The aquaculture sector faces uncertainty due to environmental changes, economic factors, and availability of food resources. Conventional aquatic feeds heavily depend on fishmeal, which has driven the search for innovative and sustainable alternatives, such as insects. These insect-based protein sources have several benefits, such as efficient nutrient utilization, short maturation periods, and profitability, addressing the economic and environmental challenges associated with conventional aquafeed ingredients. Scientific studies indicate that insects have the potential to improve flesh quality, strengthen the immune system, and reduce disease susceptibility in farmed fish, promoting sustainable and productive aquaculture systems. The integration of insects as alternative protein sources in aquatic feeds can offer a promising path towards sustainable and environmentally friendly aquaculture systems.
1. Introduction
The rapid growth of the global human population (1.6 percent per year) has exerted tremendous pressure on the food sector (Gras et al., 2023). With the declining availability of wild fish and crustaceans, aquaculture becomes a crucial protein source for both humans and animals (Alfiko et al., 2022).
The quality and composition of feeds constitute critical factors in aquaculture, impacting animal growth significantly (Xiao et al., 2018). Furthermore, the overexploitation of oceans results in unsustainable pressure on wild fish stocks, resulting in their rapid decline (Daniel, 2018, Stankus, 2021). In the coming years, this won’t be a viable source from sustainability and economic perspectives (Gasco et al., 2018). The increase in price and scarcity of these raw materials intensify the need to reduce their incorporation percentage and seek more sustainable and cost-effective alternatives in feeds while ensuring the quality and nutritional value of fish (Daniel, 2018, Stankus, 2021).
Fishmeal (FM) in aquaculture has frequently been replaced with plant proteins, with soybean being favorite due to its cost effectiveness and nutritional value (Hameed et al., 2022). However, the addition of high quantities of soybean meal in the fish diet has been negatively linked to growth, gut and liver integrity, intestinal microbiota composition, and immunological response in various carnivorous fish species (Aragão et al., 2022, Macusi et al., 2023; Y. ru Wang et al., 2017). Consequently, the researchers were forced to develop aquafeeds with innovative feed ingredients that can replace FM while mitigating the negative impacts associated with vegetable protein (Alfiko et al., 2022). In this context, insects may be a feasible alternative to FM, offering nutritional constituents more similar to FM and, therefore, presenting a promising solution for sustainable aquaculture in the near future (Alfiko et al., 2022). A wide range of insect species have been studied and used in aquaculture to prepare feed ingredients (Barroso et al., 2014). Among those approved by European regulations, Hermetia illucens, Tenebrio molitor and Musca domestica stand out due to their high nutritional value. Whole insects contain 42–63.3 % crude protein on a dry matter basis (Alfiko et al., 2022), with up to 74 % reported for defatted insect meal (Alfiko et al., 2022). Beyond the high percentages of protein, nutritional value includes an additional well-balanced essential amino acid (EAA) profile, high lipid content (10–30 %), a good source of vitamins such as vitamin B12, and bioavailable minerals such as iron and zinc (Alegbeleye et al., 2012, Gasco et al., 2020).
Despite the potential and beneficial aspects of using insects in aquaculture, as this is an emerging sector, some limiting factors must be considered. Insect feeding substrates should be standardized, since their composition impacts the nutritional composition of the protein obtained (Sogari et al., 2023). Likewise, the percentage of conventional protein sources that could be replaced by insect ingredients need to be defined (Van Huis et al., 2021) for different fish species. The selling price of insect meals can be influenced by several factors, such as the production system, the substrate used and the country where the production unit is located (Niyonsaba et al., 2021), but also by health benefits associated with bioactive compounds such as antimicrobial peptides, medium chain fatty acids and chitin in their derived forms (Borrelli et al., 2021).
2. Global Aquaculture market
In 2020, global production of aquatic animals was approximately 178 million tons, with the total production predicted to reach 202 million tons by 2030 (FAO, 2022). Over 157 million tons (89 %) were allocated for human consumption, while the remaining 20 million tons were used for non-human food purposes, with about 16 million tons for FM and oil production. The production value of fishing and aquaculture in 2020 was estimated at 367 billion euros, of which 239 billion euros came from aquaculture (FAO, 2022). Global aquaculture is unevenly distributed, with Asia being the main producer, representing, in 2020, 91.6 % of global production (and 85 % of the value). China is responsible for 56.7 % of global aquatic animal production and 59.5 % of algae production (Mair et al., 2023). The Americas, Europe and Africa represent, respectively, 3.6 %, 2.7 % and 1.9 % of global production. It is often cited that aquaculture represents the fastest growing food production sector in recent decades, with an average annual growth rate of 6.7 % over the last three decades (Mair et al., 2023).
Aquaculture contributed to a total of 122.6 million tons in live weight. Around 87.5 million tons were aquatic animals, primarily intended for human consumption, 35.1 million tons were algae, and 700 tons were shells and pearls. Over the coming years, the average annual growth rate of aquaculture is expected to decrease from 4.2 % in 2010-2020 to 2.0% in 2020–2030 tons (FAO, 2022).
However, the sector’s evolution is difficult to predict. The upcoming decade is poised to undergo substantial transformations in environmental conditions, resource accessibility, macroeconomic landscapes, international trade regulations, tariffs, and market dynamics. These shifts have the potential to impact production, markets, and trade over the medium term. Climate variability and its changing patterns, encompassing the rise in extreme weather occurrences, are expected to exert noteworthy and varied geographical effects on the availability, processing, and trade of aquatic goods. This situation might render nations more susceptible to risks. Nevertheless, adept governance that advocates for stringent fisheries management practices, responsible expansion in aquaculture, and advancements in technology, innovations, and research can help alleviate these risks (Engle and van Senten, 2022).
3. Conventional aquafeeds and its challenges
Aquaculture stands as a pivotal force in global food production, experiencing substantial growth. However, this expansion comes with notable challenges, particularly in the realm of conventional feeding practices. A central concern is the widespread reliance on FM as a primary source of proteins and lipids in aquafeeds, primarily derived from wild fish catches (Abdel-Tawwab et al., 2020; Alfiko et al., 2022; Basto et al., 2021). The sheer magnitude of this reliance is underscored by the allocation of approximately 21 million tons of fish, with 76 % directed towards aquafeed production, exerting immense pressure on wild fish stocks for non-food purposes (Iaconisi et al., 2018).
FM´s popularity in aquafeeds is rooted in its well-balanced amino acid composition and high digestibility. These attributes are crucial for nutrient uptake, digestion and the absorption of essential nutrients, especially in extensively farmed carnivorous fish species such as trout, salmon, seabass and seabream (Abdel-Tawwab et al., 2020, Iaconisi et al., 2018). However, the escalating demand for FM poses substantial challenges to the sustainability and profitability of the aquaculture industry (Alfiko et al., 2022).
The unprecedented growth of aquaculture intensifies the demand for FM, leading to a rapid decline in wild fish stocks (Alfiko et al., 2022; Stankus, 2021). The associated costs of aquafeeds, where FM constitutes a major expense, hinder the industry’s sustainable development (Alfiko et al., 2022). In light of the imperative for green, profitable, and sustainable (GPS) production, a revaluation of protein sources with comparable nutritional components is essential (Daniel, 2018).
Plant-based materials, such as soybeans, oil seeds and cereal gluten, are increasingly being used as an alternative for animal feed. However, replacing animal-based proteins with plant-based alternatives is not feasible with the aquaculture industry. Plant-based feeds contain a wide variety of anti-nutritional factors, non-starch polysaccharides, less suitable fatty acid, unbalanced essential amino acid profiles (lysine and methionine), and low palatability. Furthermore, the vegetable alternatives used may involve competition with other sectors in the food industry for both humans and animals. The global scarcity and high prices of these commodities amplify the urgency to find eco-friendly alternatives (Stankus, 2021). Moreover, ethical concerns emerge as fish suitable for direct human consumption are allocated for FM production (Stadtlander et al., 2017). FM, as a finite resource, cannot guarantee a continuous supply of cheap protein for aquafeeds (Ng et al., 2001). Certain aquaculture practices, particularly those utilising wild pelagic fish, contribute to marine ecosystem disruption during FM production (Hashizume et al., 2019).
The future of aquaculture hinges on innovative and sustainable alternatives, such as insects, to address the ecological, economic and ethical dimensions of conventional feeding practices. For such there is a need to acknowledge the legislation regarding the use of insects as a source of protein for aquafeeds.
4. Legislation
European feed regulations have imposed strict restrictions on the use of animals as feed ingredients, due to the history of bovine spongiform encephalopathy (EC/999/2001; EC, 2001). Nevertheless, a significant change occurred in 2017 with the introduction of Regulation (EU) No 2017/893, which amended Regulations (EC) No 999/2001 and (EU) No 142/2011. This amendment marked a pivotal moment as it allowed the inclusion of seven insect species in the diet of aquaculture animals Hermetia illucens (HI), Musca domestica (MD), Tenebrio molitor (TM), Alphitobius diaperinus (ADi), cricket Acheta domesticus (AD), Gryllodes sigillatus (GS) and Gryllus assimilis (GA). In the future, the revision of this list can be based on a risk assessment of insect species, considering their potential impact on health and the environment.
Regulation (EU) No 2017/893 removed the condition for reared insects that ‘products of animal origin must be sourced from a registered slaughterhouse’. This adjustment was essential because insect rearing facilities, where the insects are generally ‘slaughtered’, faced challenges in meeting the specific requirements applicable to traditional slaughterhouses. Regulation (EU) No 2019/1981 introduced a designated list of third countries that gained authorization to export insect products in accordance with the aforementioned Regulation (EU) No 2017/893. Finally, in November 2021, through Regulation (EU) 2021/1925, the EU legislator officially approved the use of Bombyx mori (BM) in aquaculture. This decision marked an expansion of the list from seven to eight authorized species. Consumer acceptance is not an issue for incorporating insects in animal feed in Europe (Stamer, 2015). In a Belgian study, findings from cross-sectional data amongst farmers, stakeholders and citizens showed that attitude towards the concept of using insects in animal feed was generally positive, particularly for applications in poultry and fish nutrition as indicated by Verbeke et al. (2015).
To foster the growth of the industrial production of insects and their use as feed in developed and developing countries, significant legislative changes are imperative in the future. Currently, two problems arise concurrently with this expansion, the first concerns the lack of local regulations, while the second concerns the lack of a stable and consistent set of regulations across international borders. More specifically, numerous local companies are interested in exporting their insect products globally, but the regulatory demands and discrepancies between countries complicates the initiatives to market and sell insect products. Additionally, within the European legal framework, constrains persist regarding the substrate options on which insects can be reared, limited to raw materials also approved for other livestock species. Overcoming these barriers requires revising current regulations to accommodate the needs and potential of the insect farming sector.
5. Insect meal quality and safety
The evaluation of the safety and quality in insect-based feed in aquaculture involves a comprehensive and multidimensional process, including microbial, chemical, and allergenicity analyses, along with assessments of nutritional content and digestibility.
As conventional feed sources face limitations, there is growing interest in alternative protein sources, with insect-based feed emerging as a promising candidate. Insects can be reared on organic substrates, contributing to the circular economy and reducing the environmental impact of aquaculture operations (Maroušek et al., 2023). Moreover, insects are rich in protein, essential amino acids, and micronutrients, making them an attractive source of nutrition for aquaculture species. Some insects also contain beneficial unsaturated fatty acids such as oleic and linoleic acid (Gasco et al., 2019). However, insects lack certain n-3 polyunsaturated fatty acids (n-3 PUFAs), such as the eicosapentaenoic and docosahexaenoic acids (EPA and DHA), crucial for marine fish feeds. These fatty acids are associated with various health benefits for humans (Lands, 2014), including cardiovascular health (Harris, 2007, Lu et al., 2011), inflammation prevention (Calder, 2008, Fetterman and Zdanowicz, 2009, Figueras et al., 2011), anti-aging effects (Dyall et al., 2010), insulin resistance (Kalupahana et al., 2010), and slows the progression of certain cancers (Astorg et al., 2004, Leitzmann et al., 2004, Westheim et al., 2023).
Table 1. Main nutritional components (%) of three insect species, soybean meal and fishmeala.
Table 2. Amino acid composition (g/16 g nitrogen) of insect meals, soybean meal and fishmeal
While the insect species intended for feed generally do not pose an imminent risk to aquaculture animals, the major risk was identified as originating from the rearing substrate used in insect farming (Maroušek et al., 2023). Substrates contaminated with mycotoxins or heavy metals can adversely affect insect survivability and growth performance. Accumulation of mycotoxins in insects is not observed so far, but further research is needed, because literature data is very limited (Schrögel and Wätjen, 2019). Contrary, metal accumulation varies depending on metal type, insect species, and developmental stage. Literature indicates that H. illucens (HI) is capable of significantly accumulate cadmium, whereas the Tenebrio molitor (TM) tends to accumulate arsenic in its larval body (Malematja et al., 2023). Regarding the rearing substrate, consistent monitoring of contaminants is an essential aspect for feed security. Considering that certain insects can transform organic waste into valuable biomass, the ban of using waste streams in animal feed, according to EU regulation, may be reconsidered in the future, particularly concerning the special case of insect farming for feed. Additionally, the existing EU limits for contaminants, such as heavy metals in animal feed, may require adjustments based on species-specific accumulation behaviour. Beyond assessing mycotoxins and heavy metals, a comprehensive safety evaluation of microbial hazards, chemical hazards (considering contamination with pesticides and veterinary medicines), as well as the allergenic potential of edible insects and derived products, must be conducted for each insect species (Precup et al., 2022, Schrögel and Wätjen, 2019).
Several studies indicate that replacing FM with insect meal, either partially or completely, has no adverse effects in immune-related parameters, including blood biochemical composition, histopathology of relevant organs, gut health, gene expression and disease resistance in numerous aquaculture species (Fawole et al., 2020, Sankian et al., 2018, Su et al., 2017, Zarantoniello et al., 2020).
The application of plant-based protein, particularly soybean meal, in aquaculture has diminished due to its association with causing intestinal enteritis (Kumar et al., 2021). Notably, in rainbow trout, the inclusion of HI meal in soybean meal-based diets has effectively prevented soybean meal-induced intestinal enteritis (Kumar et al., 2021). According to Xiang et al., (2020), insect meal contains bioactive peptides, potentially contributing to the prevention of this disease. However, the precise mechanism through which insect meal prevents soybean meal-induced enteritis in fish remains unclear and further investigations is required to characterize the bioactive peptides present in insect meals.
6. Insect species used in aquafeeds and their nutritional compositions
6.1. Most commonly used insects in aquafeed
Among the insect species tested for industrial aquafeed production, eight stand out as the most promising: HI, MD, TM, Alphitobius diaperinus, Acheta domesticus, Gryllodes sigillatus, Gryllus assimilis and BM (Fig. 1) (Alfiko et al., 2022). However, in this article we will focus on the use of HI, TM and MD as a partial or total replacement of FM (Fig. 2).
Fig. 1. Eight important insect species for replacing fish meals in aquafeed.
Fig. 2. The most relevant insect species for fish meals: H. illucens, M. domestica and T. molitor.
6.1.1. Black soldier fly (Hermetia illucens)
H. illucens larvae (HIL) exhibit exceptional characteristics that make a valuable resource for sustainable animal feed and water valorisation. Their ability to feed on diverse organic matter, coupled with a short maturation period of approximately three weeks, positions them as an efficient and sustainable source (Sheppard et al., 2002, Tomberlin and Sheppard, 2002). The pre-pupa stage of HIL simplifies the harvesting process, eliminating labour-intensive steps and enhancing their suitability for large-scale farming (Sheppard et al., 2002, Mohan et al., 2022). These advantages make HIL a promising candidate for sustainable aquafeeds and waste management, aligning with the principles of green and efficient resource utilization (Čičková et al., 2015, Romano et al., 2022; Y. S. Wang and Shelomi, 2017). Feeding trials involving HIL meal supplementation in various fish species have shown positive impacts on growth performance and feed consumption. Research demonstrates the potential to enhance the cardioprotective characteristics of fish fillets through tailored insect fatty acid profiles, further emphasising the versability and adaptability of HIL in aquafeeds (Bruni et al., 2020).
The integration of HIL into the diets of carnivorous fish, including yellow catfish (Pelteobagrus fulvidraco), rainbow trout (Oncorhynchus mykiss), Atlantic salmon (Salmo salar L.), and European seabass (Dicentrarchus labrax), shows promising results as an alternative to FM. Partial substitution with HIL meal sustains growth performance and positively influences fillet composition and consumer acceptance (Abdel-Tawwab et al., 2020, Hu et al., 2017, Moutinho et al., 2021, Renna et al., 2017, Stadtlander et al., 2017). For Atlantic salmon, complete replacement of FM with HIL meal does not compromise fillet quality (Bruni et al., 2020). In contrast, studies on omnivorous fish, such as Jian carp (Cyprinus carpio), reveal that while inclusion of dried HIL meal up to 75 % has no adverse effects on voluntary intake or growth, caution is needed at higher substitution due to signs of dietary stress and intestinal damage (S. Li et al., 2017). Careful selection of substitution levels is crucial for both carnivorous and omnivorous fish to ensure optimal growth performance and minimize potential adverse effects. Ongoing research is needed to explore long-term effects, optimize diet formulations, and understand the specific adaptation of different fish species to HIL-based diets.
Regarding the topic of waste management, a recent research investigation delved into the potential of Black Soldier Fly larvae to convert aquaculture solid waste (ASW) into biomass (Rossi et al., 2023). While these are first steps, and further studies are obviously needed to clearly understand the microbial and chemical safety of insects produced on ASW, they open the way for a potential circular economy for aquaculture feeding based on insects.
6.1.2. Yellow mealworm (Tenebrio molitor)
Feeding trials within the field of aquaculture have substantiated compelling evidence supporting the acceptance of fresh and dried TM as an alternative protein source (Alfiko et al., 2022). Responding to the escalating demand for sustainable aquafeed solutions, TM meals have emerged as substitutes for traditional FM, prompting extensive studies to assess their efficacy and integration into aquaculture practices (Terova et al., 2021). Numerous investigations have explored the use of TM meals in aquafeeds. Despite a predominant focus on growth effects resulting from the substitution of FM with mealworm meals, a significant knowledge gap persists concerning the underlying mechanisms governing these effects. To address this gap, a critical imperative is to delve into the true modes of action, digestion, and absorption of TM meal within the digestive systems of diverse aquaculture species. Employing molecular genetics and genomic approaches becomes pivotal in unravelling the intricate processes at play (Roncarati et al., 2015; Terova et al., 2021). This understanding is crucial for optimizing the utilization of TM meals in aquafeeds, ensuring both the efficacy of the substitution and the well-being of the aquaculture species.
Future research endeavors should focus on exploring the untapped nutritional potential of Tenebrio molitor as a novel raw ingredient for aquafeeds (Roncarati et al., 2015). Determining the optimal level of TM meal inclusion that does not impair fish growth performances is essential for facilitating the integration of TM meals in aquaculture practices with maximal efficiency and minimal adverse effects. These comprehensive investigations are indispensable for advancing the sustainable and nutritionally balanced evolution of aquafeeds.
6.1.3. Housefly (Musca domestica)
The utilization of MD as a supplementary feed for fish has been predominantly investigated within tilapia and catfish species, along with various aquaculture species (Alfiko et al., 2022). Diverse feeding trials conducted across multiple aquaculture species have consistently demonstrated the positive impact of incorporating maggot meal (MD, MDM meal) into fish diets, resulting in enhanced growth and feed conversion ratio while mitigating physiological stress. Furthermore, the incorporation of MDM meal into fish diets has proven to be a cost-effective strategy, reducing overall feed costs. Considering factors such as nutritional value, availability, growth and feed efficiency, MDM meal emerges as a viable alternative protein source with the potential to replace FM in aquafeeds. This substitution is particularly advantageous in developing countries, where the importation of FM entails significant costs. Future research efforts should concentrate on determining the optimal inclusion levels of MDM meal as a substitute for FM, delving into the potential economic benefits associated with such replacement (Alfiko et al., 2022).
In a broader context, the cumulative findings from the studies suggest that MDM meal holds promise as a viable and sustainable alternative to FM across diverse fish diets, contributing to robust growth performance and efficient nutritional utilization. These results underscore the importance of meticulous consideration and optimization of the inclusion levels of MDM meal in dietary formulation.
6.2. Nutritional composition
The significance of an optimal nutritional composition for enhancing production parameters in aquaculture is widely recognized. Recently, an increasing number of feeding trials have been performed using insect meals to replace partial FM in aquaculture species. Overall, the majority of experiments have demonstrated promising outcomes when replacing a part of FM with insect meals, albeit with variations depending on the fish and insect species involved. However, it appears that replacing more than 30 % of FM with insect meals has resulted in a reduction in fish growth, as indicated by studies conducted by Hua (2021) and Liland et al. (2021).
Insect meal production is developing rapidly in China, Europe, North America, Australia and Southeast Asian countries (Henry et al., 2015; Nogales-Mérida et al., 2019). It is widely known that the nutritional composition of insects depends on rearing substrates, and their fatty acid profile reflects their diet. Enriching insect substrates with these fatty acids can positively modify the insect fatty acid profile (Liland et al., 2017). Nutritional analyses, including crude protein, amino acids, fat content, fatty acid profiles and minerals, have been conducted on eight insect species mentioned above (Sánchez-Muros et al., 2014). Details information on the nutritional components of each insect species can be found in several published reports (Allegretti et al., 2017, De Souza-Vilela et al., 2019). This summary focuses on three key insect species – HI, MD and TM – highlighting their major nutritional compositions.
These three insect species exhibit a substantial crude protein (CP) level ranging from 42.1 % to 60.7 % as indicating in Table 1 . Although, this level of CP is lower than that found in FM, but is similar to soybean meal (Allegretti et al., 2018; Henry et al., 2015). Amino acid profiles vary among the insect species, with TM CPs containing less lysine compared to FM, while Diptera (HI and MD) CPs are notably rich in lysine. Sulphur amino acid contents in insects are lower than in FM. Threonine levels are similar among three insect species as shown in Table 2 (Henry et al., 2015; Sánchez-Muros et al., 2014). Tryptophan levels in the other two insect species, except for MD maggot (MDM) meal, are generally lower, suggesting potential supplementation with synthetic amino acids for optimal growth, depending on the specific requirements of the fish species. Diptera present superior amino acid profiles compared to soymeal (Table 2), making them preferable alternatives for replacing FM in aquafeeds (Henry et al., 2015; Sánchez-Muros et al., 2014). All three insect species have higher fat content than FM, ranging from 18.9 % to 36.1 % (van Huis, 2020). Insects tend to accumulate fat, particularly in their embryonic stages.
The fat content varies across different species, and even within a species, there is a considerable variation influenced by factors such as developmental stage and diet (Barros-Cordeiro et al., 2014, Barroso et al., 2019). In comparison to fish oil, insect meals have lower amounts of omega-3 fatty acids, with a notable presence of saturated fatty acids (Makkar et al., 2014). TM and MDM meals exhibit higher concentrations of unsaturated fatty acids, while in Hermitia illucens larvae (HIL) have a lower unsaturated fatty acid content (Gasco et al., 2020, Hawkey et al., 2021, van Huis, 2020). The lipid contents and fatty acid profiles in insect meals are well-recognized to be heavily influenced by their diet, and altering the substrate composition can bring about changes in these aspects (Makkar et al., 2014). It is crucial to note that the fatty acid composition is affected by several factors, including insect feeds, culturing conditions and the stage of insect harvest.
The ash content of the three insect species is minimal, except HIL, which exceeds 15 %. HIL contains relatively higher calcium, constituting 7.6 % of dry matter, whereas other insect species exhibit very low calcium levels (Table 1). Therefore, when substituting FM with insect meals, it is essential to include calcium in aquafeeds. Enhancing the calcium content in insect larvae meals can be achieved through the fortifying the rearing substrate with calcium (Allegretti et al., 2017, De Souza-Vilela et al., 2019; Henry et al., 2015; Sánchez-Muros et al., 2014). Additionally, it is noteworthy that MDM meal exhibits notably high phosphorus levels at 1.6 %. Across the three??? mentioned insect species, carbohydrates levels are generally low (less than 20 %) (Barroso et al., 2014).
The substitution of FM with insect meals faces certain limitations. Depending on the insect species used, it becomes necessary to supplement various nutritional components in aquafeeds. This supplementation is essential to ensure the optimal nutritional characteristics of fish fillets suitable for human consumption.
Insects, the most diverse group of animals, have garnered attention as natural and nutritious feed sources for fish, particularly carnivorous and omnivorous species with high protein dietary requirements (Alfiko et al., 2022; Nogales-Mérida et al., 2019; Tran et al., 2015; van Huis, 2019). In the pursuit of sustainable aquafeed solutions, 11 insect species have been evaluated as alternative protein sources, with notable success in recent studies (Henry et al., 2015; Nogales-Mérida et al., 2019).
The replacement of substantial portion of FM with insect-based protein sources has the potential to significantly reduce the FM content in organic aquafeeds. This not only addresses the economic feasibility of aquaculture but also contributes to the overall sustainability of aquafeed production (Stadtlander et al., 2017). Moreover, insects represent a promising alternative within the context of a circular bioeconomy, aligning with the principles of sustainability and resource efficiency (Bruni et al., 2020).
6.3. Chitin challenge in digestibility
Various studies have underscored the significant nutritional value of insects, emphasizing their considerable potential. The protein fraction, accounting for 40–60 % of dry weight, and the balanced amino acid composition reinforce the relevance of these insects, suggesting that their flours can entirely or partially replace FM in aquaculture feeds (Gasco et al., 2020, Makkar et al., 2014). However, a challenge and point of discussion in the scientific community lie in the significant presence of chitin and the associated antinutritional effects.
Chitin, the second most abundant polysaccharide on Earth after cellulose, is composed of N-acetyl-2-amino-2-deoxyglucose (GlcNAc) units linked by β-(1 → 4) bonds (Abdel-Ghany and Salem, 2020, Jiménez-Gómez and Cecilia, 2020). Classified as non-digestible fiber due to the absence of chitinolytic enzymes in most organisms, this biopolymer is the main constituent of insect exoskeletons. The perception that chitin, as non-digestible fibre, negatively impacts the digestibility of lipids and proteins has led to a trend of removing chitin from foods and feeds (Kroeckel et al., 2012). However, recent studies have challenged this perspective, highlighting the potential application of insect flours with chitin and its derivatives as effective prebiotics, antibacterial compounds, and immunomodulators in fish feeds (Ahmed et al., 2021, Dawood et al., 2020, Gaudioso et al., 2021, Rimoldi et al., 2021; Terova et al., 2021).
Other studies have demonstrated that the supplementation of chitin and chitosan in the diet indeed increases growth rates, feed efficiency, and enhances disease resistance in various fish species, including rainbow trout (Oncorhynchus mykiss), Nile tilapia (Oreochromis niloticus), thinlip mullet (Liza ramada), red porgy (Pagrus major), Japanese eel (Anguilla japonica), and yellowtail (Seriola quinqueradiata) (Ahmed et al., 2021, Dawood et al., 2020, Kono et al., 1987, Qin et al., 2014; S. Elserafy et al., 2021; Shi et al., 2020). Similarly, others have shown that certain species such as cod (Gadus morhua) (Danulat, 1986), juvenile cobia (Rachycentron canadum) (Fines and Holt, 2010, channel rockcod (Sebastolobus alascanus), splitnose rockfish (Sebastes diploproa), and black cod (Anoplopoma fimbria) (Gutowska et al., 2004) have been reported to exhibit chitinase activities, that is, enzymes capable of digesting chitin.
However, based on various studies, chitin should not be seen only as a villain. This biopolymer and its derivatives have positive effects on the diversity of the intestinal microbiome, acting as prebiotics and modulating the microbial communities in the fish intestines (Ringø et al., 2006, Terova et al., 2019). Additionally, they contribute to strengthening the immune system, providing protection against infections (Esteban et al., 2001).
7. Physiological responses of fish feeding with insects
In recent years, several articles and reviews have been published regarding the nutritional value, low environmental impact, and food safety of insects approved by the EU for animal feed (EC Regulation no. 2017/893; European Commission, 2017) (Alfiko et al., 2022). These studies highlight the potential of insects such as HI, TM, and MD as promising alternatives to FM in diets for various freshwater and marine fish species, particularly focusing on Mediterranean aquaculture (Gasco et al., 2016; Henry et al., 2018; Iaconisi et al., 2017; Nogales-Mérida et al., 2019; Piccolo, 2017; Pippinato et al., 2020).
The importance of zootechnical parameters and fish health is highlighted when considering insects as a food source. Studies performed by Chemello et al. (2020), evaluated the complete or partial replacement of FM with TM meal, and the results indicated that both substitutions did not affect rainbow trout growth performance and fillet quality (Belforti et al., 2015, Iaconisi et al., 2018, Rema et al., 2019). Similarly, TM has been successfully used and well-accepted by several marine fish species (Gasco et al., 2016, Iaconisi et al., 2017, Piccolo, 2017).
Research performed on blackspot sea bream (Pagellus bogaraveo) revealed that the inclusion of full-fat T. molitor at 21 % of the feed did not affect fillet EPA or DHA content. However, when included at 40 %, it decreased the EPA content (Iaconisi et al., 2017). This suggests that dietary insect meal may induce alterations in lipid metabolism, depending on its dietary inclusion level. In a study performed by Mastoraki et al. (2020), replacing fish meal with HIL did not have an impact on the n-3 PUFAs in European seabass when compared with the control diet. In another study, Pulido et al. (2022) observed that in fillets of gilt-head sea bream fed on HIL meals, there was a decrease in n-3 PUFAs in favour of SFAs. The discrepancy in these findings may be related to the nature of HIL meals used, as well as differences in fish species, basal diets, and environmental factors (Mastoraki et al., 2020).
Although several studies have reported the replacement of FM in fish diets using MD larvae, most of them focus on freshwater species such as Nile tilapia (Oreochromis niloticus). However, research has demonstrated that MD larvae can be a viable alternative source for farmed fish, with the potential to economically replace FM, as long as the hydrophobic fraction is removed. The quality of MD larvae, in terms of amino acid profile, is comparable to that of FM, except for taurine, suggesting the need for supplementation for use in aquaculture feed.
Additional studies evaluate the inclusion of insect meal in fish diets, highlighting that growth performance appears to depend on the level of inclusion, fish species, insect species, and nutrient composition (Piccolo, 2017).
In conclusion, the use of insects in aquaculture demonstrates the potential to promote sustainability and productivity, with specific considerations on zootechnical parameters, fish health, and adequate levels of inclusion in the diet.
8. Final considerations
Insects have emerged as one of the most promising substitutes for fishmeal when compared to other new protein sources, such as bacteria, microalgae, macroalgae, and yeasts. Soon, insects may emerge as a viable solution to address the drawbacks associated with FM in the aquaculture industry. The exploration of these alternative protein sources for aquafeeds, particularly through integration of insects, represents a significant stride towards sustainable and eco-friendly aquaculture. HI, TM and MD have emerged as promising candidates for replacing FM in aquafeeds. Insect-based protein sources exhibit diverse benefits, including efficient nutrient utilization, short maturation periods, and cost effectiveness, addressing the economic and environmental challenges associated with conventional aquafeeds products. Over the past decade, numerous studies have investigated replacing FM with insects in aquaculture. All fish trials must follow specific guidelines that address the nutritional needs of each fish species, adapting each formulation accordingly. Furthermore, it is necessary to evaluate not only the quality of flesh and growth performance but also the microbiome, water impact, and metabolic and physiological responses. This underscores the emerging need for multidisciplinary studies in this field.
Despite the promising results from including insects as ingredients in aquafeed, significant gaps remain regarding their full utilization in aquaculture. Moreover, important bioactive compounds such as chitin, fatty acids, and antimicrobial peptides have been reported in insects; however, their role in aquatic animal growth and physiology is not yet well understood.
Still, the success of this alternative hinges on critical factors, including the specific fish species and incorporation levels. Further exploration is expected to yield recommended guidelines for the incorporation of insect-based products tailored to diverse fish species.
Source : Fantatto, Rafaela R., Mota, J., Ligeiro, C., Vieira, I., Guilgur, L.G., Santos, M., Murta, D., 2024. Exploring sustainable alternatives in aquaculture feeding: The role of insects.
Aquac. Rep. 37, 102228. https://doi.org/10.1016/j.aqrep.2024.102228.
