THE POTENTIAL OF LUPIN AS A SUSTAINABLE INGREDIENT IN AQUACULTURE FEED

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The aquaculture sector is facing the challenge of developing sustainable and cost-efective alternatives to traditional fish  feed components. Lupin, a versatile utilitarian legume, has garnered increasing interest due to its nutritional value, desirable efects on the environment, and economic feasibility. Lupin for its high protein content, balanced amino acid profile, ease of processing, its implications in livestock development and health, and potential means of reducing the industry ecological footprint has made it a potentially advantageous aquafeed ingredient.

Introduction                                           

In a world where the demand for seafood continues to rise as seafood protein is a high-quality protein and thus, aquaculture has emerged as a vital player in meeting this ever-growing need. However, the sustainability of this industry is under constant scrutiny, primarily due to its heavy reliance on traditional fsh meals and fsh oil as aquafeed ingredients. In addition, in the past decade, there have been looming supply and market pricing challenges related to fsh meal. Hence, as global fish stocks are dwindling and the ecological footprint of the aquaculture industry is expanding, alternative environmentally friendly sources of fish feed are urgently needed. One such source that has garnered increasing attention is lupin (Lupinus spp), a leguminous plant known for its protein content and potential as a sustainable feed ingredient. Given their comparatively favorable composition and widespread availability, plants of the genus Lupinus appear to be an intriguing substitute for soybeans. Because of its outstanding nutritional content (crude protein–33 to 43 g, crude lipid–6 to 11 g, and ash content–2.9 to 4.6) and palatability, it serves as a potential replacement for fsh meal (FM), which was formerly the most widely used protein source for aquaculture.

The 2022 FAO report indicates that the capture rates of fish and seafood have stagnated, and the majority of crucial fshing grounds have already realized their full production potential. Consequently, other alternatives for fsh meal substitution, such as the biofoc technique, feather and bone meal from poultry, and distillery products, such as DDGS (distiller grain soluble) alternatives, do provide alternatives. Still, there are always increasing concerns about their judicious use as a replacement or ingredient in feed. Diferent plant source alternatives, such as wheat, corn, rapeseed, barley, and micro- or macroalgae meal, provide an array of plant-based ingredients for aquaculture. In addition, beetle meals (black soldier fy, Hermetia ilucens), ofer promising and novel alternatives as replacement ingredients. Tenebrio molitor (beetle meal), an insect meal, as a potential substitute for fish meal (FM) was emphasized by  Morken et al., (2011) but meta-analysis studies revealed that inclusion levels range between 20 and 30% provided maximum growth and decreased growth was observed at inclusion levels greater than 50%. These fndings was further supported by a meta-analysis. This was primarily due to the chitin which has a crystalline nature reduces the ingredient utilization in the aquafeed industry. In addition, deficit quantities of essential fatty acids (n-3 fatty acids) in full-fat insect meals also hampered the growth of European seabass (D. labrax) was reported.

The use of purifed ingredients such as casein and gelatin (in combination) is also a promising candidate replacement ingredient, although it needs to be supplemented with indispensable amino acids. SBM, popularly known as a soybean meal, is used extensively as an FM replacement. It is favored over its peer ingredients because of its high protein content and nutritionally balanced amino acid profle. However, serious environmental issues have been raised due to its non-eco-friendly methods of cultivation, such as deforestation, and the growth of a single crop without crop rotation leads to a decrease in soil fertility and quality. Additionally, SB is largely utilized for human consumption as opposed to animal husbandry. A World Bank report by Dunia (2020) demonstrated that there was an increase in the cost of soybeans ue to their utility in both human and livestock production. Although plant-based ingredients are attractive in terms of their protein content and favorable amino acid constitution, the presence of natural toxicants, viz., antinutritional factors such as protease inhibitors (trypsin, chymotrypsin), fiber, phytate or phytic acid, phytosterols, hemagglutinins, saponin, oligosaccharides, phytoestrogens, tannins, and gossypol, hinders nutrient utilization and hence their application as feed ingredients in aquaculture.

A delve into the realm of lupin

Lupin (Lupinus spp.) a member of the Fabaceae family, is a species-rich (more than 300 species) family of legumes that thrives in a myriad of climatic setups, such as those spanning from subarctic to semidesert to subtropical regions, showcasing a varied climatic range and adaptations. Lupins were commonly called lupini and were recognized as a bluebonnet plant that closely resembles soy in terms of its protein composition. Only four of the genera in this genus—white lupin (L. albus, WHL), narrow-leaf lupin (L. angustifolius, NLL), yellow lupin (L. luteus, YEL), and pearl lupin (L. mutabilis)—are grown as ornamental plants. Wide application of lupin were infested primary into food industry attributed to their properties. Food formulation requires ingredients with high emulsion and foam-forming capabilities, and lupin protein isolates provide these qualities. Lupin four has been diferentiated into its fiber for further processing and utilization. Enthusiasm for lupin production is on the rise, driven by its diverse applications in enhancing a wide array of goods, ranging from baker’s confectionaries such as pastries, breads, and chips to dairy replacements. Lupin, recognized for its exceptional protein content, serves not only as a therapeutic substance but also as a valuable green agricultural waste (manure). Additionally, owing to its high alkaloid levels, it acts as a natural producer of insecticides. This expanding interest in lupin production has been substantiated by various studies that further contributed to the versatility of lupin, with enriched lupin being incorporated into various items of high dietary value. Notable examples include lupin-enriched pasta, tofu, mufns, tempe, biscuits, and noodles. The term “lupin” extends beyond its applications to denote a classic Mediterranean culinary component utilized in the production of lupin four and fakes, often referred to as lupini beans. Integral to a healthy ecosystem, lupin is a multifaceted resource that signifcantly contributes to both agriculture and nutrition. Thus, lupin is a widely used legume for application.

  1 An overview of the nutritional profle of Lupin

Lupins are categorized as non-starchy grain legumes and are an excellent source of food ingredients because they contain high levels of indispensable amino acids, vital dietary minerals, protein (approximately 40%), and dietary fber (approximately 28%). Furthermore, it additionally features lower levels of fat (approximately 6%). Lupin seeds can serve as a viable source of alimentary polysaccharides, specifcally cellulose, contributing to the formulation of dietary meals with high nutritional standards. When animal proteins are not utilized, the high-protein fraction (25–40%) can be a primary food ingredient. Therefore, lupin, which has a high protein content, can act as a primary food ingredient. Lupin, however, has advantages over soybean as a feed ingredient since it has greater dietary fber levels (pertaining to 28%) than soya bean (about to 19%).

    2 Lupin inpar with its contemporary aquafeed ingredients

The aquafeed industry relied heavily on fsh meal as the major ingredient as they are highly nutritive, and widely accepted by fsh hence it was known as a highly palatable aquafeed ingredient. It was easily procurable for the industry until a decline in marine production due to overfshing which subsequently led to excessive exploitation of the resource. Thus, the search for cheap, alternative, and locally available ingredients evolved. This led to the application of a spectrum of feed ingredients as fish meal substituents. In this search, a novel plant-based substitute for fish meal was lupin. Table 1 depicts the proximate composition of diferent lupin seeds, processed lupin, conventional feed ingredients such as fish meal, soybean meal and novel protein ingredients from insects like black solider fy meal and Tenebrio molitor. When comparing the proximate composition of the various aquafeed ingredients and lupin, fish meal is placed first followed by the black solider and mealworm, following these is lupin, which stands as the third in the list, although the conventional feed ingredient may possess high crude protein, their application in the feed may is a matter of production feasibility. In terms of the crude lipid content, the mealworm is ranked frst followed by black soldier fy larvae and lupin. Since ingredients with high crude lipid may pose a challenge during processing and storage of the ingredient, hence lupin which stands as the third best ingredient in terms of crude lipid may be a suitable candidate lipid source of the ingredient. In terms of ash and mineral content, the processed lupin stands frst followed by other conventional feed. Thus, it can be proposed the use of lupin is highly economical, has longer storage, and easily available and cultivable ingredient compared to other conventional feed ingredients. The proximate composition of lupin and other  conventional feed ingredients are showed in Table 1.

The fatty acid and amino acid profle of lupin versus conventional feed ingredients is depicted in Table 2, lupin ranks high in terms of myristic acid, and linoleic acid. When compared to linolenic acid, mealworm followed by lupin stands second on the list. Lupin, hence is rich in essential fatty acids viz the linolenic and linoleic, a special attention to linoleic acid content. The amino acid profle of conventional ingredients versus lupin is depicted in Table 2. Inferring from the Table 2, alanine amino acid content is high in lupin followed by conventional feed ingredients. When comparing the arginine content in lupin and conventional feed ingredients, lupin has the highest arginine content. In addition, phenylalanine and tyrosine content in lupin was observed to be high when compared to other conventional feed ingredients. Aspartic acid and serine content was observed to be high in lupin when compared to others. With this, it can be inferred that the amino acid profle of lupin is remarkable and can easily be substituted for conventional feed ingredients.

Impact of lupin on the fish health and growth

   1 Growth performance and feed utilization

Lupin’s introduction to the aquafeeds paved the way for potentially feasible and an available ingredient. The impact of lupin on the growth and health of fish was studied intensively. A comprehensively reviewed study by Szczepanski and colleagues detailed the lupin’s potential as an alternate fish feed ingredient. The study tabulated the lupin as a feed aquafeed ingredient for various fishes. In fishes like salmon and trout, it was found that lupin protein digestibility (85.2%)

was higher when compared to that of the full-fat soybean meal (79.5%). However, as a plant source of ingredients, they lack the methionine and lysine essential amino acids, thus reduced growth was observed in higher inclusion (40%). In addition, the presence of non-starch polysaccharides, oligosaccharides, and anti-nutritional factors, contribute to the decrease in growth in salmonids. Hence, an inclusion of 25% lupin replacement with fish meal was found to improve the growth and feed acceptability of rainbow trout. Similarly, in Atlantic salmons, a partial replacement of lupin by 20 to 40% inclusion was deduced. In fishes like carps (Cyprinids), for common carp, it was found to be 12.5% partial replacement of soybean meal with lupin seed meal was found to provide better weight gain and feed efficiency ratio. Similarly in black carp, a partial replacement of soybean meal with lupin seed meal by 30% improved weight gain and feed efficiency ratio. In blackhead seabream (Acanthopagrus schlegelii), a partial replacement of soybean meal with lupin seed meal with 30% favored growth. In seabass, a dietary lupin seed meal inclusion at 40–50% with proper seed processing techniques improves the growth. In tilapia, dietary lupin seed can be up to 50% can be incorporated to produce high growth. Turbot (Psetta maxima), an inclusion of 50% dietary lupin was found to improve growth. In cobia (Rachycentron canadum), a dietary lupin inclusion of 10.5% provided growth as that of a fish meal. In shellfishes like Penaeus monodon (black tiger shrimp), lupin seed meal can replace up to 40–50% of soybean meal. For the Litopenaeus vannamei (white leg shrimp), 100 g per kg (10%) inclusion provided better growth when compared to 20 or 30% inclusion.

   2 Immune response

Maintaining the health of the fish in a culture environment is considered to be one of the central goals besides growth in aquaculture. Fish health could be compromised due to the presence of stressors in the culture environment. To

alleviate these, antioxidants, anti-inflammatory, ant-bacterial, etc. are provided. Antioxidants play an important role in maintaining the levels of reactive species such as the reactive oxygen and reactive nitrogen species. Antibacterial compounds help fishes against invading pathogens. An investigation on the antioxidant properties of lupin seeds was conducted. Tests for estimating antioxidant properties, such as Oxidograph and Rancimat, revealed the presence of alpha, beta and gamma varieties of tocopherol compounds in the lupin seeds, and long-term storage and high irradiation treatments decreased the tocopherol content of the lupin seeds. Radiation treatment was performed to estimate the chemical composition of the constituents, such as tannins, fatty acids (FAs), proteins and fats. The antioxidants found in lupin function as potent ACE inhibitors and impede lipid oxidation and atherosclerosis, according to studies by. The antioxidant effects of three lupin species, Lupinus albus (white), Lupinus angustifolius (narrow leaf ), and Lupinus luteus (yellow), were described in detail by Siger et al., (2012). Polyphenolic compounds primarily occur in the peripheral parts or the external regions of the seed. Table 7 shows the composition of the antioxidant compounds and their biological activities. The antibacterial properties of lupin have been investigated by  (Lampart et al., (2003). The test of the seeds revealed the antibacterial effects of Lupin seeds due to the presence of polyphenols, which are independent of nature (free polyphenols) and alkaloids. Hence, the relatively high total phenolic content corresponds to the antibacterial activity of the lupin.

Challenges and prospects of lupin

Though lupin promises to be a potential alternative to conventional feed ingredients, the presence of antinutritional actors may impact negatively fish growth and nutrient digestibility. Hence, suitable processing methods need to be

employed to decrease the anti-nutritional factors. Occupational exposure to lupin allergens can result from the manufacturing, transportation, processing, or handling of lupin products, including finished goods. Compared with consumers, employees in industries utilizing lupins may encounter a broader spectrum and increased levels of exposure. In agricultural and food research, potential contact through ingestion and skin exposure may occur during tasks such as grinding, processing, and baking of lupin products. Such interactions are also feasible in diverse occupational settings, as emphasized by Abeshu and Kefale (2017). Individuals susceptible to exposure may develop occupational sensitization and allergies that manifest as conditions such as asthma, as indicated by research findings. Additionally, severe reactions, including anaphylaxis, have been documented in the literature. To systematically monitor and analyze issues related to occupational lung conditions linked to lupin exposure, various databases, such as Surveillance of Work‐related and Occupational Respiratory Disease (SWORDS), Surveillance of Shiyang, Surveillance of Australian Workplace-Based Respiratory Events (SABRE), the Swedish Register of Reported Occupational Disease (SRROD), and Asmapro, actively collect data from these registries.

Lupin has the potential to become a high-value protein source in various sectors, including food, pharmaceuticals, and feed production. Incorporating lupin as a feed ingredient offers a strategic avenue to broaden the spectrum of available protein sources, reducing the reliance on conventional aquafeed ingredients with reduced entanglements of environmental issues. Limitations in the application of lupin may be due to its anti-nutritional factors, processing, and bioavailability. Nonetheless, overcoming the above challenges can be done with proper processing of lupin, and practicing safety measures help in alleviate the problem. Hence, the future implications of unlocking the potential of lupin as a sustainable aquafeed ingredient are promising.

Conclusion

Lupin, an environmentally friendly feed ingredient for fish plays a significant role in addressing critical challenges in aquaculture. Lupin offers a wealth of nutritional benefits, including high protein content and favorable amino acid

profiles, making it an attractive candidate for enhancing the growth and health of farmed fish. Moreover, its ecological advantages, such as nitrogen fixation and reduced greenhouse gas emissions, demonstrate its potential to support the sustainability of aquaculture systems. This review emphasizes the need for continued research and development to unlock Lupin’s full potential in aquaculture and strive for a more sustainable and healthier future. Overall, lupin has proven to be a promising solution in the pursuit of a more sustainable and nourished world.

Reference Open access : Malarvizhi, K., Kalaiselvan, P. & Ranjan, A. Unlocking the potential of lupin as a sustainable aquafeed ingredient: a comprehensive review. Discov Agric 2, 43 (2024). https://doi.org/10.1007/s44279-024-00054-x

Photo source : https://en.wikipedia.org/wiki/Lupin_bean

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