Abstract
The aquaculture sector is facing the challenge of developing sustainable and cost-effective alternatives to traditional fish feed components. Lupin, a versatile utilitarian legume, has garnered increasing interest due to its nutritional value, desirable effects 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. This review explores the promising nature of lupin in aquaculture, focusing on its nutritional value, digestibility, and impact on fish health and growth. The review also discusses at recent discoveries, challenges, and potential breakthroughs to provide insight into how lupin might advance the development of sustainable aquaculture techniques.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
1 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 [1]. However, the sustainability of this industry is under constant scrutiny, primarily due to its heavy reliance on traditional fish meals and fish oil as aquafeed ingredients [2, 3]. In addition, in the past decade, there have been looming supply and market pricing challenges related to fish meal [4]. 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 fish meal (FM), which was formerly the most widely used protein source for aquaculture [5].
The 2022 FAO report indicates that the capture rates of fish and seafood have stagnated, and the majority of crucial fishing grounds have already realized their full production potential [6]. Consequently, other alternatives for fish meal substitution, such as the biofloc technique [7], 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 [8]. Different plant source alternatives, such as wheat [9,10,11], corn [12], rapeseed [13, 14], barley [15, 16], and micro- or macroalgae meal [17,18,19], provide an array of plant-based ingredients for aquaculture. In addition, beetle meals (black soldier fly, Hermetia ilucens), offer 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 [15] 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% [19,20,21]. These findings was further supported by a meta-analysis [20]. This was primarily due to the chitin which has a crystalline nature reduces the ingredient utilization in the aquafeed industry [21]. 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 by [22].
The use of purified 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 [23,24,25,26,27]. 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 profile [28]. 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 [29]. A World Bank report by [30] demonstrated that there was an increase in the cost of soybeans due 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 [31], viz., antinutritional factors such as protease inhibitors (trypsin, chymotrypsin), fiber, phytate or phytic acid, phytosterols, hemagglutinins, saponin, oligosaccharides, phytoestrogens, tannins, and gossypol [32,33,34], hinders nutrient utilization and hence their application as feed ingredients in aquaculture.
2 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 [28]. Lupins were commonly called lupini and were recognized as a bluebonnet [35] 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 [36]. 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 flour has been differentiated into its fiber for further processing and utilization [37]. 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 [38,39,40,41,42] 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 [43], tofu [44], muffins [45], tempe [46], biscuits [47], and noodles [48]. The term “lupin” extends beyond its applications to denote a classic Mediterranean culinary component utilized in the production of lupin flour and flakes, often referred to as lupini beans. Integral to a healthy ecosystem, lupin is a multifaceted resource that significantly contributes to both agriculture and nutrition. Thus, lupin is a widely used legume for application.
2.1 An overview of the nutritional profile 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 fiber (approximately 28%). Furthermore, it additionally features lower levels of fat (approximately 6%) [49]. Lupin seeds can serve as a viable source of alimentary polysaccharides, specifically cellulose, contributing to the formulation of dietary meals with high nutritional standards. When animal proteins are not utilized, the high-protein fraction (25–40% [50]) 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 fiber levels (pertaining to 28%) than soya bean (about to 19%) [51].
2.2 Lupin in-par with its contemporary aquafeed ingredients
The aquafeed industry relied heavily on fish meal as the major ingredient as they are highly nutritive, and widely accepted by fish hence it was known as a highly palatable aquafeed ingredient [4]. It was easily procurable for the industry until a decline in marine production due to overfishing which subsequently led to excessive exploitation of the resource [52]. Thus, the search for cheap, alternative, and locally available ingredients evolved [53]. 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 different lupin seeds, processed lupin, conventional feed ingredients such as fish meal, soybean meal and novel protein ingredients from insects like black solider fly 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 first followed by black soldier fly 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 first 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 profile 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 profile 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 profile of lupin is remarkable and can easily be substituted for conventional feed ingredients.
3 The scenario of the global lupin market
The lupin market is predominantly situated in the Asia–Pacific region, with a strong focus on Australia, and is projected to expand further in North America and Europe. A noteworthy agricultural achievement was recorded in 2017 when 930,717 hectares of cultivable land across the globe yielded approximately 1610,969 tonnes of lupin, as reported by A. Cattaneo in the FAO 2018 reports. According to these findings, the lupin market's valuation reached USD 333.00 million in 2022, and projections suggest a growth to USD 426.33 million by 2030 maintaining a compound annual growth rate (CAGR) of 2.69% from 2023 to 2030 [61] as shown in Fig. 1.
Predicted Global Lupin Seed production [52]
3.1 Major niches in the market for lupin seeds
A significant element in the market's expansion in the food and beverage sector is the rising demand for lupin. The bean of lupin is also a rich source of fiber, protein, and potent vitamins, which contributes to its popularity for consumers who are concerned about their health. The growing demand for vegan goods and growing knowledge of dairy alternatives to meet dietary needs are major factors propelling the growth of the Lupin market.
The global production trends of lupin [62] (refer Fig. 2) gradually increased throughout the past decades. The maximum production in the year 2021, was around 2.57 billion kg with Australia alone providing 865.62 million kg followed by Poland at 222.139 million kg. From the year 2012–2022, there is an increasing production trend of about 51.47%, displaying growing production to satisfy the demand created. Figure 3 shows the top 10 global producers of lupin [63]. From the above graph, it's apparent that Australia contributes around 58.65% to global lupin production. Ranking second in the list is Poland contributing about 21.70%. Other countries provide a significant contribution to the global production. Lupin industry’s leading players are the prominent companies that were scrutinized and identified as key stakeholders within the industry. These include Blooming Foods, Lupina, Frank Food Products, Soja Austria, Lupins for Life, Coorow Seeds Golden West Foods Pty. Ltd., and Barentz International. Terrena, and Ugaoo.
Global production trend of lupin
Top 10 producers of lupin
3.2 Market segmentation
Market segmentation is the division of the market of a product in terms of consumer preferences. The global lupin market is driven by the application, production type, and regional requirements of lupin seeds. These factors generate “demand” for the product and act as accelerators for the global cultivation and production of lupin. In Fig. 4, the factors involved in the creation of the “demand” for the lupin seeds are listed below [61].
Market segmentation of Lupin
4 Classification of lupin
Lupins, based on the alkaloid content were classified as sweet and bitter lupin. Sweet lupin contains lower levels of alkaloids. But whereas bitter lupin contains higher levels of alkaloid content [64]. The following section describes in detail the sweet and bitter lupins. Hence, for this reason, sweet lupin is preferentially cultivated. Cultivation of the low-alkaloid Australian sweet lupin in Western Australia yields the majority of the world’s lupin seed, a crucial nitrogen-fixing rotation crop that supports sustainable grain production. Australian lupin seeds, which are traditionally utilized for livestock feed, are now gaining attention for their potential in human food applications, with recent research exploring the utilization of lupin seed fractions, including flour protein concentrates/isolates and dietary fiber [65]. In addition, Barlock lupin, gunyidi lupin, jenabillup lupin, leeman lupin, luxor lupin, and made up lupin are also trade names for lupin [66]. Pulse Australia’s guidelines for receiving and exporting albus lupins state that the allowable limit for bitter contaminants is set at 2 seeds/200 g. Given the typical size of albus seeds at 0.35 g each, this translates to a bitter seed frequency threshold of 1 in 285 seeds, or 0.35%.
4.1 Sweet lupin
Lupin types that generate very little or no alkaloids, fats, or ANF are referred to as sweet lupin. As a consequence, they possess greater quantities of protein than legumes such as soybeans. The commonly referred sweet lupins include Lupinus angustifolius, Lupinus albus, and Lupinus luteus. The gene responsible for the sweet taste of lupin is the “pauper” gene [62]. Moreover, to prevent the production of bitter varieties, crossing-over techniques are well utilized (by outcrossing between two sweet varieties), and the production of distinct sweetness genes is crucial for preserving this consistency. Blue lupin, also known as Lupinus angustifolius and characterized by its narrow leaves, is widely cultivated in Australia, Germany, and Poland, maintaining a high level of popularity in these regions.
4.1.1 Use of sweet lupin
Livestock feed: Lupin is utilized for its specialized nutritional profile in animal feeds. Livestock such as cattle, sheep, poultry, and aquaculture. Blue, white, and yellow lupins, three Mediterranean lupin varieties, are commonly farmed for use as animal and bird feed [28].
Food industry: Sweet lupin is used as a value-added food ingredient in the food industry. They are added to different cuisines, such as tofu, vegan natured sausages, flour and flakes. Wheat is partially replaced with lupin flour in the food processing industry to add flavor and a rich, creamy texture to the flour.
4.2 Bitter lupin
The bitter lupin is commonly referred to as the “lupini bean”, which accounts for the high amounts of bitter-tasting alkaloids that are present in both the vegetative material and the seeds of wild varieties of the broadleaf lupin Lupinus albus and pearl lupin (Lupinus mutabilis), which are cultivated in South America. It is customary that these large and bitter seeds are cultivated in nations such as Italy and in immigrant communities to employ them in this market sector, as people here prefer bitterness. Consequently, Australia has developed a tiny amount of lupini beans. The “lupine” regions typically have more rainfall and colder climates, including Tasmania, northeastern Victoria (near Benalla and Myrtleford), and the extreme lower southeastern region of South Australia, where large seed sizes and high yields are easily attainable. When the relatively infrequent presence of bitter seeds contaminates the sweet lupin harvest, there is a risk that the total alkaloid content in the bulk crop may exceed the Food Standard limit of 200 mg/kg for lupin alkaloids. Bitter seeds possess an alkaloid content ranging from 1.5% to 2.2%, equivalent to 15,000 to 22,000 mg per kilogram, which is ten thousand times greater than that found in sweet seeds.
4.2.1 Permeation of bitterness in lupin
It is well known that sweet or bitter varieties are influenced by genetics. Honeybees act as pollen carriers between sweet and bitter varieties; if they are cultivated in close proximity, this will pave the way for breeding between (outcross-breeding) varieties. This leads to the introduction of the genes responsible for bitterness in the sweet variety. It is also known that the bitter variety produces healthier and larger seeds than does the sweet variety, especially under adverse conditions. To guarantee the purity of future harvests, tests were conducted to verify that the certified seeds were free of bitterness. These certified seeds were subjected to a rigorous assessment spanning multiple generations using an ultraviolet (UV) lamp to confirm the absence of any bitter impurities. Certification is achieved after ensuring compliance with acceptable limits, and this certification is completed before the seeds are distributed.
5 Nutritional composition
The most frequently consumed component of the lupin plant is its seed, which is renowned for its substantial protein and dietary fiber content and minimal levels of antinutritional elements, such as phytates, protease inhibitors, and lectins. This lupin seed, a highly advantageous constituent for both human and animal consumption, can be rendered even more beneficial through the removal of alkaloids by debittering or the development of sweeteners through selective breeding, as emphasized by [67]. Reports indicate that the grain legume Lupinus angustifolius, commonly known as "sweet lupin," is predominantly cultivated in Western Australia and is characterized by its trace alkaloid content and low levels of fat and antinutritional components, as documented by [68].
5.1 Protein
Lupin is utilized for its protein content (30–40%). White lupin, which is also called “sweet lupin”, has various protein classifications. The major classes are the albumin family and globulin family. They are present at a ratio of 1:9 [69]. Pioneering research performed on the [70] separation of two fractions via electrophoresis of cellulose acetate on their constituent fractions. According to their mobility in the electrophoresis, they were termed the alpha (α), beta (β) and gamma (γ) bands. Table 3 shows the different protein fractions, functionalities, structures, and monomer information. The protein from lupin bean, which belongs to the legume family, is a source of amino acids that contain sulfur, specifically Met (methionine) and Cys (cysteine). Additionally, it shows comparatively lower levels of valine (Val) and tryptophan (T) while being rich in lysine. Lupine protein is characterized by elevated levels of glutamic acid, aspartic acid, and arginine [71].
The lupin seed, which can be deduced from the above, is rich in protein and is primarily used in animal nutrition since its protein profile is similar to that of eggs, with a match of 95% [83]. Compared to blue and yellow lupin seeds, lupin white seeds exhibit a greater essential amino acid index (EAAI) and protein efficiency ratio (PER), as determined by the availability of lysine and tyrosine [84]. The biological functions of important protein fractions are discussed below. γ-conglutin, due to its interaction with insulin receptors, aids in reducing glucose levels in the blood, thus acting as a hypoglycemic substance [85]. They also help to lower the serum levels of triglycerides and cholesterol [86].
5.2 Lipids
The seed seeds of lupine contain a significant quantity of oil, despite the plant not being classified as an oilseed. White or sweet lupine has a fat level of 2–3 g per 100 g [87, 88]. Nevertheless, lupine seeds exhibit a conspicuously low-fat composition; therefore, L. albus has emerged as a potentially valuable reservoir of advantageous vegetable fat sources. The oil obtained from unprocessed seeds predominantly comprises unsaturated fatty acids, accompanied by a minimal quantity of saturated fatty acid [89]. Alpha-linolenic acid (omega-3, 18:3) is the major unsaturated fatty acid, followed by oleic (omega-9, 18:1) and linoleic (omega-6.18:2) acids. L. albus in particular has a high linolenic acid content [71, 90,91,92]. Maintaining elevated levels of long-chain polyunsaturated fatty acids (PUFAs) and restricting the intake of saturated fatty acids (SFAs) in the diet is believed to contribute to optimal health. Specifically, the ratio of ω-6 to ω-3 fatty acids plays a crucial role in mitigating risk and preventing cardiac and other metabolic diseases. Among lupine seeds, the PUFA to SFA ratio ranges from 1.3 to 2.9:1 [93].
5.3 Carbohydrate
Unlike many other vegetables, lupine seeds contain minimal amounts of starch, making them a unique and nutritionally intriguing source of carbohydrates [94]. The small quantity of starch present can be categorized as resistant starch, which means that it undergoes slow digestion, leading to the steady flow of glucose into the blood [90]. Consequently, the predominant carbohydrates in fully developed lupine seeds are oligosaccharides and non-starchy polysaccharides, primarily originating from the cellular composition of the seed walls. Sucrose and indigestible galactosidase from the raffinose family are among the oligosaccharides present within cotyledons. The sugars found in polysaccharides constitute a significant portion of the cytosol-enclosing cell wall. Because of their polysaccharide content, lupins are excellent sources of dietary fiber. Compared with many other plants, white lupine possesses the greatest proportion of dietary fiber (40%) within its kernel. It additionally possesses a minimal GI (glycemic index) compared to any grain that is consistently consumed [95, 96]. Following the debittering procedure, 89% of the dietary fiber in L. albus is insoluble fiber. Cellulose accounts for the bulk of insoluble dietary fiber (79%). Hemicellulose and lignin constitute 14% and 7%, respectively, of the total [97, 98].
5.3.1 Lupin kernel
The Lupin kernel is a part of the lupin seed which is removed during the dehulling process. After dehulling, the seed is sent for further processing and this kernel ends up as a by-product of the dehulling of lupin seeds. Lupin kernel fiber (LKF) is a product that has a neutral gustatory flavor, a velvety feel, and potent oil- and water-binding capabilities. As a key byproduct of protein isolates produced from lupin, it is often dried to produce pure fiber food elements, which has favorable impacts on medical investigations on indices for metabolic ailments such as cardiovascular disease, overweight (obesity), and diabetes 2. It is considered a “prebiotic (probiotic substrate) fiber component” because it enhances the chemical setting in the colon and the balance of gastrointestinal microorganisms [65].
They are composed of fibers that are soluble and insoluble in nature. The soluble portion and a greater variety of polysaccharide classes, such as cellulose, non-starch non-cellulosic glucans, and pectin compounds, are present in greater amounts in the lupin kernel fiber, while lignin is absent [99]. The description of lupin kernel cell wall fiber reveals a composition comprising galactans with 1,4-linkages forming long chains and extensively branched arabinans connected through 1,5-linkages, with these arabinans being linked to the rhamnose units found within the central rhamnogalacturonan backbone [100]. The primary constituents of dietary fiber within the kernels consist predominantly of Raffinose family oligosaccharides, namely, verbascose, stachyose, and raffinose, in addition to non-starch polysaccharides. In mesophyll cells, this fiber assumes a thicker wall structure. Its composition comprises specific monosaccharides, including xylose (2.6%), glucose (7.6%), arabinose (11.5%), uronic acids (8.1%), and galactose (67.6%) [101, 102].
In an investigation [97], aimed at determining carbohydrate levels in the raffinose family during the developmental stages of different legumes. In this study, he showed that the quantity of the α-galactoside family, which is composed of the raffinose family, increased with maturation, and there was a negative correlation between maturation (days after flowering, DAF) and the presence of substances such as glucose, sucrose, fructose, galactose and myo-inositol. In lupin, the onset of this phenomenon occurred 45 DAF, and the maximum content of raffinose family carbohydrates was notably 10.4% in lupin compared to that in other legumes, such as peas and faba beans, whose contents were 3.8% and 4.5%, respectively. Soluble fibers, in contrast to insoluble fibers, are thought to have more advantageous metabolic effects. Their viscosity, for instance, can assist in controlling the level of glucose in the blood by overseeing the breakdown and uptake of nutrients [103]. Conversely, their capacity to ferment can (a) promote the maintenance of a balanced gut microbiota; and (b) produce an array of metabolically beneficial fermentation byproducts, such as short-chain fatty acids, which not only contribute to the regulation of cholesterol but also act as a conducive substrate for the cultivation of optimal and healthy colon cells [104, 105]. In contrast, the lupin hull (seed coat) is composed of low quantities of protein, lipids, micronutrients and phytochemicals. These fibers are primarily composed of nonstarch polysaccharides, which constitute approximately 96.5%, are primarily composed of cellulose and minor quantities of lignin, and are classified as insoluble fibers [106]. Soluble fibers constitute approximately 3.5% of the total fiber content. Thus, lupin showcases a promising alternative for conventional feed ingredients.
5.4 Antinutritional factors associated with Lupin
Substances that are identified as antinutritional agents are compounds present in food or feed that impede the optimal utilization of nutrients, affecting processes such as intake, digestion, and absorption. [107]. Compounds that are heat labile and heat stable are the two principal kinds of antinutritional factors. During heat processing, antinutritional substances such as proteinase inhibitors, lectins, and saponins are deactivated or removed [108]. The group of substances that are resistant to heat includes phytic acid, polyphenols (tannin, the most typical carbohydrate), oligosaccharides of the raffinose family and quinolizidine family alkaloids. In contrast, lupine species that possess substantially fewer lectins and trypsin inhibitors than other legumes, including kidney bean, cowpea and soybean [109]. The principal antinutritional components of sweet lupine are related to polyphenols, phytic acid, and Raffinose Family Oligosaccharides (RFOs); hence, the goal of plant biologists is to develop a sweet lupin that is free of alkaloids and can be eaten instantly by animals or humans after soaking in flowing water and then quickly transformed into food that is rich in protein [84]. The antinutritional constituents phytic acid, oligosaccharides, lectins, alkaloids, and saponins are frequently detected in very low or barely detectable amounts in white lupine seeds as shown in Fig. 5. Table 4 shows the composition of different ANFs present in the lupin, their location, their effects due to consuming ANFs, permissible limits, the processing technique applied for deactivating the ANFs and their applications. The limitation in the application of quinolizidine in various fields and its consumption by humans is its antinutritional properties, i.e., alkaloids coming under the quinolizidine group [110,111,112]. The elimination of these chemicals can be accomplished either by adopting genotypes with low concentrations of these substances or by using various processes, such as selection extraction, heating, soaking, fermentation, or germination [97, 113,114,115].
Major Anti nutritional factors present in Lupin. (Drawn using PubChem)
6 Methods of protein extraction from lupin and their effects on bioavailability
The physicochemical and structural properties of proteins, as well as their ability to alter their domain structures in response to environmental changes, are strongly associated with their lucrative properties, which are essential to the manufacturing of food [127, 128]. Environment-related variables can be categorized into two distinct categories: those that interact with food components such as ions, water, carbohydrates, lipids, proteins, and flavorings and those that are specific to the surrounding environment and include parameters such as temperature, pH, and ionic strength [129]. Throughout the steps of extraction, which follow application, and processing, several factors can directly impact these properties. The proper application of isolation methods and the maintenance of adequate storage conditions are essential for the preservation and improvement of these functional qualities. Due to the presence of quinolizidine alkaloid (QA), some lupin cultivars are poisonous. Considering that these compounds are secondary metabolites, their concentration varies depending on the species being cultivated, the cultivar, the days in culture, and the culture location [130].
6.1 Extraction process
The three primary processes, (1) utilizing water for extraction; (2) natural breakdown through biological processes; and (3) utilizing chemicals for extraction, are comprised of recognized debittering procedures. Based on the above, commercially formed techniques for concentration of the protein isolate are given by [131], The following three techniques can be employed for separating substances: (i) micellization, which is accomplished by salt-induced extraction and consequent dilutive precipitation; (ii) use of acid for extraction process; and (iii) initial alkaline extraction procedure, which is followed by either isoelectric coagulation or ultrafiltration. Diverse extraction processes and the corresponding protein isolate yields were documented by [131, 132]. As an alternative method for isolating lupin protein for use in dairy-related industries, [133] used the enzymatic hydrolysis of carbohydrates to isolate lupin protein.
Novel techniques are being developed since the application of thermal treatments poses challenges for preserving the nutritional value, quality, and functional attributes of food nutrients. In light of this, the use of novel ultrasound (US), i.e., low-power ultrasonication in the high-frequency range (100 kHz to 1 MHz) operating at less than 1 W per square centimeter (W cm−2) for the assessment of the physicochemical characteristics of food and high-power ultrasound in the frequency spectrum of 20 to 100 kilo-Hertz, was applied to change the properties of the food [134]. Table 5 shows the extraction processes for [130, 135]. Thus, the extracted protein isolates can be used as an aquafeed feed supplement [5]
7 In vitro fermentation of lupin seeds
According to a study on fermentation, the reduction of macromolecular proteins and ANFs to free amino acids, low-molecular-weight proteins, or peptides is primarily linked to increased nutrient quality and accessibility (bioavailability) [136]. In the context of the above, another experiment was performed in vitro fermentation of Broad beans (Vicia faba) vs. lupin seeds (Lupinus albus). According to their research, broad beans had a slightly reduced quantity of short-chain fatty acids (T-SCFAs) at 78.41 mM, but lupin seeds had a greater quantity at 81.52 mM. These findings suggest a more dynamic and improved regulation of the metabolomic functional output and gut microbiota [137]. In an experimental study using solid-state fermentation of lupin vs wheat and quinoa using Lactobacillus reuteri K777 and Lb. plantarum K779 strains for 72 h to enhance the health-related properties of lupin flour [138]. In continuation of the above study, another experimental design was made to study the cytotoxicity of flours of lupin, wheat and quinoa. The abovementioned study reports that fermented lupin flour has five times more cytotoxic activity than wheat and quinoa fermented flour against Caco-2, which is a short form of colon cancer cells [139]. An experiment to observe the effects of fermentation by Candida utilis, K. lactis, and Saccharomyces cerevisiae on the alkaloid content. The results of the study revealed an increase in protein (crude protein) content after fermentation and a decrease in NSP (primarily contributed by the oligosaccharide family of raffinose), phytate and alkaloid content (ANFs). Superior results were obtained when Candida utilis was used [140]. To study the effect of solid-state fermentation of lupin flour and use of filamentous fungi, such as Aspergillus sojae and Aspergillus ficuum was performed [141]. The changes in the physical, chemical and functional properties of lupin-based flour were observed. They help decrease the phytic acid content and enzyme protein digestion under in vitro conditions, thus facilitating easy digestion of the bolus.
8 Lupin seed digestibility
The lupin seed digestibility in fish is generally high [142]. Table 6 depicts few works on lupin seed digestibility in fish. From this, it can be inferred that the increased nutrient digestibility especially of protein and energy was high in rainbow trout when fed with lupin seed [142,143,144]. In addition, this was supported in porcine as well.
9 Impact of lupin on the fish health and growth
9.1 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 [5] 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%) [145, 146]. 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%) [147, 148]. In addition, the presence of non-starch polysaccharides, oligosaccharides, and anti-nutritional factors as discussed in Sect. 5.4 and Tables 4 and 6, 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 [149] of rainbow trout. Similarly, in Atlantic salmons, a partial replacement of lupin by 20 to 40% inclusion was deduced [150].
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 [151, 152]. Similarly in black carp, a partial replacement of soybean meal with lupin seed meal by 30% improved weight gain and feed efficiency ratio [153]. In blackhead seabream (Acanthopagrus schlegelii), a partial replacement of soybean meal with lupin seed meal with 30% favored growth [154]. In seabass, a dietary lupin seed meal inclusion at 40–50% with proper seed processing techniques improves the growth [155, 156]. In tilapia, dietary lupin seed can be up to 50% can be incorporated to produce high growth [157]. Turbot (Psetta maxima), an inclusion of 50% dietary lupin was found to improve growth [136]. In cobia (Rachycentron canadum), a dietary lupin inclusion of 10.5% provided growth as that of a fish meal [137]. In shellfishes like Penaeus monodon (black tiger shrimp), lupin seed meal can replace up to 40–50% of soybean meal [138]. For the Litopenaeus vannamei (white leg shrimp), 100 g per kg (10%) inclusion provided better growth when compared to 20or 30% inclusion [139].
9.2 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 [140]. Anti-bacterial compounds help fishes against invading pathogens. An investigation on the antioxidant properties of lupin seeds [158] 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 [141, 158,159,160]. The antioxidant effects of three lupin species, Lupinus albus (white), Lupinus angustifolius (narrow leaf), and Lupinus luteus (yellow), were described in detail by [38]. Polyphenolic compounds primarily occur in the peripheral parts or the external regions of the seed [40]. Table 7 shows the composition of the antioxidant compounds and their biological activities. The antibacterial properties of lupin have been investigated by [40]. 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.
10 Challenges and prospects of lupin
Though lupin promises to be a potential alternative to conventional feed ingredients, the presence of antinutritional factors 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 [53]. Individuals susceptible to exposure may develop occupational sensitization and allergies that manifest as conditions such as asthma, as indicated by research findings [161]. Additionally, severe reactions, including anaphylaxis, have been documented in the literature [162,163,164]. 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 [165, 166].
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.
11 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.
Data availability
No datasets were generated or analysed during the current study.
References
Maulu S, Hasimuna OJ, Monde C, Mweemba M. An Assessment of post-harvest fish losses and preservation practices in Siavonga district, Southern Zambia. Fish Aquatic Sci. 2020;23(1):25. https://doi.org/10.1186/s41240-020-00170-x.
Hazreen-Nita MK, Kari ZA, Mat K, Rusli ND, Sukri SAM, Harun HC, Lee SW, Rahman MM, Norazmi-Lokman NH, Nur-Nazifah M. Olive oil by-products in aquafeeds: opportunities and challenges. Aquac Rep. 2022;22: 100998.
Dawood MAO. Dietary copper requirements for aquatic animals: a review. Biol Trace Elem Res. 2022;200(12):5273–82. https://doi.org/10.1007/s12011-021-03079-1.
Rawles SD, Thompson KR, Brady YJ, Metts LS, Aksoy MY, Gannam AL, Twibell RG, Ostrand S, Webster CD. Effects of replacing fish meal with poultry by-product meal and soybean meal and reduced protein level on the performance and immune status of pond-grown sunshine bass (Morone Chrysops\times M. saxatilis). Aquac Nutr. 2011;17(3):e708–21.
Szczepański A, Adamek-Urbańska D, Kasprzak R, Szudrowicz H, Śliwiński J, Kamaszewski M. Lupin: a promising alternative protein source for aquaculture feeds? Aquac Rep. 2022;26: 101281.
FAO. The State of World Fisheries and Aquaculture 2022. Towards Blue Transformation. Geneva: The State of World Fisheries and Aquaculture (SOFIA); 2022.
Kuhn DD, Lawrence AL, Crockett J, Taylor D. Evaluation of bioflocs derived from confectionary food effluent water as a replacement feed ingredient for fishmeal or soy meal for shrimp. Aquaculture. 2016;454:66–71.
Davies SJ, Gouveia A. Response of common carp fry fed diets containing a pea seed meal (Pisum sativum) subjected to different thermal processing methods. Aquaculture. 2010;305(1–4):117–23.
Kamaszewski M, Prasek M, Ostaszewska T, Dabrowski K. The Influence of feeding diets containing wheat gluten supplemented with dipeptides or free amino acids on structure and development of the skeletal muscle of carp (Cyprinus carpio). Aquacult Int. 2014;22:259–71.
Tusche K, Arning S, Wuertz S, Susenbeth A, Schulz C. Wheat gluten and potato protein concentrate—promising protein sources for organic farming of rainbow trout (Oncorhynchus mykiss). Aquaculture. 2012;344:120–5.
Davies SJ, Morris PC, Baker RTM. Partial substitution of fish meal and full-fat soya bean meal with wheat gluten and influence of lysine supplementation in diets for rainbow trout, Oncorhynchus mykiss (Walbaum). Aquac Res. 1997;28(5):317–28.
Potki N, Falahatkar B, Alizadeh A. Growth, hematological and biochemical indices of common carp Cyprinus carpio fed diets containing corn gluten meal. Aquacult Int. 2018;26:1573–86.
Dossou S, Koshio S, Ishikawa M, Yokoyama S, Dawood MA, El Basuini MF, El-Hais AM, Olivier A. Effect of partial replacement of fish meal by fermented rapeseed meal on growth, immune response and oxidative condition of red sea bream juvenile, Pagrus major. Aquaculture. 2018;490:228–35.
Luo Y, Ai Q, Mai K, Zhang W, Xu W, Zhang Y. Effects of dietary rapeseed meal on growth performance, digestion and protein metabolism in relation to gene expression of juvenile cobia (Rachycentron canadum). Aquaculture. 2012;368:109–16.
Morken T, Kraugerud OF, Barrows FT, Sørensen M, Storebakken T, Øverland M. Sodium diformate and extrusion temperature affect nutrient digestibility and physical quality of diets with fish meal and barley protein concentrate for rainbow trout (Oncorhynchus mykiss). Aquaculture. 2011;317(1–4):138–45.
Zaretabar A, Oraji H, Yegane S, Keramat A. The effects of replacing fish meal with barley protein concentrate on digestive enzyme activity and hepatic enzymes of caspian salmon (Salmo trutta Caspius). Iran Sci Fish J. 2020;28:111.
Mulvaney WJ, Winberg PC, Adams L. Comparison of macroalgal (Ulva and Grateloupia Spp.) and formulated terrestrial feed on the growth and condition of juvenile abalone. J Appl Phycol. 2013;25:815–24.
Ju ZY, Deng D-F, Dominy W. A defatted microalgae (Haematococcus pluvialis) meal as a protein ingredient to partially replace fishmeal in diets of pacific white shrimp (Litopenaeus vannamei, Boone, 1931). Aquaculture. 2012;354:50–5.
Xia S, Yang H, Li Y, Liu S, Zhou Y, Zhang L. Effects of different seaweed diets on growth, digestibility, and ammonia-nitrogen production of the sea cucumber Apostichopus japonicus (Selenka). Aquaculture. 2012;338:304–8.
Liland NS, Araujo P, Xu XX, Lock E-J, Radhakrishnan G, Prabhu AJP, Belghit I. A meta-analysis on the nutritional value of insects in aquafeeds. JIFF. 2021;7(5):743–59. https://doi.org/10.3920/JIFF2020.0147.
Soetemans L, Uyttebroek M, Bastiaens L. Characteristics of chitin extracted from black soldier fly in different life stages. Int J Biol Macromol. 2020;165:3206–14.
Basto A, Calduch-Giner J, Oliveira B, Petit L, Sá T, Maia MR, Fonseca SC, Matos E, Pérez-Sánchez J, Valente LM. The use of defatted tenebrio molitor larvae meal as a main protein source is supported in European sea bass (Dicentrarchus Labrax) by data on growth performance, lipid metabolism, and flesh quality. Front Physiol. 2021;12: 659567.
Ferraris RP, Catacutan MR, Mabelin RL, Jazul AP. Digestibility in Milkfish, Chanos chanos (Forsskal): effects of protein source, fish size and salinity. Aquaculture. 1986;59(2):93–105.
Kamaszewski M, Ostaszewska T. The effect of feeding on morphological changes in intestine of pike-perch (Sander lucioperca L.). Aquac Int. 2014;22:245–58.
Ostaszewska T, Dabrowski K, Palacios ME, Olejniczak M, Wieczorek M. Growth and morphological changes in the digestive tract of rainbow trout (Oncorhynchus mykiss) and pacu (Piaractus mesopotamicus) due to casein replacement with soybean proteins. Aquaculture. 2005;245(1–4):273–86.
Terjesen BF, Lee K-J, Zhang Y, Failla M, Dabrowski K. Optimization of dipeptide-protein mixtures in experimental diet formulations for rainbow trout (Oncorhynchus mykiss) alevins. Aquaculture. 2006;254(1–4):517–25.
Zehra S, Khan MA. Dietary phenylalanine requirement and tyrosine replacement value for phenylalanine for fingerling Catla catla (Hamilton). Aquaculture. 2014;433:256–65.
Abraham EM, Ganopoulos I, Madesis P, Mavromatis A, Mylona P, Nianiou-Obeidat I, Parissi Z, Polidoros A, Tani E, Vlachostergios D. The use of lupin as a source of protein in animal feeding: genomic tools and breeding approaches. Int J Mol Sci. 2019;20(4):851.
Byerlee D, Stevenson J, Villoria N. Does intensification slow crop land expansion or encourage deforestation? Glob Food Sec. 2014;3(2):92–8.
Dunia, B. World Bank Commodities Price Data (The Pink Sheet). Diambil dari: http://pubdocs.worldbank.org/en/992071585858056509/CMO-Pink-Sheet-April-2020.pdf. 2020.
Urugo MM, Tringo TT. Naturally occurring plant food toxicants and the role of food processing methods in their detoxification. Int J Food Sci. 2023;2023:1.
Krogdahl Å, Penn M, Thorsen J, Refstie S, Bakke AM. Important antinutrients in plant feedstuffs for aquaculture: an update on recent findings regarding responses in salmonids. Aquac Res. 2010;41(3):333–44.
Martins SJ, Rocha GA, de Melo HC, de Castro Georg R, Ulhôa CJ, de Campos Dianese É, Oshiquiri LH, da Cunha MG, da Rocha MR, de Araújo LG. Plant-associated bacteria mitigate drought stress in soybean. Environ Sci Pollut Res. 2018;25:13676–86.
Sharma A. A review on traditional technology and safety challenges with regard to antinutrients in legume foods. J Food Sci Technol. 2021;58(8):2863–83.
D’Agostina A, Antonioni C, Resta D, Arnoldi A, Bez J, Knauf U, Wäsche A. Optimization of a pilot-scale process for producing lupin protein isolates with valuable technological properties and minimum thermal damage. J Agric Food Chem. 2006;54(1):92–8. https://doi.org/10.1021/jf0518094.
Gladstones JS. Lupins as crop plants. Field Crop Abstr. 1970;23:123–48.
Porras-Saavedra J, Guemez-Vera N, Montañez-Soto JL, Fernandez-Martinez MC, Yanez-Fernandez J. Comparative study of functional properties of protein isolates obtained from three lupinus species. Adv Biorese. 2013;4(4):106–16.
Siger A, Czubinski J, Kachlicki P, Dwiecki K, Lampart-Szczapa E, Nogala-Kalucka M. Antioxidant activity and phenolic content in three lupin species. J Food Compos Anal. 2012;25(2):190–7.
James LF, Panter KE, Gaffield W, Molyneux RJ. Biomedical applications of poisonous plant research. J Agric Food Chem. 2004;52(11):3211–30.
Lampart-Szczapa E, Siger A, Trojanowska K, Nogala-Kalucka M, Malecka M, Pacholek B. Chemical composition and antibacterial activities of lupin seeds extracts. Food Nahrung. 2003;47(5):286–90.
Gaultier F, Foucault-Bertaud A, Lamy E, Ejeil AL, Dridi SM, Piccardi N, Piccirilli A, Msika P, Godeau G, Gogly B. Effects of a vegetable extract from Lupinus albus (LU105) on the production of matrix metalloproteinases (MMP1, MMP2, MMP9) and tissue inhibitor of metalloproteinases (TIMP1, TIMP2) by human gingival fibroblasts in culture. Clin Oral Invest. 2003;7:198–205.
Farrell DJ, Perez-Maldonado RA, Mannion PF. Optimum inclusion of field peas, faba beans, chick peas and sweet lupins in poultry diets. II. Broiler experiments. Br Poultry Sci. 1999;40(5):674–80. https://doi.org/10.1080/00071669987070.
Jayasena V, Nasar-Abbas SM. Development and quality evaluation of high-protein and high-dietary-fiber pasta using lupin flour. J Texture Stud. 2012;43(2):153–63.
Jayasena V, Tah WY, Nasar-Abbas SM. Effect of coagulant type and concentration on the yield and quality of soy-lupin tofu. Qual Assur Saf Crops Foods. 2014;6(2):159–66.
Rumiyati R, James AP, Jayasena V. Effects of lupin incorporation on the physical properties and stability of bioactive constituents in muffins. Int J Food Sci Technol. 2015;50(1):103–10.
Priatni S, Devi AF, Kardono LB, Jayasena V. Quality and sensory evaluations of tempe prepared from various particle sizes of lupin beans [Evaluasi Sensorik Dan Kualitas Tempe Dari Kacang Lupin Berbagai Ukuran Partikel]. J Teknol dan Ind Pangan. 2013;24(2):209–209.
Jayasena V, Nasar-Abbas SM. Effect of lupin flour incorporation on the physical characteristics of dough and biscuits. Qual Assur Saf Crops Foods. 2011;3(3):140–7.
Jayasena V, Leung PP, Nasar-Abbas SM. Effect of lupin flour substitution on the quality and sensory acceptability of instant noodles. J Food Qual. 2010;33(6):709–27.
Güémes-Vera N, Martinez-Herrera J, Hernandez-Chavez JF, Yanez-Fernandez J, Totosaus A. Comparison of chemical composition and protein digestibility, carotenoids, tannins and alkaloids content of wild lupinus varieties flour. Pak J Nutr. 2012;11(8):676–82.
Erickson JP. Lupins show potential as protein source for livestock. Feedstuffs. 1985;57(5):22–4.
Bähr M, Fechner A, Hasenkopf K, Mittermaier S, Jahreis G. Chemical composition of dehulled seeds of selected lupin cultivars in comparison to pea and soya bean. LWT Food Sci Technol. 2014;59(1):587–90.
Olsen RL, Hasan MR. A limited supply of fishmeal: impact on future increases in global aquaculture production. Trends Food Sci Technol. 2012;27(2):120–8.
Béné C, Arthur R, Norbury H, Allison EH, Beveridge M, Bush S, Campling L, Leschen W, Little D, Squires D. Contribution of fisheries and aquaculture to food security and poverty reduction: assessing the current evidence. World Dev. 2016;79:177–96.
Inra, proximate composition, Feedipedia www.feedipedia.org. Accessed 16 Apr 2024.
Abeshu Y, Kefale B. Effect of some traditional processing methods on nutritional composition and alkaloid content of lupin bean. Int J Bioorg Chem. 2017;2(4):174–9.
Oteri M, Di Rosa AR, Lo Presti V, Giarratana F, Toscano G, Chiofalo B. Black soldier fly larvae meal as alternative to fish meal for aquaculture feed. Sustainability. 2021;13(10):5447.
Lee JW, Kil DY, Keever BD, Killefer J, McKeith FK, Sulabo RC, Stein HH. Carcass fat quality of pigs is not improved by adding corn germ, beef tallow, palm kernel oil, or glycerol to finishing diets containing distillers dried grains with solubles. J Anim Sci. 2013;91(5):2426–37.
INRA, feedipedia. www.feedipedia.org. Accessed 18 Apr 2024.
Cho JH, Kim IH. Fish meal–nutritive value. Anim Physiol Nutr. 2011;95(6):685–92. https://doi.org/10.1111/j.1439-0396.2010.01109.x.
Liu Z, Liu Q, Zhang D, Wei S, Sun Q, Xia Q, Shi W, Ji H, Liu S. Comparison of the proximate composition and nutritional profile of byproducts and edible parts of five species of shrimp. Foods. 2021;10(11):2603.
Research and Markets report. Global Lupin Market Size, Trends, and Growth Opportunity, By Product Type, By Application, By Region and forecast till 2030. https://www.researchandmarkets.com/reports/5781500/global-lupin-market-size-trends-growth. Accessed 22 Sep 2023.
Luckett D. Lupine Bean–a bitter contamination risk for sweet albus lupines. primefacts 682. NSW Government, Industry and Investment, 2010.
FAO. Lupin production and top producing countries. https://www.tridge.com/intelligences/lupin-bean/production. Accessed 13 Apr 2024.
Tirdilová I, Vollmannová A, Čéryová S, Obtulovič P, Árvay J, Zetochová E. Impact of 3-year period as a factor on the content of biologically valuable substances in seeds of white lupin. Plants. 2022;11(16):2087.
Malekipoor R, Johnson SK, Bhattarai RR. Lupin kernel fibre: nutritional composition, processing methods, physicochemical properties, consumer acceptability and health effects of its enriched products. Nutrients. 2022;14(14):2845. https://doi.org/10.3390/nu14142845.
Lupin varieties. https://www.seednet.com.au/products/lupins. Accessed 18 Oct 2023.
Cowling WA, Buirchell BJ, Tapia ME. Lupin. Lupinus L. Maccarese: International Plant Genetic Resources Institute; 1998.
Dagnia SG, Petterson DS, Bell RR, Flanagan FV. Germination alters the chemical composition and protein quality of lupin seeds. J Sci Food Agric. 1992;60(4):419–23. https://doi.org/10.1002/jsfa.2740600403.
Duranti M, Restani P, Poniatowska M, Cerletti P. The Seed globulins of Lupinus albus. Phytochemistry. 1981;20(9):2071–5.
Blagrove RJ, Gillespie JM. Isolation, purification and characterization of the seed globulins of Lupinus angustifolius. Funct Plant Biol. 1975;2(1):13–27.
Manickavasagan A, Thirunathan P. Pulses: processing and product development. Cham: Springer Nature; 2020.
Duranti M, Consonni A, Magni C, Sessa F, Scarafoni A. The Major proteins of lupin seed: characterisation and molecular properties for use as functional and nutraceutical ingredients. Trends Food Sci Technol. 2008;19(12):624–33.
Müntz K. Deposition of storage proteins. In: Soll J, editor. Protein trafficking in plant cells. Dordrecht: Springer; 1998. p. 77–99. https://doi.org/10.1007/978-94-011-5298-3_4.
Salmanowicz BP, Weder JKP. Primary Structure of 2S Albumin from Seeds of Lupinus albus. Z Lebensm Forsch A. 1997;204(2):129–35. https://doi.org/10.1007/s002170050049.
Gayler KR, Wachsmann F, Kolivas S, Nott R, Johnson ED. Isolation and characterization of protein bodies in Lupinus angustifolius. Plant Physiol. 1989;91(4):1425–31.
Duranti M, Sessa F, Carpen A. Identification, purification and properties of the precursor of conglutin β, the 7S storage globulin of Lupinus albus L. Seeds J Exp Bot. 1992;43(10):1373–8.
Magni C, Scarafoni A, Herndl A, Sessa F, Prinsi B, Espen L, Duranti M. Combined 2D electrophoretic approaches for the study of white lupin mature seed storage proteome. Phytochemistry. 2007;68(7):997–1007.
Shewry PR, Napier JA, Tatham AS. Seed storage proteins: structures and biosynthesis. Plant Cell. 1995;7(7):945.
Duranti M, Faoro F, Harris N. The unusual extracellular localization of conglutin γ in germinating Lupinus albus seeds rules out its role as a storage protein. J Plant Physiol. 1994;143(6):711–6.
Duranti M, Scarafoni A, Di Cataldo A, Sessa F. Interaction of metal ions with lupin seed conglutin γ. Phytochemistry. 2001;56(6):529–33. https://doi.org/10.1016/S0031-9422(00)00426-X.
Duranti M. The structure of lupine seed proteins. Nahrung. 1986;30(3–4):221–7. https://doi.org/10.1002/food.19860300303.
Restani P, Duranti M, Cerletti P, Simonetti P. Subunit composition of the seed globulins of Lupinus albus. Phytochemistry. 1981;20(9):2077–83.
Egaña JI, Uauy R, Cassorla X, Barrera G, Yañez E. Sweet lupin protein quality in young men. J Nutr. 1992;122(12):2341–7.
Sujak A, Kotlarz A, Strobel W. Compositional and nutritional evaluation of several lupin seeds. Food Chem. 2006;98(4):711–9. https://doi.org/10.1016/j.foodchem.2005.06.036.
Magni C, Sessa F, Accardo E, Vanoni M, Morazzoni P, Scarafoni A, Duranti M. Conglutin gamma, a lupin seed protein, binds insulin in vitro and reduces plasma glucose levels of hyperglycemic rats. J Nutr Biochem. 2004;15(11):646–50. https://doi.org/10.1016/j.jnutbio.2004.06.009.
Sirtori CR, Lovati MR, Manzoni C, Castiglioni S, Duranti M, Magni C, Morandi S, D’Agostina A, Arnoldi A. Proteins of white lupin seed, a naturally isoflavone-poor legume, reduce cholesterolemia in rats and increase LDL receptor activity in HepG2 cells. J Nutr. 2004;134(1):18–23. https://doi.org/10.1093/jn/134.1.18.
Sedláková K, Straková E, Suchỳ P, Krejcarová J, Herzig I. Lupin as a perspective protein plant for animal and human nutrition–a review. Acta Vet Brno. 2016;85(2):165–75.
Písaříková B, Zralỳ Z. Nutritional value of lupine in the diets for pigs (a review). Acta Vet Brno. 2009;78(3):399–409.
Uzun B, Arslan C, Karhan M, Toker C. Fat and fatty acids of white lupin (Lupinus albus L.) in comparison to sesame (Sesamum indicum L.). Food Chem. 2007;102(1):45–9.
Trugo LC, Baer E, Baer D. Lupin: breeding. EncyclopeD Food Grains. 2016. https://doi.org/10.1016/B978-0-12-394437-5.00211-4.
Calabrò S, Cutrignelli MI, Lo Presti V, Tudisco R, Chiofalo V, Grossi M, Infascelli F, Chiofalo B. Characterization and effect of year of harvest on the nutritional properties of three varieties of white lupine (Lupinus albus L.): nutritional properties of three varieties of white lupine. J Sci Food Agric. 2015;95(15):3127–36. https://doi.org/10.1002/jsfa.7049.
Chiofalo B, Presti VL, Chiofalo V, Gresta F. The productive traits, fatty acid profile and nutritional indices of three lupin (Lupinus spp.) species cultivated in a mediterranean environment for the livestock. Anim Feed Sci Technol. 2012;171(2–4):230–9. https://doi.org/10.1016/j.anifeedsci.2011.11.005.
Pereira A, Ramos F, Sanches Silva A. Lupin (Lupinus albus L.) seeds: balancing the good and the bad and addressing future challenges. Molecules. 2022;27(23):8557. https://doi.org/10.3390/molecules27238557.
Arnoldi A, Greco S. Nutritional and nutraceutical characteristics of lupin protein. Nutrafoods. 2011;10(4):23–9. https://doi.org/10.1007/BF03223356.
Getachew P. Chemical composition and the effects of traditional processing on nutritional composition of Gibto (Lupinus albus. L) Grown in, Gojam Area. Thesis, Addis Ababa University, 2009.
Phan HT, Ellwood SR, Adhikari K, Nelson MN, Oliver RP. The first genetic and comparative map of white lupin (Lupinus albus L.): identification of QTLs for anthracnose resistance and flowering time, and a locus for alkaloid content. DNA Res. 2007;14(2):59–70.
Kohajdová Z, Karovičová J, Schmidt Š. Lupin composition and possible use in bakery—a review. Czech J Food Sci. 2011;29(3):203–11. https://doi.org/10.17221/252/2009-CJFS.
Zerihun N. Contribution of white lupin (Lupinus albus L.) for food security in north-western Ethiopia: a review. Asian J Plant Sci. 2012;11(5):200–5.
Mohamed AA, Rayas-Duarte P. Composition of Lupinus albus. Cereal Chem. 1995;72(6):643–7.
Cheetham NW, Cheung PC-K, Evans AJ. Structure of the principal non-starch polysaccharide from the cotyledons of Lupinus angustifolius (Cultivar Gungurru). Carbohyd Polym. 1993;22(1):37–47.
Brillouet JM, Riochet D. Cell wall polysaccharides and lignin in cotyledons and hulls of seeds from various lupin (Lupinus L.) species. J Sci Food Agric. 1983;34(8):861–8.
Crawshaw LA, Reid JG. Changes in cell-wall polysaccharides in relation to seedling development and the mobilisation of reserves in the cotyledons of Lupinus angustifolius cv. Unicrop. Planta. 1984;160:449–54.
Anderson JW, Baird P, Davis RH, Ferreri S, Knudtson M, Koraym A, Waters V, Williams CL. Health benefits of dietary fiber. Nutr Rev. 2009;67(4):188–205. https://doi.org/10.1111/j.1753-4887.2009.00189.x.
Slavin JL. Position of the American dietetic association: health implications of dietary fiber. J Am Diet Assoc. 2008;108(10):1716–31. https://doi.org/10.1016/j.jada.2008.08.007.
Slavin J. Fiber and prebiotics: mechanisms and health benefits. Nutrients. 2013;5(4):1417–35. https://doi.org/10.3390/nu5041417.
Mohamed A, Rayas-Duarte P. Nonstarchy polysaccharide analysis of cotyledon and hull of Lupinus albus. Cereal Chem. 1995;72(6):648–51.
Udousoro II, Ekop RU, Udo EJ. Effect of thermal processing on antinutrients in common edible green leafy vegetables grown in Ikot Abasi, Nigeria. Pak J Nutr. 2013;12(2):162.
Dello JPE. Contaminants and toxins in animal feeds. FAO animal production and health paper, 2004, No. 160. Edinburgh: Scottish Agricultural College (SAC); 2004.
Martin-Cabrejas MA, Esteban RM, Waldron KW, Maina G, Grant G, Bardocz S, Pusztai A. Hard-to-cook phenomenon in beans: changes in antinutrient factors and nitrogenous compounds during storage. J Sci Food Agric. 1995;69(4):429–35. https://doi.org/10.1002/jsfa.2740690405.
Michael JP. Indolizidine and quinolizidine alkaloids. Nat Prod Rep. 2002;19(6):719–41.
Michael JP. Indolizidine and quinolizidine alkaloids. Nat Prod Rep. 2003;20(5):458–75.
Torres KB, Quintos NR, Necha LLB, Wink M. Alkaloid profile of leaves and seeds of Lupinus hintonii CP Smith. Z Naturforsch C. 2002;57(3–4):243–7.
Martínez-Villaluenga C, Frías J, Vidal-Valverde C. Functional lupin seeds (Lupinus albus L. and Lupinus luteus L.) after extraction of α-galactosides. Food Chem. 2006;98(2):291–9. https://doi.org/10.1016/j.foodchem.2005.05.074.
Pastor-Cavada E, Juan R, Pastor JE, Alaiz M, Vioque J. Analytical nutritional characteristics of seed proteins in six wild lupinus species from Southern Spain. Food Chem. 2009;117(3):466–9. https://doi.org/10.1016/j.foodchem.2009.04.039.
Prusinski J. White lupin (Lupinus albus L.)—nutritional and health values in human nutrition—a review. Czech J Food Sci. 2017;35(2):95–105. https://doi.org/10.17221/114/2016-CJFS.
Resta D, Boschin G, D’Agostina A, Arnoldi A. Evaluation of total quinolizidine alkaloids content in lupin flours, lupin-based ingredients, and foods. Mol Nutr Food Res. 2008;52(4):490–5. https://doi.org/10.1002/mnfr.200700206.
Magalhães SCQ, Fernandes F, Cabrita ARJ, Fonseca AJM, Valentão P, Andrade PB. Alkaloids in the valorization of european Lupinus Spp. seeds crop. Ind Crops Prod. 2017;95:286–95. https://doi.org/10.1016/j.indcrop.2016.10.033.
Wiedemann M, Gurrola-Díaz CM, Vargas-Guerrero B, Wink M, García-López PM, Düfer M. Lupanine Improves glucose homeostasis by influencing KATP channels and insulin gene expression. Molecules. 2015;20(10):19085–100. https://doi.org/10.3390/molecules201019085.
Villalpando-Vargas F, Medina-Ceja L. Effect of sparteine on status epilepticus induced in rats by pentylenetetrazole, pilocarpine and kainic acid. Brain Res. 2015;1624:59–70. https://doi.org/10.1016/j.brainres.2015.07.017.
Trugo LC, Donangelo CM, Duarte YA, Tavares CL. Phytic acid and selected mineral composition of seed from wild species and cultivated varieties of lupin. Food Chem. 1993;47(4):391–4. https://doi.org/10.1016/0308-8146(93)90183-G.
Johnson CR, Thavarajah P, Fenlason A, McGee R, Kumar S, Combs GF Jr. A global survey of low-molecular weight carbohydrates in lentils. J Food Compos Anal. 2015;44:178–85.
Lucas MM, Stoddard FL, Annicchiarico P, Frías J, Martinez-Villaluenga C, Sussmann D, Duranti M, Seger A, Zander PM, Pueyo JJ. The future of lupin as a protein crop in Europe. Front Plant Sci. 2015;6:705.
Zhang J, Song G, Mei Y, Li R, Zhang H, Liu Y. Present status on removal of raff inose family oligosaccharides—a review. Czech J Food Sci. 2019;37(3):141–54.
Mironenko AV, Domash VI, Chekhova AN, Sharova ZN. Activities of protein-inhibitors of proteases in seeds of different varieties of yellow and white lupine plants. Prikl Biokhim Mikrobiol. 1979;15(5):760–3.
Cabello-Hurtado F, Keller J, Ley J, Sanchez-Lucas R, Jorrín-Novo JV, Aïnouche A. Proteomics for exploiting diversity of lupin seed storage proteins and their use as nutraceuticals for health and welfare. J Proteomics. 2016;143:57–68. https://doi.org/10.1016/j.jprot.2016.03.026.
Luckett D. Lupin bean: a bitter contamination risk for sweet albus lupins. NSW department of primary industries, Agnote DPI-498. 2004. p. 18.
Hettiarachchy NS, Ziegler GR. Protein functionality in food systems. Boca Raton: CRC Press; 1994.
Kinsella JE. Functional properties of soy proteins. J Am Oil Chem Soc. 1979;56(31):242–58. https://doi.org/10.1007/BF02671468.
Deshpande SS, Damodaran S. Structure-digestibility relationship of legume 7S proteins. J Food Sci. 1989;54(1):108–13. https://doi.org/10.1111/j.1365-2621.1989.tb08579.x.
Aguilar-Acosta L, Serna-Saldivar S, Rodríguez-Rodríguez J, Escalante-Aburto A, Chuck-Hernández C. Effect of ultrasound application on protein yield and fate of alkaloids during lupin alkaline extraction process. Biomolecules. 2020;10(2):292. https://doi.org/10.3390/biom10020292.
Shrestha S, van’t Hag L, Haritos VS, Dhital S. Lupin proteins: structure, isolation and application. Trends Food Sci Technol. 2021;116:928–39.
Lo B, Kasapis S, Farahnaky A. Lupin protein: isolation and techno-functional properties, a review. Food Hydrocoll. 2021;112: 106318.
Kuznetsova L, Zabodalova L, Baranenko D. On the potential of lupin protein concentrate made by enzymatic hydrolysis of carbohydrates in dairy-like applications. Agron Res. 2014;12(3):727–36.
Knorr D, Zenker M, Heinz V, Lee D-U. Applications and potential of ultrasonics in food processing. Trends Food Sci Technol. 2004;15(5):261–6.
Wäsche A, Müller K, Knauf U. New processing of lupin protein isolates and functional properties. Nahrung. 2001;45(6):393. https://doi.org/10.1002/1521-3803(20011001)45:6%3c393::AID-FOOD393%3e3.0.CO;2-O.
Burel C, Boujard T, Tulli F, Kaushik SJ. Digestibility of extruded peas, extruded lupin, and rapeseed meal in rainbow trout (Oncorhynchus mykiss) and turbot (Psetta maxima). Aquaculture. 2000;188(3–4):285–98.
Pham HD, Siddik MA, Fotedar R, Chaklader MR, Foysal MJ, Nguyen CM, Munilkumar S. Substituting fishmeal with lupin Lupinus angustifolius kernel meal in the diets of cobia Rachycentron canadum: effects on growth performance, nutrient utilization, haemato-physiological response, and intestinal health. Anim Feed Sci Technol. 2020;267: 114556.
Smith DM, Tabrett SJ, Glencross BD. Growth response of the black tiger shrimp, Penaeus monodon fed diets containing different lupin cultivars. Aquaculture. 2007;269(1–4):436–46.
Weiss M, Rebelein A, Slater MJ. Lupin kernel meal as fishmeal replacement in formulated feeds for the whiteleg shrimp (Litopenaeus Vannamei ). Aquacult Nutr. 2020;26(3):752–62. https://doi.org/10.1111/anu.13034.
Aklakur M. Natural antioxidants from sea: a potential industrial perspective in aquafeed formulation. Rev Aquac. 2018;10(2):385–99. https://doi.org/10.1111/raq.12167.
Shahidi F, Chandrasekara A. Millet grain phenolics and their role in disease risk reduction and health promotion: a review. J Funct Foods. 2013;5(2):570–81.
Glencross B, Hawkins W, Veitch C, Dods K, Mccafferty P, Hauler R. The influence of dehulling efficiency on the digestible value of lupin (Lupinus angustifolius) kernel meal when fed to rainbow trout (Oncorhynchus mykiss). Aquac Nutr. 2007;13(6):462–70. https://doi.org/10.1111/j.1365-2095.2007.00499.x.
Glencross B. The influence of soluble and insoluble lupin non-starch polysaccharides on the digestibility of diets fed to rainbow trout (Oncorhynchus mykiss). Aquaculture. 2009;294(3–4):256–61. https://doi.org/10.1016/j.aquaculture.2009.06.010.
Glencross BD, Boujard T, Kaushik SJ. Influence of oligosaccharides on the digestibility of lupin meals when fed to rainbow trout, Oncorhynchus mykiss. Aquaculture. 2003;219(1–4):703–13.
Hughes SG. Use of lupin flour as a replacement for full-fat soy in diets for rainbow trout (Oncorhynchus mykiss). Aquaculture. 1991;93(1):57–62.
Hughes SG. Assessment of lupin flour as a diet ingredient for rainbow trout (Salmo gairdneri). Aquaculture. 1988;71(4):379–85.
Hernández AJ, Román D, Hooft J, Cofre C, Cepeda V, Vidal R. Growth performance and expression of immune-regulatory genes in rainbow trout (Oncorhynchus mykiss ) juveniles fed extruded diets with varying levels of lupin (Lupinus albus), Peas (Pisum sativum) and rapeseed (Brassica napus). Aquacult Nutr. 2013;19(3):321–32. https://doi.org/10.1111/j.1365-2095.2012.00961.x.
De la Higuera M, Garcia-Gallego M, Sanz A, Cardenete G, Suarez MD, Moyano FJ. Evaluation of lupin seed meal as an alternative protein source in feeding of rainbow trout (Salmo gairdneri). Aquaculture. 1988;71(1–2):37–50.
Hernández AJ, Roman D. Phosphorus and nitrogen utilization efficiency in rainbow trout (Oncorhynchus mykiss) fed diets with lupin (Lupinus albus) or soybean (Glycine max) meals as partial replacements to fish meal. Czech J Anim Sci. 2016. https://doi.org/10.17221/8729-CJAS.
Salini MJ, Adams LR. Growth performance, nutrient utilisation and digestibility by atlantic salmon (Salmo salar L.) fed tasmanian grown white (Lupinus albus) and narrow-leafed (L. angustifolius) lupins. Aquaculture. 2014;426:296–303.
Anwar A, Wan AH, Omar S, El-Haroun E, Davies SJ. The Potential of a solid-state fermentation supplement to augment white lupin (Lupinus albus) meal incorporation in diets for farmed common carp (Cyprinus carpio). Aquac Rep. 2020;17: 100348.
Anwar A. Inclusion of lupin meal and effect of a commercial feed supplement (SynergenTM) in diets for carp, Cyprinus carpio. 2013. Master Thesis, University of Plymouth. p 144.
Yang SD, Lin TS, Liou CH, Chien YH, Peng HK, Liao I-C. Partial substitution of white fish meal with soybean meal or lupin meal in diets for fingerling black carp (Mylopharyngodon piceus). J Fish Soc Taiwan. 2001. https://doi.org/10.5555/20023050378.
Zhang Y, Øverland M, Xie S, Dong Z, Lv Z, Xu J, Storebakken T. Mixtures of lupin and pea protein concentrates can efficiently replace high-quality fish meal in extruded diets for juvenile black sea bream (Acanthopagrus schlegeli). Aquaculture. 2012;354:68–74.
Fotedar R, Munilkumar S. Effects of organic selenium supplementation on growth, glutathione peroxidase activity and histopathology in juvenile barramundi (Lates calcarifer Bloch 1970) fed high lupin meal-based diets. Aquaculture. 2016;457:15–23.
Van Vo B, Bui DP, Nguyen HQ, Fotedar R. Optimized fermented lupin (Lupinus angustifolius) inclusion in juvenile barramundi (Lates calcarifer) diets. Aquaculture. 2015;444:62–9.
Bowyer PH, El-Haroun ER, Salim HS, Davies SJ. Benefits of a commercial solid-state fermentation (SSF) product on growth performance, feed efficiency and gut morphology of juvenile Nile tilapia (Oreochromis niloticus) fed different UK lupin meal cultivars. Aquaculture. 2020;523: 735192.
Galleano M, Pechanova O, Fraga CG. Hypertension, nitric oxide, oxidants, and dietary plant polyphenols. Curr Pharm Biotechnol. 2010;11(8):837–48.
Sato S, Mukai Y, Yamate J, Kato J, Kurasaki M, Hatai A, Sagai M. Effect of polyphenol-containing azuki bean (Vigna angularis) extract on blood pressure elevation and macrophage infiltration in the heart and kidney of spontaneously hypertensive rats. Clin Exp Pharm Physiol. 2008;35(1):43–9. https://doi.org/10.1111/j.1440-1681.2007.04743.x.
Taku K, Umegaki K, Sato Y, Taki Y, Endoh K, Watanabe S. Soy isoflavones lower serum total and LDL cholesterol in humans: a meta-analysis of 11 randomized controlled trials. Am J Clin Nutr. 2007;85(4):1148–56.
Crespo JF, Rodríguez J, Vives R, James JM, Reaño M, Daroca P, Burbano C, Muzquiz M. Occupational IgE-mediated allergy after exposure to lupine seed flour. J Allergy Clin Immunol. 2001;108(2):295–7.
Hieta N, Hasan T, Mäkinen-Kiljunen S, Lammintausta K. Lupin allergy and lupin sensitization among patients with suspected food allergy. Ann Allergy Asthma Immunol. 2009;103(3):233–7.
Campbell C, Jackson A, Thomas PS, Yates DH. Occupational asthma due to inhalation of lupin dust: a new cause of occupational asthma in Australia. J Allergy Clin Immunol. 2007;119:1133–9.
Parisot L, Aparicio C, Moneret-Vautrin DA, Guerin L. Allergy to Lupine Flour. Allergy. 2001;56(9):918–9.
Campbell CP, Yates DH. Lupin allergy: a hidden killer at home, a menace at work; occupational disease due to lupin allergy: occupational lupin sensitization. Clin Exp Allergy. 2010;40(10):1467–72. https://doi.org/10.1111/j.1365-2222.2010.03591.x.
Bakerly ND, Moore VC, Vellore AD, Jaakkola MS, Robertson AS, Burge PS. Fifteen-year trends in occupational asthma: data from the shield surveillance scheme. Occup Med. 2008;58(3):169–74. https://doi.org/10.1093/occmed/kqn007.
Author information
Authors and Affiliations
Contributions
KM and PK wrote the main manuscript text and figures. AR has offered mentorship, contributed to the conceptualization, and reviewed the draft of the manuscript. All authors reviewed the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
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
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s44279-024-00054-x