternative method is autolysis (Figure 3), which requires higher temperatures than silage and does not necessarily require an acidic pH. The autolysis conditions (pH, solid/liquid ratio, and temperature) usually need to be optimized for each raw material used. Response surface methodology is a common method used to optimize the experimental parameters of fish autolysis [59,60,61]. However, the efficiency of the production of free amino acids in both silage and autolysis can be low to medium compared with that of enzymatic hydrolysis.

3.4. Use of Fish Protein Hydrolysates in Agriculture

When fish byproducts do not meet the standards to be processed into fishmeal, they can be converted into liquid or solid forms of fertilizers, as when fish viscera protein hydrolysates are used as ingredients. Historically, civilizations such as Egyptians, Incas, Mayans, and Norwegians have used fish by-products to fertilize their crops [62]. Fish protein hydrolysates can be used as biostimulants to increase plant nutrition, fruit and vegetable quality, and crop productivity [63,64]. However, phytotoxic effects and growth depression have also been reported [65]. In addition, there was some concern about the use of animal-derived protein hydrolysates as biostimulants, leading to the implementation of European Regulation 354/2014 and later European Regulation 2021/1165, which prohibit the application of these products on the edible parts of plants in organic production. However, Corte et al. [66] reported that protein hydrolysates did not negatively affect eukaryotic cells or soil ecosystems and that they can be used in farming without causing any harm to the environment or human health.
Among the CMCs mentioned in Regulation (EU) 2019/1009 [11], composting (CMC 3) is one of the most relevant methods to valorize fish by-products. Composting is a biotransformation process of organic materials into stable and complex macromolecules under the action of microorganisms such as fungi, bacteria, or enzymes [4]. It was reported that soil fertilization with compost produced with fish by-products increases the leaf yield of lettuce and increases the content of nitrogen, phosphorus, potassium, sodium, calcium, and magnesium in leaves [4].
According to Ahuja et al. [62], OMRI (Organic Materials Review Institute) has allowed the use of 154 commercial fish fertilizers until 2020, but only a few have been deeply investigated in scientific research, most of them in the United States and Canada. Some examples are given by Madende and Hayes [12]. These fertilizers are produced in the form of pellets, hydrolyzed powder, and emulsion-based liquids.

4. Fish Viscera

Viscera constitute 8–15% of the whole fish weight and contain high-quality proteins, long-chain omega-3 fatty acids, vitamins A and D, and minerals such as Fe, Zn, and Se [55]. In Europe alone, it is estimated that between 200 and 400 million tonnes of fish viscera are generated annually from aquaculture, with over half originating from salmon produced in Norway [67]. Table 5 shows that in the whole picture of Europe, in 2021, more viscera were produced from captures rather than from aquaculture (607,000–1,140,000 tonnes vs. 216,000–406,000 tonnes, respectively). However, the viscera obtained from captures can sometimes be thrown into the sea by fishermen to better preserve the captured fish and to save space, so that the real number of the weights of the viscera landing is much lower than the one proposed in Table 5. Instead of processing plants, fish gutting at home, restaurants, and hotels can make the collection of viscera difficult logistically.
Among the fish species most farmed in Europe, salmon tops the list, followed by trout, gilt-head bream, seabass, carp, and turbot (Table 6). Among these species, between 1,554,000 and 1,813,000 tonnes of by-products and between 207,000 and 388,500 tonnes of viscera are generated in total. The production of salmon in Norway was only approximately 1,600,000 tonnes of live weight in 2021 [67], which means that between 128,000 and 240,000 tonnes of viscera can be valorized.

Fish Viscera Protein Hydrolysates

In general, fish viscera are disposed to landfills, to the sea, or used in the production of fishmeal where rendering plants are present nearby. All the problems surrounding climate change and the rise of the circular economy make the first two choices unacceptable. However, their processing in fishmeal plants can be difficult because they deteriorate very quickly because of the high microbial load of the gastrointestinal tract, together with their storage and transportation to the fishmeal plants under inappropriate conditions, and because of their content of water, which can reach 80% [40], resulting in high energy costs in the rendering process [53,70]. For these reasons and owing to their protein content, the production of fish viscera protein hydrolysates may be a suitable route for their valorization. Moreover, the main advantage of using viscera for hydrolysis is the possibility of using the endogenous enzymes (pepsin, trypsin, etc.) contained in the digestive system, which are very effective and can reduce the economic cost of the process by producing silage and autolysates, as mentioned in the previous section. Among the studies that have used endogenous enzymes for autolysis and even optimized the experimental conditions are Domínguez et al. [60] and Nikoo et al. [61]. The enzymatic hydrolysis of fish viscera seems to be a promising and profitable process to valorize these by-products.
The viscera of some species may have a high oil content, which can be used for feed, and the protein content can be used to obtain protein hydrolysates. There is no published work on the production of fish viscera hydrolysates for biostimulant purposes. In fact, some specific words related to this topic were searched in Scopus [71], and the results are displayed in Figure 4, where it can be observed that in the last 25 years, publications about fish viscera hydrolysis and autolysis increased until they reached their peak during the last 5 years. However, publications about fertilizers produced from fish viscera have not increased, and publications about biostimulant fertilizers produced from fish viscera are lacking. Moreover, the use of viscera hydrolysates seems to be a feasible option for the production of amino acid-based biostimulants, as they can comply with legislation. For example, Spanish legislation (RD 506/2013) establishes a minimum of 6% of free amino acids in dry matter for the composition of a biostimulant labeled as amino acids, and the viscera hydrolysates obtained with enzymatic hydrolysis and silage by the authors of the present review achieved percentages of free amino acids of 50.3 ± 3.7 and 49.2 ± 1.2 (D.M. basis), respectively [30]. The amino acid composition of fish viscera hydrolysates is influenced by the enzyme used, the fish species, and the hydrolysis parameters. As reported by Villamil et al. [40] for the composition of several viscera hydrolysates, the most common amino acid is Glu, followed by Asp and Arg or Gly, as well as Met, depending on the species. In an experiment for obtaining trout viscera hydrolysates, Glu, Lys, Leu, and Arg were the most abundant obtained through acid autolysis, whereas Glu, Leu, Ala, and Val were obtained via commercial enzymes [30].
With respect to the economic feasibility of processing fish viscera into biostimulants, a comparative study of different options to process fish co-streams by Venslauskas et al. [72] revealed the importance of having good-quality raw material and extraction via the same process as other valuable materials, such as fish oil, to make the process profitable. The different processes used to obtain viscera hydrolysates must be compared in terms of amino acid yield, yield of quality co-products, and processing costs, which are related mainly to the cost of the enzymes and the energy consuming steps (hydrolysis, enzyme inactivation, concentration through evaporation, and drying). The source of energy may also determine the environmental impact of the process [73]. However, if the final product is not provided in its dry powder form but rather as a liquid fertilizer, the energy consumption may be significantly lower. When the fish hydrolysate is derived for the production of fertilizers instead of other more valuable options, such as fish feed or nutraceuticals, the cost of the enzymes becomes significant, and the use of silage or autolysis can be a suitable alternative. However, the addition of exogenous enzymes makes the hydrolytic process more controllable, avoiding the variability in the endogenous enzymatic activity [74], and here, the agronomic efficiency of the final product, which depends on the FAA concentration and the amino acid profile, to be verified through adequate field trials, can make a difference. Thus, further research is needed in the field of the use of fish viscera hydrolysates as biostimulants to assess their technoeconomic feasibility and the environmental impact of their production, always complying with European Regulation 2019/1009, mentioned in Section 2.1.

5. Conclusions and Future Outlook

Although fish viscera are mainly used for the production of fishmeal or are simply disposed of in landfills, their use for the production of protein hydrolysates, which can be used as ingredients for biostimulants, seems a promising alternative for areas where fishmeal plants are not accessible. This option not only promotes a circular economy but also enhances plant nutrition and crop productivity thanks to hydrolysates rich in free amino acids. The availability of raw materials is assured for decades, and the use of other fish by-products can also be integrated into this value chain. The profitability of the production of fish viscera hydrolysates should be considered compared to the production of fishmeal in some cases. Amino-acid-based biostimulants produced from fish by-products appear as promising and effective products that will grow in the global market in the coming years. However, more studies are needed to evaluate the effectiveness of fish-derived products as biostimulants. It is crucial to compare the sustainability of different ways to produce bio-based fertilizers in terms of environmental, economic, and social impact compared to the currently used fertilizers of mineral origin. To obtain reliable data with this aim, scaled-up trials of the production of viscera hydrolysates using different approaches are needed to compare their performance and evaluate the quality of the products obtained. With continued research and innovation, fish-derived biostimulants have the potential to revolutionize sustainable agriculture and contribute significantly to global food security.

Author Contributions

Conceptualization, H.D., B.I., J.L. and C.B.; investigation, H.D., B.I. and C.B.; data curation, H.D.; writing—original draft preparation, H.D.; writing—review and editing, H.D., B.I., J.L. and C.B.; supervision, C.B.; funding acquisition, C.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research has been developed within the SEA2LAND project which has received funding from the European Union Research and Innovation H2020 program, contract No. 101000402 (this work reflects the views of the author(s) only, and the European Union cannot be held responsible for any use which may be made of the information contained therein). This paper is contribution No. 1239 from AZTI, Food Research, Basque Research and Technology Alliance (BRTA).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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Figure 1. Two schematic flowcharts of enzymatic hydrolysis of fish waste. Compiled from Domínguez et al. [30] on the left and Vázquez et al. [37] on the right.
Figure 1. Two schematic flowcharts of enzymatic hydrolysis of fish waste. Compiled from Domínguez et al. [30] on the left and Vázquez et al. [37] on the right.
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Sustainability 16 08779 g002
Figure 2. Two schematic flowcharts of acid autolysis or silage of fish waste. Compiled from Domínguez et al. [30] on the left and Arason et al. [58] on the right.
Figure 2. Two schematic flowcharts of acid autolysis or silage of fish waste. Compiled from Domínguez et al. [30] on the left and Arason et al. [58] on the right.
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Figure 3. Schematic flowchart of the autolysis of fish waste. Compiled from Domínguez et al. [60].
Figure 3. Schematic flowchart of the autolysis of fish waste. Compiled from Domínguez et al. [60].
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Sustainability 16 08779 g004
Figure 4. Results of the search in Scopus with different keyword combinations from 1952 to 2024.
Figure 4. Results of the search in Scopus with different keyword combinations from 1952 to 2024.
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Table 1. Product Function Category (PFC) of products according to Regulation 2019/1009 of the European Commission [11].
Table 1. Product Function Category (PFC) of products according to Regulation 2019/1009 of the European Commission [11].
Product Function Category (PFC)
  • Fertilizer
  (a) Organic
  (b) Organo-mineral
  (c) Inorganic
2.
Liming material
3.
Soil improver
4.
Growing medium
5.
Inhibitor
6.
Plant biostimulant
7.
Fertilizing product blend
Table 2. Component Material Category (CMC) of the products according to Regulation 2019/1009 of the European Commission [11].
Table 2. Component Material Category (CMC) of the products according to Regulation 2019/1009 of the European Commission [11].
Component Material Category (CMC)
(1)
Virgin material substances and mixtures
(2)
Plants, plant parts or plant extracts
(3)
Compost
(4)
Fresh crop digestate
(5)
Digestate other than fresh crop digestate
(6)
Food industry by-products
(7)
Microorganisms
(8)
Nutrient polymers
(9)
Polymers other than nutrient polymers
(10)
Derived products within the meaning of Regulation (EC) No 1069/2009 (animal by-products)
(11)
By-products within the meaning of Directive 2008/98/EC (industrial by-products)
(12)
Precipitated phosphate salts and derivates (struvite)
(13)
Thermal oxidation materials and derivates (ash)
(14)
Pyrolysis and gasification materials (biochar)
(15)
Recovered high purity materials
Table 3. Contaminant limit values (mg/kg dry matter) for plant biostimulants according to Regulation 2019/1009 of the European Commission [11].
Table 3. Contaminant limit values (mg/kg dry matter) for plant biostimulants according to Regulation 2019/1009 of the European Commission [11].
ContaminantLimit Value (mg/kg Dry Matter)
Mercury (Hg)1
Cadmium (Cd)1.5
Hexavalent chromium (Cr VI)2
Inorganic arsenic (As)40
Nickel (Ni)50
Lead (Pb)120
Copper (Cu)600
Zinc (Zn)1500
Table 4. Examples of the use of commercial enzymes to produce fish protein hydrolysates and the experimental conditions applied.
Table 4. Examples of the use of commercial enzymes to produce fish protein hydrolysates and the experimental conditions applied.
Raw MaterialEnzymeDosepHTemperature
(°C)		Time (Hours)Reference
Seabream heads
Seabass heads		Alcalase0.2% *8.2
8.5		57.1
58.4		3
3		Valcarcel et al. [44]
Tuna visceraAlcalase1% *8.5552Garofalo et al. [42]
Rainbow trout frames
and trimmings
Salmon heads		Alcalase
Alcalase		0.1% *
0.2% *		8.3
9		56
64		3
3		Vázquez et al. [45]
Cod visceraAlcalase1 g/100 g
of sample		Unadjusted5524Aspmo et al. [41]
Mackerel wasteAlcalase0.5% *7.5551Ramakrishnan et al. [43]
Rainbow trout visceraAlcalase +
Protana Prime		1% *7607Domínguez et al. [30]
Trout wasteAlkaline protease1% (enzyme
/substrate)		8601Korkmaz et al. [46]
Cod visceraProtamex1 g/100 g
of sample		Unadjusted5524Aspmo et al. [41]
Bighead carpFlavourzyme4% (enzyme
/substrate)		6.5506Alahmad et al. [29]
* Dose on the basis of the protein content in the sample.
Table 5. Quantification of captures, aquaculture production, and the estimated range of by-products and viscera weights for each case in every country of Europe. The estimated weight of by-products was calculated assuming 60–70% of the total weight, and in the case of the viscera, it was 8–15% of the total weight. All the data are expressed in tonnes. Data on captures and aquaculture, in 2021, were obtained from FishStatJ software 4.01.0 [67,68].
Table 5. Quantification of captures, aquaculture production, and the estimated range of by-products and viscera weights for each case in every country of Europe. The estimated weight of by-products was calculated assuming 60–70% of the total weight, and in the case of the viscera, it was 8–15% of the total weight. All the data are expressed in tonnes. Data on captures and aquaculture, in 2021, were obtained from FishStatJ software 4.01.0 [67,68].
CountryCapturesEstimated Range
of by-Products Weight		Estimated Range
of Viscera Weight		AquacultureEstimated Range
of by-Products Weight		Estimated Range
of Viscera Weight
Albania75894553–5312607–113880484829–5634644–1207
Austria350210–24528–5348752925–3413390–731
Belgium13,8058283–96641104–20,171223134–15618–33
Belarus605363–42448–9185045102–5953680–1276
Bosnia-Herzegovina305183–21424–4638192291–2673305–573
Bulgaria55,48433,291–38,8394439–832312,5657539–87961005–1885
Croatia59,96035,976–41,9824797–899425,97015,582–18,1792078–3896
Cyprus1357814–950109–20478454707–5492628–1177
Czechia33141988–2320265–49720,99112,595–14,6941679–3149
Denmark415,261249,157–290,68333,221–62,28932,10019,260–22,4702568–4815
Estonia63,18937,913–44,2325055–9478849509–59468–127
Faroe Islands532,282319,369–372,59742,583–79,842115,65069,390–80,9559252–17,348
Finland124,83574,901–87,3849987–18,72514,3998639–10,0791152–2160
France362,379217,427–253,66528,990–54,35747,91028,746–33,5373833–7187
Germany176,847106,108–123,79314,148–26,52718,29410,976–12,8061464–2744
Greece46,76428,058–32,7353741–7015130,17178,103–91,12010,414–19,526
Hungary46012761–3221368–69017,84710,708–12,4931428–2677
Iceland1,027,250616,350–719,07582,180–154,08853,13631,882–37,1954251–7970
Ireland184,761110,857–129,33314,781–27,71413,3818029–93671070–2007
Italy94,01656,410–65,8117521–14,10260,48436,290–42,3394839–9073
Latvia116,41369,848–81,4899313–17,462901541–63172–135
Liechtenstein000000
Lithuania91,25354,752–63,877730051353081–3595411–770
Luxembourg000000
Moldova00012,9007740–90301032–1935
Malta23531412–1647188–35316,4339860–11,5031315–2465
Montenegro753452–52760–113640384–44851–96
Netherlands261,571156,943–183,10020,926–39,23655403324–3878443–831
North Macedonia514308–36041–7731691901–2218254–475
Norway2,115,4961,269,298–1,480,847169,240–317,3241,662,675997,605–1,163,873133,014–249,401
Poland201,321120,793–140,92516,106–30,19844,78626,872–31,3503583–6718
Portugal156,07693,646–109,25312,486–23,41186715203–6070694–1301
Romania34762086–2433278–52111,7147028–8200937–1757
Serbia23541412–1648188–35373084385–5116585–1096
Slovakia18151089–1271145–27223041382–1613184–346
Slovenia241145–16919–361256754–879100–188
Spain743,530446,118–520,47159,482–111,53070,28542,171–49,2005623–10,543
Sweden155,92593,555–109,14812,474–23,38911,7967078–8257944–1769
Switzerland1486892–1040119–22323341400–1634187–350
Ukraine34,50720,704–24,1552761–517616,88210,129–11,8171351–2532
United Kingdom523,488314,093–366,44241,879–78,523219,198131,519–153,43917,536–32,880
TOTAL7,587,5274,552,516–5,311,269607,002–1,138,1292,700,9871,620,592–1,890,691216,079–405,148
Table 6. Quantification of carp, seabass, gilt-head bream, salmon, trout, and turbot from aquaculture in every country of Europe. The data were obtained from FishStatJ software [67] and the APROMAR website [69]. The estimated weight of the by-products was calculated assuming that it accounts for 60–70% of the total weight, and in the case of the viscera, it accounts for 8–15% of the total weight.
Table 6. Quantification of carp, seabass, gilt-head bream, salmon, trout, and turbot from aquaculture in every country of Europe. The data were obtained from FishStatJ software [67] and the APROMAR website [69]. The estimated weight of the by-products was calculated assuming that it accounts for 60–70% of the total weight, and in the case of the viscera, it accounts for 8–15% of the total weight.
Countries of Europe, 2021Carp (Tonnes)Seabass (Tonnes)Gilt-Head Bream (Tonnes)Salmon (Tonnes)Trout (Tonnes)Turbot (Tonnes)
Albania-24633724-1861-
Austria666--83205-
Belgium7557---127-
Belarus356.25482-3317-
Bosnia-Herzegovina------
Bulgaria5986--15468-
Croatia363090397519-350-
Cyprus-26805097-52-
Czechia18,709---1070-
Denmark-14-166828,476-
Estonia----712-
Faroe Islands---115,650--
Finland----13,551-
France147022901850-38,800-
Germany4610---8725-
Greece151,23266,891-1911-
Hungary12,707---74-
Iceland---46,4586341-
Ireland---12,844537-
Italy19973948176-41,97130
Latvia564---183-
Liechtenstein------
Lithuania3734---131-
Luxembourg------
Moldova-2212640---
Malta10,580-----
Montenegro-4336-561-
Netherlands----50100
North Macedonia299---2828-
Norway---1,562,41597,774-
Poland18,941---19,298-
Portugal-8343091-8573538
Romania7369---2747-
Serbia5649---1556-
Slovakia740---800-
Slovenia131---921-
Spain-23,0377823--7629
Sweden----11,703-
Switzerland---1621230-
Ukraine13,450---312-
United Kingdom168--205,00013,253-
Total fish weight117,51699,301106,9291,944,206310,75111,297
Estimated range of
by-products weight		70,510–82,26159,581–69,51164,157–74,8501,166,524–1,360,944186,451–217,5266778–7908
Estimated range of
viscera weight		9401–17,6277944–14,8958554–16,039155,536–291,63124,860–46,613904–1695
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MDPI and ACS Style

Domínguez, H.; Iñarra, B.; Labidi, J.; Bald, C. Fish Viscera Hydrolysates and Their Use as Biostimulants for Plants as an Approach towards a Circular Economy in Europe: A Review. Sustainability 2024, 16, 8779. https://doi.org/10.3390/su16208779

AMA Style

Domínguez H, Iñarra B, Labidi J, Bald C. Fish Viscera Hydrolysates and Their Use as Biostimulants for Plants as an Approach towards a Circular Economy in Europe: A Review. Sustainability. 2024; 16(20):8779. https://doi.org/10.3390/su16208779

Chicago/Turabian Style

Domínguez, Haizea, Bruno Iñarra, Jalel Labidi, and Carlos Bald. 2024. "Fish Viscera Hydrolysates and Their Use as Biostimulants for Plants as an Approach towards a Circular Economy in Europe: A Review" Sustainability 16, no. 20: 8779. https://doi.org/10.3390/su16208779

APA Style

Domínguez, H., Iñarra, B., Labidi, J., & Bald, C. (2024). Fish Viscera Hydrolysates and Their Use as Biostimulants for Plants as an Approach towards a Circular Economy in Europe: A Review. Sustainability, 16(20), 8779. https://doi.org/10.3390/su16208779

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