Fish waste silage, a green process for low feedstock availability. A Review¹

Ensilado de desechos de pescado, una actividad sustentable para bajos volúmenes de procesamiento

Claudia Carina Libonatti redlab@vet.unicen.edu.ar

National University of the Center of the Buenos Aires Province, Argentina

Daniela Alejandra Agüería dagueria@vet.unicen.edu.ar

National University of the Center of the Buenos Aires Province, Argentina

Javier Breccia javierbreccia@gmail.com

National University of La Pampa, Argentina

Esta obra está bajo una Licencia Creative Commons Atribución-NoComercial-SinDerivar 4.0 Internacional.

Fishing-related activities fulfill the dual function of representing a major source of food worldwide and constitute as a livelihood for a large number of people. World fish production was estimated to be about 179 million tons in 2018 (with China, Peru, Chile and Japan being the main marine fish catcher countries), where 83 % was used for human consumption and most of the rest ended up as fishmeal and fish oil (Organización de las Naciones Unidas para la Alimentación y la Agricultura [FAO], 2020). The different fishing activities result in a waste volume related to the processing of species (filleting cuts, viscera, heads, and bones), the discards of the companion fauna, species of low commercial value or the losses related to handling problems (FAO, 2014; Toledo Pérez & Llanes Iglesias 2006).

Fish waste represented half of the raw material volume of the industry and is a source of low–cost nutrients (Oetterer, 2002). The use of fishing waste in different parts of the world is allocated to animal feed and is of great interest as it represents an environmental and public benefit as well as reducing the cost of animal production. However, there were numerous reports about diverse products such as finfish or shellfish wastes for biodiesel, biogas as well as source of natural pigments and chitin (Cadavid-Rodríguez et al., 2019; Castro et al., 2018; Cira et al., 2002; dos Santos et al., 2015; Nges et al., 2012).

In countries such as Argentina, Norway, and China, waste generated from fishing activities is mainly used to produce fishmeal and oils (Ramírez, 2013). When fish were fed with animal protein, mainly fish meal, growth indicators and feed utilization were improved (Zhoug et al., 2004). Fish meal production is the most common process for recovery the nutrients from fish processing byproducts. However, the long distances to fish meal plants, the cost of transport, and law restrictions on fish meal production reduce the feedstock and raise the price of fish meal (Palkar et al., 2017). Since high costs and limited availability of fishmeal have forced companies to reduce or eliminate this component in their products, the situation promotes alternative processes where fish silage could be a promising choice (Hardy, 2010; Tacon & Metian, 2008).

Fish silage production is a technology with lower costs. Although fish silage preparation usually depends on the locally available raw materials and conditions, it recovers the nutrients contained in fishery residues and allows their use as animal feed (Ferraz de Arruda et al., 2007; Gomez et al., 2014; Inoue et al., 2013; Valério Geron et al., 2007). The use of fish processing waste could reduce the cost of producing fish feed by approximately 15 to 20 % (Li et al., 2009). Although the amount of fishmeal replacement depends on fish species specific on and its growth stage (Moon & Gatlin, 1994; Mondal et al., 2011), 75 % fish meal could be replaced without any compromise on the growth and nutritive value of the raw material (Cheng et al., 2003).

The silage provides a double benefit: it protects the environment against the risk of contamination generated by untreated waste and reduces the costs of animal feed production (Samaddar & Kaviraj, 2014). The aim of this review was to compile, organize and summarize literature related to biological fermentation of fish waste and its applications.

Fish silage is an ancient preservation technique (Raa et al., 1982) that was adopted in the 1930s from a method that using sulfuric and hydrochloric acids to preserve forages (Hammoumi et al., 1998). The process involve crushing fish, which accelerates the pH reduction to 4. This result in a semi-liquid product is rich in proteins, amino acids, phosphorus, and calcium. The product has a slight malted smell and can be used as protein source in animal feed (Raa et al., 1982), particularly for fish (Goddard & Al-Yahyai, 2001; Pinto de Carvalho et al., 2006; Vidotti et al., 2002) and chickens (Bello, 1997).

Some investigations demonstrated that fish silage has the potential to be used as a nitrogen source and probiotic ingredient for poultry feeding (Hammoumi et al., 1998). In their study, the chemical and physico-chemical properties of raw sardine waste and the resulting silage were compared. The silage was found to contain an average of 11.34 % protein, 6.12 % fat, and 7.94 % ash.

Additionally, the potential of sardine waste silages as fishmeal substitute for fishmeal in the production of Dicentrachus labrax was assessed. Fermentation with Lactobacillus plantarum, supplemented with molasses and organic acid acidification at 35 °C resulted in a product with 13.2 % protein, 12 % fat, and 2.1 % ash (Davies et al., 2020). Although there were variations in the composition of silages, these values were quite similar to those obtained from the previous study and could be attributed to differences in the raw materials used.

The main cause of liquefaction of fish silages is considered to be the lower pH value and the endogenous enzymatic activities. This process can be achieved by either chemical or biological means, with the purpose of reducing the pH to inhibit the spoilage flora and extend the preparation’s half-life (Dapkevicius et al., 2000; Raa et al., 1982). The rapid decrease in pH promotes favorable microbiological and enzymatic processes that help preserve the quality of fish silage (Ramírez Ramírez, 2009).

Chemical fish waste silage can be prepared by direct acidification with organic acid, inorganic acid, or mixture of both (Copes et al., 2006; Fagbenro & Jauncey, 1993; Gullu et al., 2015; Toledo Pérez & Llanes Iglesias, 2006). While the cost of organic acids is higher than mineral acids such as hydrochloric acid and sulfuric acid, handling inorganic acids requires trained operator and safety equipment. Organic acids like formic acid and propionic acid are less dangerous and have higher bactericidal and antifungal effects (Wicki et al., 2007).

The quality and freshness of raw materials are crucial for the production of silage since protein digestibility, fatty acids content, and vitamins levels depend on them (van ’t Land et al., 2017). This is particularly important for a product that may be used in aquaculture and animal production.

Fermentation using lactic acid bacteria is preferable to chemical silage because it has beneficial effects such as antibacterial activity and prevents lipid oxidation during ripening (Raa et al., 1982). Lactic acid bacteria produce various compounds that inhibit spoilage microflora, including organic acids, diacetyl, hydrogen peroxide, and bacteriocins (Yusuf & Hamid, 2013).

The freshness of the fish waste used for silage production is generally considered important, but the raw material may sometimes have microbiological variability due to conditions at the fishing plants. To homogenize the raw material and reduce the microbiological load, Góngora et al. (2012) cooked the fish waste before chopping it.

Although the silage technology is simply, it has some disadvantages such as high water content, making it difficult to transport. Co-dried fish silage used as an aquafeed ingredient that is easy to package, store, and transport. Some aquaculture experiences have used fish silage with co-dried ingredients such as soybean, cornbean, barley flour, and wheat bran (Fagbenro & Jauncey, 1994a; Najim et al., 2014). Fagbenro & Jauncey (1995) highlighted that fermented fish silage co-dried with protein feedstuffs can provide up to 50 % of dietary protein without affecting feed efficiency, fish growth, or health.

Lactic acid bacteria (LAB) are Gram positive, non-sporulated, coccus or bacillus bacteria that can ferment carbohydrates and produce lactic acid as the main fermentation product (Hayek & Ibrahim, 2013). LAB belongs to the Phylum Firmicutes, class Bacilli, order Lactobacillales, and are distributed across five different families, 62 genera, and over 500 species of low guanine-cytosine content (33-51 %) bacteria. The Lactobacillaceae family includes most of GRAS species (GRAS: Generally Recognized as Safe, US-FDA) within 31 genera to date. Currently, the delineation of taxonomic ranges is based on phylogenetic analysis, average nucleotide identities (AAI), physiological characteristics, and ecological niche (Zheng et al., 2020).

The most commonly used LAB as starter cultures in the production of biological silages are Lactobacillus spp., Carnobacterium spp., Leuconostoc mesenteroides, Pediococcus acidilactici (Bhaskar et al., 2007; Faid et al., 1994; Fagbenro & Jouncey, 1995; Vazquez et al., 2008; Vazquez et al., 2011). Some of the more well-known species for their high synergism and mutualism used in commercial yogurt production are Lactobacillus bulgaricus and Streptococcus thermophilus (Fernández Herrero et al., 2013; Fernández Herrero et al., 2015; Valério Geron et al., 2007). However, some processes have been performed by native LAB strains isolated from fish (Gelman et al., 2001; Holguín et al., 2009).

Researchers have evaluated the use of Weissella paramesenteroides, isolated from bee bread, as a potential tool for biological fish silage through encapsulation (Libonatti et al., 2018).

Certain LAB strains are considered probiotic due to their beneficial effects on the digestive tract and immune system of consumers. Evidence supports the use of LAB in animal production (Espeche et al., 2012; Topic Popovic et al., 2017; Zhang et al., 2012), including in aquaculture, where probiotics have been shown to activate non-specific immune responses and increase the number of erythrocytes, granulocytes, macrophages, and lymphocytes in various fish species (Irianto & Austin, 2003; Kim & Austin, 2006; Nayak et al., 2007).

In recent years, the applications of LAB have been extended beyond probiotics. Gaspar et al. (2013) particularly highlight the use of LAB as cell factories for the production of high-value complex pharmaceuticals and food ingredients, such as colors, aromas, and texturizing agents. For the specific purpose of fish fermentation, Lactobacillus plantarum and other species within the plantarum group have been found the better adapted bacteria (Bhaskar et al., 2007; Castro et al., 2018; Dapkevičius et al., 1998; Davies et al., 2020; Evers & Carroll, 1996; Faid et al., 1994; Fagbenro & Jouncey, 1994a; 1994b; Fagbenro & Jouncey, 1995; Góngora et al., 2012; Hammoumi et al., 1998; Vázquez et al., 2008; Vázquez et al., 2011).

Fish has a low concentration of carbohydrates, so it is necessary to add an aditional source of these substrates to increase the production of lactic acid during fermentation (Góngora et al., 2012; Ramírez Ramírez, 2009). Therefore, the selection of the carbohydrate and its appropriate level are determining factors in achieving efficient systems for fast acidification within the economic equation of the process (Cira et al., 2002; Davies et al., 2020; Góngora et al., 2012). The availability of the substrate in the region where the silage is produced is key condition for an economically sustainable process (Parín & Zugarramurdi, 1997).

Several sources of substrates have been tasted for fish fermentation, including molasses (Table 1), sucrose, high fructose corn syrup, whey, honey, glucose, and fruits (Table 2). Molasses is one of the most widely used substrates due to its high content of soluble carbohydrates, low cost, and the ability to improve the stability and sensory characteristics of the silages (Evers & Carroll, 1996; Fagbenro & Jauncey, 1998; Zahar et al., 2002). However, other reports have highlighted the potential of carbon sources from vegetable and fruit waste (Bello, 1997; Davies et al., 2020).

Table 1
Research that uses molasses as a carbohydrate source in the production of biological fish silage.

Tabla 1. Estudios que utilizan la melaza como fuente de hidratos de carbono en la elaboración de ensilado biológico de pescado.

Faid et al. (1994); Fagbenro and Jauncey (1994a); Fagbenro and Jauncey (1994b); Fagbenro and Jauncey (1995), Evers and Carroll (1996); Ahmed and Mahendrakar (1996); Hammoumi et al. (1998); Zahar et al. (2002); Valério Geron et al. (2007); Ramírez Ramírez et al. (2016); Castro et al. (2018); Shabani et al. (2019); Davies et al. (2020)

Table 2
Research that uses glucose, honey, sucrose and other carbohydrates in the production of biological fish silage.

Tabla 2. Estudios que utilizan glucosa, miel, sacarosa y otros hidratos de carbono en la elaboración de ensilados biológicos de pescado.

Bhaskar et al. (2007); Llanes Iglesias et al. (2010); Kumar Rai et al. (2010); Vázquez et al. (2011); Góngora et al. (2018); Góngora et al. (2012); Nges et al. (2012); Libonatti et al. (2018)

Around half of the articles reviewed related to fish silage, (23 articles) were conducted to the elaboration of biological silage as additive for animal feed, the rest were focused on other applications such as chitin, carotenoids, peptones extraction, oils recovery and methane production (Table 3).

Table 3
Applications of biological fermentation of fish waste

Tabla 3. Aplicaciones de la fermentación biológica de residuos de pescado.

Ahmed and Mahendrakar (1996); Bhaskar et al. (2007); Castro et al. (2018); Dapkevičius et al. (1998); Davies et al. (2020); Evers and Carroll (1996); Faid et al. (1994); Fagbenro and Jauncy (1994a); Fagbenro and Jauncey (1994b); Fagbenro and Jauncey (1995); Fagbenro and Jauncey (1998); Góngora et al. (2018); Gomez et al. (2014); Hammoumi et al. (1998); Inoue et al. (2013); Kumar Rai et al. (2010); Llanes Iglesias et al. (2010); Nges et al. (2012); Ramírez Ramírez et al. (2016); Shabani et al. (2019); Vázquez et al. (2008); Vidotti et al. (2002)

This comprehensive review provides valuable insights into the potential of utilizing a range of carbohydrate sources, biological starters, and fish waste for fermentation processes. The findings highlight the feasibility of using fish waste for various applications, including the recovery of chemicals from fish biomass. By promoting the use of this sustainable technology, this work can help to advance the transition towards a circular bioeconomy and contribute to the scientific community’s efforts to find eco-friendly solutions for waste valorization and resource recovery.

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