Cultivation of Black Soldier Fly (Hermetia illucens) Larvae for the Valorization of Spent Coffee Ground: A Systematic Review and Bibliometric Study

Abstract

The global surge in coffee consumption has led to the generation of significant amounts of spent coffee grounds (SCG), a by-product of the brewing process. If it is left unprocessed in the landfill, it will generate methane, one of the greenhouse gases, and therefore accelerate global warming. The intersection of SCG and its potential as a substrate for black soldier fly (BSF) larvae cultivation as one of the pathways for processing SCG becomes intriguing as we seek sustainable waste management solutions. The combination of both nutrition and toxic alkaloids (caffeine) makes SCG and/or other coffee parts intriguing for recycling (or upcycling) via BSF cultivation to generate insect protein. Due to its remarkable capacity to bioconvert organic waste into high-value proteins and fats, the black soldier fly, Hermetia illucens, has garnered attention in waste management and animal feed production. This comprehensive review sheds light on the recent development of using SCG as a substrate for BSF larvae.

1. Introduction

1.1. Black Soldier Fly (BSF)

BSF larvae (Hermetia illucens) consume a wide range of organic waste. With a feed assimilation rate of 1.0–1.5 g g⁻¹ day⁻¹ [1,2,3,4], BSF larvae greatly assist in the reduction of the volume of waste, ensuring a more sustainable and effective waste management strategy. BSF larvae have been identified as efficient decomposers of organic waste. Several attributes and studies strengthen the superiority of BSF larvae in reducing organic waste such as fruit and vegetable waste, manure, meat waste, etc. into high-quality protein and lipids, which can be used as feedstock for poultry, fish, or swine, presenting an economic opportunity [5] and therefore making them versatile for waste management [6].

Owing to their rapid consumption of large amounts of organic waste, BSF larvae convert waste materials into their body mass, leaving behind significantly reduced waste volume [7,8]. More interestingly, they not only significantly reduce the amount of waste but are also able to reduce pathogen counts such as Escherichia coli and Salmonella sp., making the end product safer for disposal or use as soil amendment [9]. Thus, the utilization of BSF larvae in waste management is not just a method of waste reduction but a holistic approach to waste valorization, pathogen reduction, and environmental protection. Their ability to effectively reduce and valorize organic waste underscores the need for more widespread adoption and research into the BSF lifecycle and its integration into sustainable waste management systems.

BSF larvae possess high nutritional value and are rich in proteins as well as fats and other nutrients, making them an excellent source of feed for poultry, fish, and even pets. Their high nutritional content is rooted in their unique composition, which includes proteins, lipids, and other essential micronutrients, such as proteins (around 42–63%) [10], lipids (about 15–35%) [11], essential amino acids (often comparable to those of fish meal, a standard high-quality protein source) [12], minerals (such as calcium, phosphorus, magnesium, and potassium), and several vitamins [13].

Moreover, BSF larvae also have some antimicrobial peptides (that can be beneficial for the animals consuming them, potentially improving gut health and disease resistance [14]), as well as chitin (a polysaccharide that has potential benefits such as supporting the immune system and promoting gut health in animals) [15]. The nutritional profile of BSF larvae highlights their potential as an alternative and sustainable protein source for animal feed [5]. As the global demand for animal feed continues to increase, the high nutritional content of BSF larvae, coupled with their environmental benefits, makes them a compelling option for future feed formulations.

In addition to the aforementioned excellence of BSF larvae, by consuming and degrading organic waste as well as livestock manure, BSF larvae also simultaneously bioconvert greenhouse gases, such as methane and nitrous oxide, that might be produced from unprocessed and untreated organic wastes [16,17,18]. On the other hand, animal feed, especially fishmeal and soy, is associated with high GHG emissions during its production. BSF larvae can be used as an alternative protein source, reducing the demand for such feeds [19].

As BSF larvae consume organic carbon during their growth, a significant portion of this carbon is stored in their bodies, thus serving as a form of short-term carbon sequestration [17]. Furthermore, their frass can also be utilized as a soil amendment that serves as an alternative to synthetic fertilizers associated with high GHG emissions [20]. The high lipid content in BSF larvae can be extracted and converted into biodiesel. Producing biodiesel from BSF larvae can reduce dependence on fossil fuels, thereby offsetting the associated GHG emissions [5,21]. Incorporating BSF larvae into waste management and agricultural systems can serve as a multifaceted strategy to reduce GHG emissions. From diverting waste from landfills to providing sustainable feed alternatives, the benefits of BSF are evident. Adopting such innovative solutions will be vital in the ongoing quest to combat climate change and its impactful damages.

1.2. Spent Coffee Grounds (SCG) as a Potential Organic Substrate

SCG is the byproduct remaining after the brewing process of coffee beans. Over the past years, there has been growing interest in SCG due to its potential applications in various sectors, ranging from bioenergy production to food supplementation [22] and also in nanotechnology [23,24,25,26]. SCG is rich in dietary fibers (predominantly cellulose, hemicellulose, and lignin) [27]. It also has a reasonable amount of antioxidants (chlorogenic acid, of 10.7% to 23.82%, with the yield of extracts from coffee parts (pulp, husk, silverskin, spent waste) of 11.7% to 25.0%) [28] for potential use as nutraceuticals or food supplements, and also lipids (around 8–20% of SCGs dry weight [29], as a prospective candidate for biodiesel production [30,31]). However, it should be noted that SCG, as organic waste, if left without proper treatment (such as dumped in landfills), will generate CH₄ as one of the greenhouse gases and an agent of global warming [32,33].

Furthermore, SCG is also a source of minerals, namely potassium, phosphorus, magnesium, and calcium [34], and also some antioxidants and bioactive compounds such as chlorogenic acids (a major group of polyphenolic compounds in coffee, with antioxidant, anti-inflammatory, antiviral, and antihyperglycemic activities, 4–8% of dry weight) [35], melanoidins (about 25% of dry weight, responsible for the color of roasted coffee, possess antioxidant and antimicrobial properties) [36], and especially caffeine (around 1% of SCGs dry weight) [35,37]. Given the vast amounts of SCG produced worldwide due to the popularity of coffee, understanding its composition is crucial. This knowledge not only helps divert waste from landfills but also unlocks potential sustainable applications in various industries, especially for BSF-driven bioconversion.

1.3. The Effects of Feeding SCG to BSF

BSF has emerged as a significant player in the domain of waste management and for producing high-quality animal feed [38,39,40]. By modifying the nutritional inputs [41,42,43,44] of the BSF, researchers can control the quality and yield of its larvae, which serve as protein sources. One promising nutritional input is spent coffee grounds (SCG) [45,46,47,48,49]. We aim to review the influence of SCG in BSF feed, considering the effect on growth rate, nutritional profile, waste degradation, and the potential benefits and challenges. One challenge encountered was the caffeine content in SCG. High caffeine concentrations could pose toxicity risks to BSF larvae and, subsequently, to the animals consuming them. Thus, finding the optimal ratio of SCG in the feed mix is crucial for ensuring maximum yield and nutritional quality. To the best of our knowledge, this kind of study assessing the optimum composition of SCG in the feed for BSF is not available yet.

2. Materials and Methods

This study employs a systematic literature review and is supplemented with bibliometric analysis based on the analysis from the Scopus database (https://scopus.com, accessed on 1 October 2023). It is one of the largest databases utilized for reviews and bibliometric analysis due to its vast array of abstracts and citations from a multitude of journals, conferences, and books, thoroughly curated and inspected by a Content Selection and Advisory Board [50,51]. From the Scopus web, the keyword “illucens” was inputted. The usage of this single keyword in the scientific name of BSF is practiced because there is little difference in the results obtained from inputting “illucens” and “black soldier fly” [5].

We conducted a systematic review following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement. The PRISMA diagram for this study (accessed October 2023) is shown in Figure 1. Initially, there were 1683 titles shown under the “illucens” keyword. The results were filtered for the new recent titles from the last decase (2014–2023) to 1607 titles. These titles of BSF research were further sieved down to 22 titles with relation to SCG, or coffee, or coffee-related products. Moreover, those with minimum adherence were removed, and therefore there are 18 key papers to be further discussed in this study.

In addition to the systematic literature review about the effects of SCG on the growth of BSF, this paper also employed bibliometric mapping/analysis. The aforementioned 18 core papers, along with their essential keywords (provided by the authors), were analyzed using VOSViewer software (version 1.6.17) to provide visualization and mapping of the interconnection for this research. The mapping will be very useful to the development of future research directions, either for BSF cultivation, SCG utilization, or a combination of both.

3. Results

The state-of-the-art of the effects of SCG (and/or other parts of coffee) on BSF larvae cultivation is shown in Table 1. Furthermore, the effects of SCG-fed BSF larvae as a feed for fishes are shown in Table 2. Table 1 contains 12 entries, while Table 2 has 6 entries, totaling 18 reports as a result of the PRISMA procedure stated in Figure 1.

Table 1 displays various research results conducted to optimize the rearing of BSF larvae that focus on different rearing substrates, conditions, and their effects on larval growth and development. There are several research works in Table 1, such as feeding BSF (1) directly with coffee or spent coffee ground, (2) with algae-enriched coffee or coffee silverskin, (3) with various carbohydrate or protein sources (either mixed with coffee or not), and also (4) the application of SCG-derived BSF frass. There are some mixed results from Table 1, which indeed make this kind of research exciting.

3.1. Cultivation of BSF Larvae Using SCG and/or Coffee Parts

In Table 1, Permana and coworkers et al. [52] investigated the use of SCG with 7-day-old BSF larvae. Different feeding rates are tested, namely 12.5, 25, 50, 100, and 200 mg/larvae/day. Their study concluded that the optimal feeding rate is 200 mg/larvae/day, where it leads to a development time of around 25.6 days, efficient digestion conversion of 5%, pupae biomass of 14.8 mg, growth rate of 1.41 mg/day, waste reduction index of 0.997, and pupae protein content of up to 33.45%. In other research, Ospina-Granobles and Carrejo-Gironza used the Castillo variety of Coffea arabica to feed BSF larvae [53]. From their study, it is evident that different feeding rates (100, 160, and 200 mg/larvae/day) impacted the weight reduction index, larval development time, and the efficiency of the conversion of ingested food. With 100 mg/larvae/day, the reduction percentage of coffee pulp is 62.88% (wet basis), and the efficiency of conversion of ingested food = 7.89%. For the feeding of BSF using coffee at 160 mg/larvae/day, it achieves the highest weight of 115.9 mg with the shortest average development time of 38.65 days.

Truzzi et al. [54] detailed the use of coffee silverskin enriched with Schizochytrium sp. algae. The best results are observed with a 10% inclusion rate of Schizochytrium sp., enhancing the lipid and protein content in prepupae and increasing the levels of omega-3 fatty acids. Perhaps their study is the only report of the fatty acid profile of BSF larvae reared with coffee products. Based on their results, the majority of the fatty acids (with >10 g/100 g fatty acids) of BSF larvae fed with coffee silverskin enriched with algae generally are C12:0, C16:0, C18:0, and C18:1n9 (lauric acid, palmitic acid, stearic acid, and elaidic acid (trans-9-octadecanoic acid), respectively). However, for those enriched with Schizochytrium sp., C20:5n3 and C22:6n3 emerge (eicosapentaenoic acid and docosahexanoic acid, respectively). Those enriched with Isochrysis sp. do not show any new fatty acids with a composition of >10 g/100 g fatty acids. Similar to the fatty acid profile of BSF larvae fed with coffee silverskin, those reared with a total mix diet (composed of ground corn, barley, bran, alfalfa, wheat, etc.) [55] also show C12:0 and C16:0 fatty acids (lauric acid and palmitic acid, respectively) as the dominant ones (>10 g/100 g total defatted fatty acid (TDFA)). The BSF larvae fed a total mix diet also have C14:0 (myristic acid) as the majority of fatty acids, besides C12:0 and C16:0. On the other hand, it is also detected that there are C18:1 cis-9 and C18:2n-6 fatty acids (oleic acid and linoleic acid, respectively), although the concentration is quite moderate (3.69–8.5 g/100 g TDFA). Based on the comparison of profiles of fatty acids, it can be concluded that the profiles of fatty acids of BSF larvae are varied as a function of the substrates for the rearing process.

On the other hand, Milanovic et al. [56] also used the algae-enriched coffee as the feed for BSF. The algae are Schizochytrium limacinum and Isochrysis galbana. The results indicate a high prevalence of tetracycline resistance genes and an impact on antibiotic resistance (AR) gene distribution in larvae and frass. In another study about algae-enriched coffee silverskin, Osimani et al. [57] mapped different bacterial dominances in the larvae’s microbiota and the frass. As identical algae are used (Schizochytrium limacinum and Isochrysis galbana), they present different microorganism communities. BSF reared with coffee silverskin with no algae enrichment showed the larvae’s microbiota was dominated by Paenibacillus. bacteria are still present in the S. limacinum- and I. galbana-enriched coffee silverskin, but with the presence of other genera in the larvae’s microbiota such as Enterococcus, Lysinibacillus, and Morganella (for S. limacinum-enriched silverskin) and even high abundances of Brevundimonas, Enterococcus, and Paracoccus (I. galbana-enriched silverskin). In the BSFs frass, Brevundimonas are detected for both BSF reared with algae-enriched silverskin, with the addition of Alcaligenes genera specifically for that of I. galbana-enriched coffee silverskin.

As the work by Osimani et al. [57] might be the only study of microorganism mapping of BSF reared with coffee products (coffee silverskin enriched with algae (Schizochytrium limacinum, Isochrysis galbana), it is highlighted that they have viable counts of lactic acid bacteria (Lactococcus, Lactobacillus, Enterococcus, Weissella, Leuconostoc) [57], as coffee byproducts are dominated by lactic acid bacteria according to a study by Pothakos and coworkers [58]. Furthermore, they also noted that the frass from insects is dominated by saprophytic microorganisms [57]. However, although the reports discussed in Table 1, entries 3–5, are from the same group that disclosed the details of the parameters of the BSF larvae cultivation, the weight evolution of the BSF larvae in their reports is not available. They just harvested or collected the larvae when the tegument color changed from white to black, without mentioning any specific duration.

Hadj Saadoun et al. tested several substrates (brewery-spent grains, tomato peels and seeds, cow’s milk whey, grape stalk, bread dough, and SCG) for BSF prepupae [59]. Brewery-spent grains showed the best larval performance (0.22 g/prepupae). Other larval performances are 0.19 g/prepupae (tomato peels), and 0.14 g/prepupae (cheese). However, there is no development for SCG-fed BSF larvae (they died after 15 days, or survival rate = 0%, due to the high content of indigestible fibers and caffeine as a toxic alkaloid) [60]. Moreover, the highest ratio between unsaturated and saturated fatty acids is 1.34 (cow’s milk and whey), while the lowest ratio is 0.37 (tomato peels and seeds).

Fischer et al. (Table 1, entry 7) experimented with SCG, donut dough, and a blend of SCG and dough (1:1) for BSF larvae and prepupae for 35 days, observing variations in survival, growth, and nutritional content [45]. Their best result is obtained from the feeding of BSF using SCG:donut dough 1:1, with a survival rate of 81%, with its frass containing the highest nitrogen (~4.20% dry matter (DM), compared to other feeding experiments. The result for feeding SCG:donut 1:1 is comparable to soybean meal and organic fertilizers. Feeding with sole SCG provided a survival rate of 45%, and surprisingly, that of the donut dough is much lower, with a survival rate of 24%. Although BSF larvae fed with donut dough are the longest (21.44 mm) and the largest (0.23 g), their net production is the lowest (0.60 ± 1.01 g/day/m³). On the other hand, those fed with SCG:donut 1:1 have similar length (19.12 mm) and weight (0.18 g) but a net production of 4.42 ± 1.02 g/day/m³. Based on the results, it can be concluded that the mixture of SCG and donut dough works in synergy by covering each other’s drawbacks.

Sideris et al. compared SCG, brewer’s spent grain (BSG), and a mix of both as substrates. BSG alone or in combination showed better results than SCG alone (larvae underperformed, with a very long development time = 35 days and a larval yield of <0.77 g in DM) [61]. The best result (for aspects of substrate mass reduction, protein conversion rate, and bioconversion rate) is acquired for feeding with reference feed (BΩ-321 feed, Viozois S.A., Greece) that is 67.38% in substrate mass reduction, 45.77% protein conversion rate, and 23.28% bioconversion rate, besides the fast development time of 11 days only. Although the performance is lower, the usage of SCG, BSG, and brewer’s yeast (BY) provides an alternative feed from waste by-products from food industries that will drive sustainability with comparable performance to that of the commercial feed (18.48–44.80% substrate mass reduction, 17.55–30.15 protein conversion rate, 6.25–17.22% bioconversion rate, and 8–17 days of development time).

Villa et al. (Table 1, entry 9) explored a mixture of sludge (S), brewery spent grains (BSG), coffee waste (C), and whey (W) with various compositions as a feed to BSF [46]. The mixtures affected larval development, size, and weight differently. With S:BSG:C:W = 50:10:10:30, BSF larvae are not developed (final height after 23 days = ~6 mm, final weight ≤ 10 mg). When the composition is tuned to S:BSG:C:W = 50:10:30:10 (increased portion of coffee waste), the larvae size and weight are significantly different (p-value < 0.05) when compared to the control (final height after 23 days = ~15–18 mm, final weight = 81.9 ± 5.3 mg). However, when coffee waste and waste are eliminated, leaving S:BSG = 50:50, or brewery spent grain is increased to 30%, with S:BSG:C:W = 50:30:10:10, then no significant difference is observed for larvae size and weight when compared to the control (final weight after 23 days is still between 15 and 18 mm, and final weight = ~90 mg).

Romano et al. examined the nutritional profile of BSF larvae reared for two weeks on sweet potato, SCG, or dough [47]. Each substrate affected the larve’s nutritional content and bioconversion efficiency differently. For BSF larvae fed with sweet potato and with SCG (separately), the length and weight of the larvae and prepupae are in a similar range of around 17 mm and 17 g, respectively. It is shown in Table 1, entry 10, that those fed with SCG show significantly higher crude protein (~65% dry weight), with the highest composition of palmitic acid (24.85%) and linoleic acid (23.30%) compared to those fed with sweet potato (17.45%, 12.40%, respectively) or dough (15.21%, 18.92%, respectively). It also produces the highest total amino acid content (39.49 ± 2.57%). However, those fed with sweet potatoes have the strongest growth and nutritional profile of BSF larvae. This is due to the fact that its percentage of prepupae is similar to that of those fed with SCG (in the range of 36%) and higher than that of those fed with dough (prepupae percentage of 15%). On the other hand, those with sweet potatoes also have similar larval length, larval weight, and total amino content to those fed with SCG. However, as it has the highest lauric acid content (43%) that is considered to have anti-obesity properties for mammals, BSF larvae fed with sweet potato are considered to be the best compared to those fed with SCG (lauric acid content of only 27%).

As previously mentioned, most of the innovations in the BSF feed are the enrichment of SCG or other coffee parts with algae or their combination with various wastes. However, there is only one research study about the fermented SCG for BSF feed, as reported by Kharkratoke et al. [62]. They used fermented SCG in various proportions (0–100%) mixed with fruit and vegetable pulp residue for BSF feed. With 0% fermented SCG (or purely fruit and/or vegetable pulp residue), the waste reduction efficiency and feed conversion rate are the highest among all (~90%). With 20% fermented SCG mixed with fruit and vegetable pulp residue, the BSF larvae are developed in a short period of time (~15 days), with a high survival rate (~95%), and high bioconversion efficiency (~85%). The largest prepupal size is between 20% and 40% fermented SCG (similarly at around 120 mm length and 90 mg weight). However, those of 40% fermented SCG have a low substrate reduction rate (~65%) and a long prepupation time (~21 days), compared to those of 20% fermented SCG (~85% substrate reduction rate and a short prepupation time of 15 days). As the composition of fermented SCG is prolonged between 60–80%, the development time is getting longer to fall between 25–35 days, with a passable substrate reduction time of 55–68%. It is then worsened when BSF larvae are fed with 100% fermented SCG, as indicated by longer development times (45–53 days), a reduced larval survival rate (65%), and a substrate reduction rate (~30%).

An interesting result is reported in Table 1 by Horgan et al. [37]. They studied the effects of incorporating control SCG (aged < 1 months), aged SCG (7 and 14 months), and SCG-derived BSF frass into soil or 1 cm on soil on the growth of radish and tomato, while assessing their repellency to slug herbivory (Arion atar, Deroceras laeve, Derocerus reticulatum, and Lehmannia marginata). Fresh SCG inhibited plant growth while simultaneously reducing slug herbivory (radish plant height ~9 cm, radish leaf consumed by slug < 5%, tomato plant height ~7 cm, area of tomato leaf consumed by SCG < 1 mm²). In addition, SCG-derived BSF frass mixed in the soil or on top of the soil resulted in declined plant growth, yellowing, and reduced height (radish plant height ~5 cm, tomato plant height 2.5 cm, where there was no further exploration for leaf consumption by slug). The 14-month-old SCG promoted plant growth with no repellency effect on slugs (radish plant height 13 cm, radish leaf consumed by slug 10–80%, tomato plant height 15 cm, area of tomato leaf consumed by SCG 10–35 mm²). The best result is achieved when 7-month-old SCG is applied, where plant growth is promoted while simultaneously reducing slug herbivory (radish plant height 10 cm, radish leaf consumed by slug < 5%, tomato plant height 8 cm, area of tomato leaf consumed by SCG < 3 mm²).

Related to the interesting effect of frass in the study by Horgan [37], BSF larvae frass is also stated as a biologically unstable soil amendment [63], which is a result of the rapid composting process in the presence of phytotoxic substances. In order to be suitable as a soil amendment, the BSF larvae frass have to be stabilized via post-treatment, for instance, thermophilic composting [63]. Ammonium nitrogen (NH₄⁺-N) is highly suggested as the main driver of the phytotoxicity [64] in frass. This might be the reason why frass, as an organic excrement of BSF larvae, showed a negative effect on plant growth in the study by Horgan and coworkers [37].

Table 1. Compilation of the existing research of cultivation of BSF by using SCG as a feed component.

No.	Name of Rearing Substrate	Rearing Conditions	Results	Reference
1.	SCG	BSF larvae, 7 days old, feeding rate of 200, 100, 50, 25, and 12.5 mg/larvae/day	Best results for feeding with 200 mg/larvae/day − Development Time: 25.6 ± 2.19 days − Efficiency of digestion conversion: 5 ± 0.49% − Pupae Biomass: 14.8 ± 2.15 mg − Growth Rate: 1.41 ± 0.17 mg/day − Waste reduction index: 0.997 ± 0.11 − Pupae Protein Content: Up to 33.45%	[52]
2.	Coffea arabica (Castillo variety (0.5% caffeine))	BSF larvae, 100 mg/larvae/day	Reduction percentage of coffee pulp = 62.88% (wet basis) Efficiency of conversion of ingested food: 7.89%	[53]
		BSF larvae, 160 mg/larvae/day	Highest weight reduction index (wet basis) is 0.85%
		BSF larvae, 200 mg/larvae/day	Highest weight = 115.9 mg. Shortest average development time = 38.65 days.
3.	Coffee silverskin (100%)	BSF larvae of 6 days old, in 9 groups × 5 replicates × 150 larvae = 6750 larvae. Feeding rate = 100 mg/day. Chamber temperature = 27 ± 1 °C, relative humidity (RH) = 65 ± 5%, 24 h darkness in plastic boxes 28 × 19 × 14 cm3. Note: Weight evolution of BSF larvae is not available	Best inclusion rate = Schizochytrium sp. 10%. The prepupae of BSF show increased lipid and protein content in prepupae, and high amounts of unsaturated fatty acids, especially omega-3. There is no information on the weight evolution of BSF. The BSF larvae were harvested when the tegument color changed from white to black.	[54]
	Coffee silverskin with algae (Schizochytrium sp., 0, 5, 10, 20, 25%)
	Coffee silverskin with algae (Isochrysis galbana, 0, 5, 10, 20, 25%)
4.	Coffee silverskin (100%)	BSF larvae of 6 days old, in 9 groups × 5 replicates × 150 larvae = 6750 larvae. Feeding rate = 100 mg/day. Note: Weight evolution of BSF larvae is not available	High prevalence of tetracycline resistance genes. No significant effect on AR gene distribution in larvae.	[56]
	Coffee silverskin enriched with Schizochytrium limacinum, (5, 10, 20, 25%)
	Coffee silverskin with Isochrysis galbana (5, 10, 20, 25%)		High prevalence of tetracycline resistance genes. Significant accumulation of AR genes in frass samples, especially at high percentages (>20%) of I. galbana.
5.	Coffee silverskin (100%)	BSF larvae of 6 days old, in 9 groups × 5 replicates × 150 larvae = 6750 larvae. Feeding rate = 100 mg/day. Chamber temperature = 27 ± 1 °C, 65 ± 5% RH, 24 h dark photoperiod, in plastic boxes 28 × 19 × 14 cm3. Note: Weight evolution of BSF larvae is not available	Dominance of Paenibacillus in the larvae’s microbiota	[57]
	Coffee silverskin enriched with Schizochytrium limacinum, (5, 10, 20, 25%)		Presence of Enterococcus, Lysinibacillus, Morganella, and Paenibacillus in the larvae’s microbiota. Dominance of Brevundimonas and Alcaligenes in frass.
	Coffee silverskin with Isochrysis galbana, (5, 10, 20, 25%)		High relative abundances of Brevundimonas, Enterococcus, Paracoccus, and Paenibacillus in larvae. Predominance of Brevundimonas in frass.
6.	Brewery spent grains, tomato peels and seeds, cows’ milk, whey, grape stalks, bread dough, and SCG.	Chamber (32.5 × 32.5 × 32.5 cm3) temperature = 27 ± 0.5 °C, 60–70% RH, with light:dark = 16:8 h, with 400–500 larvae per chamber.	− Best larval performance at 0.22 g/prepupae (beer), 0.19 g/prepupae (tomato peels), and 0.14 g/prepupae (cheese). − No development for SCG-fed BSF larvae (died after 15 days, survival rate = 0%). − Highest ratio between unsaturated and saturated fatty acids at 1.34 (cow’s milk and whey), while the lowest ratio is 0.37 (tomato peels and seeds).	[59]
7.	SCG	BSF larvae and prepupae fed for 35 days. Feeding of 6.8 kg feed in container 0.9 × 1.2 × 1.5 m3.	Survival: 45%. Longer and heavier BSFP from dough. Fatty acids higher in BSFL. Frass: Higher potassium (~1.00% dry matter (DM)), lowest phosphorus (<0.30% DM), moderate nitrogen content (~3.25% DM) Larval length = 16.86 ± 0.29 mm Larval weight = 0.11 ± 0.01 g Net production = 0.75 ± 0.58 g/day/m3	[45]
	Donut dough		Survival: 24%. Longer and heavier BSFP from dough. Lowest nitrogen content (~2.75% DM), lowest potassium (<0.25% DM), lowest calcium (<0.1% DM). Higher amino acid composition in BSFL. Larval length = 21.44 ± 0.59 mm Larval weight = 0.23 ± 0.01 g Net production = 0.60 ± 1.01 g/day/m3
	Blend (coffee and dough, 1:1)		Survival: 81%. Stage and food affected protein, lipid, glycogen content. Frass: Highest nitrogen (~4.20% DM). Comparable to soybean meal and organic fertilizers. Larval length = 19.12 ± 0.72 mm Larval weight = 0.18 ± 0.01 g Net production = 4.42 ± 1.02 g/day/m3
8.	SCG	BSF rearing with controlled climate chamber (14.5 × 9.5 × 9.5 cm3, 30 °C, 70% RH, with 24 h dark photoperiod. Total amount of feed per larva = 240 mg in DM. Variation: 200 and 300 larvae per container (1.45 and 2.17 larvae per cm2, respectively.	Larvae underperformed. Development time = 35 days. Larval yield 0.61–0.77 g in DM.	[61]
	Brewer’s spent grain (BSG)		Better results than those solely reared with SCG. Development time = 9 days. Larval yield 6.02–8.53 g in DM (for 200 and 300 larvae per container, respectively).
	SCG and/or BSG and/or brewers’ yeast (BY)		Acceptable values in substrate mass reduction (18.48–44.80%, SCG + BY and BSG + BY, respectively), protein conversion rate (17.55–30.15%, SCG + BY and BSG + BY, respectively), and bioconversion rate (6.25–17.22%, SCG + BY and BSG + BY, respectively). Development time = 8–17 days (for BSG + BY, and SCG + BY, respectively). Larval yields 2.99–12.72 g in DM (for SCG + BY 200 and BSG + BY 300, respectively). For SCG + BSG + BY, the development time is 12 days, with larval yield of 6.93–10.53 g in DM (for 200 and 300 larvae, respectively).
	Reference feed (layer feed BΩ-321 (Viozois S.A., Athens, Greece))		Highest values in substrate mass reduction (67.38%), protein conversion rate (45.77%), and bioconversion rate (23.28%) among all feeds. Development time = 11 days. Larval yield 11.32–16.78 g in DM (for 200 and 300 larvae, respectively).
9.	Mixture of sludge-containing media (S), with brewery spent grains (BSG), coffee waste (C), and whey (W).	Fed to BSF with composition of S:BSG:C:W = 50:10:10:30, reared for 23 days.	Larvae did not complete their development, with very poor performance of: Final height = ~6 mm Final weight ≤ 10 mg	[46]
		Control (feed from Entocycle.com, with unknown composition)	Final height = ~15–18 mm Final weight = 94.5 ± 7.2 mg
		S: BSG:C:W = 50:10:30:10	Final height = ~15–18 mm Final weight = 81.9 ± 5.3 mg
		S: BSG:C:W = 50:50:0:0	Final height = ~15–18 mm Final weight = 91.0 ± 0.1 mg
		S: BSG:C:W = 50:30:10:10	Final height = ~15–18 mm Final weight = 84.0 ± 6.0 mg
10.	Sweet potato, 2 weeks	BSF larvae cultivated for 2 weeks. Temperature controlled room of 3.6 × 3.6 m2, 30 °C, 60–64% RH.	− Material reduction = 29.9 ± 1.3% − Percentage of prepupae = 36.4 ± 5.6% − Survival rate = 87.0 ± 5.6% − Length (larvae, prepupae) = ~16.8 mm, ~17.6 mm − Weight (larvae, prepupae) = ~16.9 mg, ~17.5 mg − Highest percentage (~43%) of lauric acid (C12) − Supported growth and best nutritional profile of BSF larvae − High total amino acid content (38.33 ± 2.39%)	[47]
	SCG, 2 weeks		− Material reduction = 63.4 ± 3.3% − Percentage of prepupae = 36.5 ± 5.8% − Survival rate = 98.6 ± 1.3% − Length (larvae, prepupae) = ~16.7 mm, ~17.4 mm − Weight (larvae, prepupae) = ~16.8 mg, ~17.2 mg − Significantly higher crude protein than the other diets (~65% dry weight, while others are ~40%) − Highest composition of C16:0 (palmitic acid, 24.85%) and C18:2n-6 (linoleic acid, 23.30%) compared to those fed with sweet potato (17.45%, 12.40%, respectively) or dough (15.21%, 18.92%, respectively). − Highest total amino acid content (39.49 ± 2.57%)
	Dough, 2 weeks		− Material reduction = 92.6 ± 12.2% (best material reduction) − Percentage of prepupae = 15.1 ± 1.2% (lowest percentage of prepupae among sweet potatoes and dough). − Survival rate = 83.3 ± 2.9% − Length (larvae, prepupae) = ~18.5 mm, ~19.5 mm (significantly larger/heavier BSF larvae). − Weight (larvae, prepupae) = ~18.5 mg, ~19.5 mg − Lowest total amino acid content (30.33 ± 0.18%)
11.	Fruit and vegetable pulp residue (apple 12%, pineapple 12%, carrot 25%, tomato 44%, guava 5%, beetroot 1.5%, celery 0.5%) mixed with 0% fermented SCG	Larvae kept in plastic containers with diameter 24.5 cm × height 12.5 cm, with 28–34 °C, 70–90% RH, light:dark = 13 h: 11 h. Feeding rate = 200 mg/larvae/day.	− Survival rate = ~85% − Duration of prepupation = ~10 days − Weight (larvae, prepupae) = 121 mg, 64 mg − Substrate reduction rate = ~90% − Highest waste reduction efficiency and feed conversion rate, similar to 20% fermented SCG. Served as the control.	[62]
	Pulp with 20% fermented SCG		− Survival rate = ~95% − Duration of prepupation = ~15 days − Weight (larvae, prepupae) = 116 mg, 90 mg − Substrate reduction rate = ~85% − Short rearing time, high survival rate, and high substrate reduction rate. Supported the largest prepupae size. − Recommended for rearing BSF larvae.
	Pulp with 40% fermented SCG		− Survival rate = ~92% − Duration of prepupation = ~21 days − Weight (larvae, prepupae) = 136 mg, 91 mg − Substrate reduction rate = ~65% − Largest prepupae size, high survival rate, but with long prepupation duration and not optimum reduction rate.
	Pulp with 60% fermented SCG		− Duration of prepupation = 25–35 days − Weight (larvae, prepupae) = 139 mg, 81 mg − Substrate reduction rate = ~68% − Large prepupae size, passable reduction rate, but long prepupation duration.
	Pulp with 80% fermented SCG		− Survival rate = ~80% − Duration of prepupation = 30–35 days (long development time) − Weight (larvae, prepupae) = 102 mg, 79 mg − Substrate reduction rate = ~55%
	Pulp with 100% fermented SCG		− Survival rate = ~65% − Duration of prepupation = 45–53 days − Weight (larvae, prepupae) = 117 mg, 74 mg − Substrate reduction rate = ~30% − Very long development time, low rate of substrate reduction, lightest prepupae weight.
12.	Fresh SCG (aged < 1 month, 50% water, incorporated into soil)	BSF larvae grown in the first chamber (275 × 250 × 210 cm3, 25–28 °C, 60% RH) for 3–5 days. After that, they will be grown in the second chamber (275 × 80 × 250 cm3, 28 ± 1.5 °C, 40% RH, 24 h dark photoperiod) for 12 days. Growing of radish and tomato = 30 days	Inhibited plant growth (radish and tomato, 30 days) and development; reduced slug herbivory (Arion atar, Deroceras laeve, Derocerus reticulatum, and Lehmannia marginata). Height of radish plant = ~9 cm Radish leaf consumed by slug ≤ 5% Height of tomato plant = ~7 cm Area of tomato leaf consumed by slug (SCG mixed with soil or layered on top of the soil) = 0 mm2, <1 mm2	[37]
	SCG (aged 7 months, 1 cm top dressing)		Promoted growth, while simultaneously reduced slug herbivory through repellent and host quality effects. Height of radish plant = ~10 cm Radish leaf consumed by slug ≤ 5% Height of tomato plant = ~8 cm Area of tomato leaf consumed by slug (SCG mixed with soil or layered on top of the soil) = 0 mm2, <3 mm2
	SCG (aged 14 months, incorporated into soil)		Promoted plant growth, while having no effect on slug herbivory. Height of radish plant = ~13 cm Radish leaf consumed by slug (SCG mixed with soil, or layered on top of the soil) = 10–80% Height of tomato plant = ~15 cm Area of tomato leaf consumed by slug (SCG mixed with soil or layered on top of the soil) = 10 mm2, 35 mm2
	SCG-derived BSF frass (incorporated into soil, or 1 cm top dressing)		Reduced development of plants, yellowing, reduced height. Height of radish plant = ~5 cm Radish leaf consumed by slug (SCG mixed with soil or layered on top of the soil) = not available Height of tomato plant = ~2.5 cm Area of tomato leaf consumed by slug (SCG mixed with soil or layered on top of the soil) = not available

Table 1. Compilation of the existing research of cultivation of BSF by using SCG as a feed component.

No.	Name of Rearing Substrate	Rearing Conditions	Results	Reference
1.	SCG	BSF larvae, 7 days old, feeding rate of 200, 100, 50, 25, and 12.5 mg/larvae/day	Best results for feeding with 200 mg/larvae/day − Development Time: 25.6 ± 2.19 days − Efficiency of digestion conversion: 5 ± 0.49% − Pupae Biomass: 14.8 ± 2.15 mg − Growth Rate: 1.41 ± 0.17 mg/day − Waste reduction index: 0.997 ± 0.11 − Pupae Protein Content: Up to 33.45%	[52]
2.	Coffea arabica (Castillo variety (0.5% caffeine))	BSF larvae, 100 mg/larvae/day	Reduction percentage of coffee pulp = 62.88% (wet basis) Efficiency of conversion of ingested food: 7.89%	[53]
		BSF larvae, 160 mg/larvae/day	Highest weight reduction index (wet basis) is 0.85%
		BSF larvae, 200 mg/larvae/day	Highest weight = 115.9 mg. Shortest average development time = 38.65 days.
3.	Coffee silverskin (100%)	BSF larvae of 6 days old, in 9 groups × 5 replicates × 150 larvae = 6750 larvae. Feeding rate = 100 mg/day. Chamber temperature = 27 ± 1 °C, relative humidity (RH) = 65 ± 5%, 24 h darkness in plastic boxes 28 × 19 × 14 cm3. Note: Weight evolution of BSF larvae is not available	Best inclusion rate = Schizochytrium sp. 10%. The prepupae of BSF show increased lipid and protein content in prepupae, and high amounts of unsaturated fatty acids, especially omega-3. There is no information on the weight evolution of BSF. The BSF larvae were harvested when the tegument color changed from white to black.	[54]
	Coffee silverskin with algae (Schizochytrium sp., 0, 5, 10, 20, 25%)
	Coffee silverskin with algae (Isochrysis galbana, 0, 5, 10, 20, 25%)
4.	Coffee silverskin (100%)	BSF larvae of 6 days old, in 9 groups × 5 replicates × 150 larvae = 6750 larvae. Feeding rate = 100 mg/day. Note: Weight evolution of BSF larvae is not available	High prevalence of tetracycline resistance genes. No significant effect on AR gene distribution in larvae.	[56]
	Coffee silverskin enriched with Schizochytrium limacinum, (5, 10, 20, 25%)
	Coffee silverskin with Isochrysis galbana (5, 10, 20, 25%)		High prevalence of tetracycline resistance genes. Significant accumulation of AR genes in frass samples, especially at high percentages (>20%) of I. galbana.
5.	Coffee silverskin (100%)	BSF larvae of 6 days old, in 9 groups × 5 replicates × 150 larvae = 6750 larvae. Feeding rate = 100 mg/day. Chamber temperature = 27 ± 1 °C, 65 ± 5% RH, 24 h dark photoperiod, in plastic boxes 28 × 19 × 14 cm3. Note: Weight evolution of BSF larvae is not available	Dominance of Paenibacillus in the larvae’s microbiota	[57]
	Coffee silverskin enriched with Schizochytrium limacinum, (5, 10, 20, 25%)		Presence of Enterococcus, Lysinibacillus, Morganella, and Paenibacillus in the larvae’s microbiota. Dominance of Brevundimonas and Alcaligenes in frass.
	Coffee silverskin with Isochrysis galbana, (5, 10, 20, 25%)		High relative abundances of Brevundimonas, Enterococcus, Paracoccus, and Paenibacillus in larvae. Predominance of Brevundimonas in frass.
6.	Brewery spent grains, tomato peels and seeds, cows’ milk, whey, grape stalks, bread dough, and SCG.	Chamber (32.5 × 32.5 × 32.5 cm3) temperature = 27 ± 0.5 °C, 60–70% RH, with light:dark = 16:8 h, with 400–500 larvae per chamber.	− Best larval performance at 0.22 g/prepupae (beer), 0.19 g/prepupae (tomato peels), and 0.14 g/prepupae (cheese). − No development for SCG-fed BSF larvae (died after 15 days, survival rate = 0%). − Highest ratio between unsaturated and saturated fatty acids at 1.34 (cow’s milk and whey), while the lowest ratio is 0.37 (tomato peels and seeds).	[59]
7.	SCG	BSF larvae and prepupae fed for 35 days. Feeding of 6.8 kg feed in container 0.9 × 1.2 × 1.5 m3.	Survival: 45%. Longer and heavier BSFP from dough. Fatty acids higher in BSFL. Frass: Higher potassium (~1.00% dry matter (DM)), lowest phosphorus (<0.30% DM), moderate nitrogen content (~3.25% DM) Larval length = 16.86 ± 0.29 mm Larval weight = 0.11 ± 0.01 g Net production = 0.75 ± 0.58 g/day/m3	[45]
	Donut dough		Survival: 24%. Longer and heavier BSFP from dough. Lowest nitrogen content (~2.75% DM), lowest potassium (<0.25% DM), lowest calcium (<0.1% DM). Higher amino acid composition in BSFL. Larval length = 21.44 ± 0.59 mm Larval weight = 0.23 ± 0.01 g Net production = 0.60 ± 1.01 g/day/m3
	Blend (coffee and dough, 1:1)		Survival: 81%. Stage and food affected protein, lipid, glycogen content. Frass: Highest nitrogen (~4.20% DM). Comparable to soybean meal and organic fertilizers. Larval length = 19.12 ± 0.72 mm Larval weight = 0.18 ± 0.01 g Net production = 4.42 ± 1.02 g/day/m3
8.	SCG	BSF rearing with controlled climate chamber (14.5 × 9.5 × 9.5 cm3, 30 °C, 70% RH, with 24 h dark photoperiod. Total amount of feed per larva = 240 mg in DM. Variation: 200 and 300 larvae per container (1.45 and 2.17 larvae per cm2, respectively.	Larvae underperformed. Development time = 35 days. Larval yield 0.61–0.77 g in DM.	[61]
	Brewer’s spent grain (BSG)		Better results than those solely reared with SCG. Development time = 9 days. Larval yield 6.02–8.53 g in DM (for 200 and 300 larvae per container, respectively).
	SCG and/or BSG and/or brewers’ yeast (BY)		Acceptable values in substrate mass reduction (18.48–44.80%, SCG + BY and BSG + BY, respectively), protein conversion rate (17.55–30.15%, SCG + BY and BSG + BY, respectively), and bioconversion rate (6.25–17.22%, SCG + BY and BSG + BY, respectively). Development time = 8–17 days (for BSG + BY, and SCG + BY, respectively). Larval yields 2.99–12.72 g in DM (for SCG + BY 200 and BSG + BY 300, respectively). For SCG + BSG + BY, the development time is 12 days, with larval yield of 6.93–10.53 g in DM (for 200 and 300 larvae, respectively).
	Reference feed (layer feed BΩ-321 (Viozois S.A., Athens, Greece))		Highest values in substrate mass reduction (67.38%), protein conversion rate (45.77%), and bioconversion rate (23.28%) among all feeds. Development time = 11 days. Larval yield 11.32–16.78 g in DM (for 200 and 300 larvae, respectively).
9.	Mixture of sludge-containing media (S), with brewery spent grains (BSG), coffee waste (C), and whey (W).	Fed to BSF with composition of S:BSG:C:W = 50:10:10:30, reared for 23 days.	Larvae did not complete their development, with very poor performance of: Final height = ~6 mm Final weight ≤ 10 mg	[46]
		Control (feed from Entocycle.com, with unknown composition)	Final height = ~15–18 mm Final weight = 94.5 ± 7.2 mg
		S: BSG:C:W = 50:10:30:10	Final height = ~15–18 mm Final weight = 81.9 ± 5.3 mg
		S: BSG:C:W = 50:50:0:0	Final height = ~15–18 mm Final weight = 91.0 ± 0.1 mg
		S: BSG:C:W = 50:30:10:10	Final height = ~15–18 mm Final weight = 84.0 ± 6.0 mg
10.	Sweet potato, 2 weeks	BSF larvae cultivated for 2 weeks. Temperature controlled room of 3.6 × 3.6 m2, 30 °C, 60–64% RH.	− Material reduction = 29.9 ± 1.3% − Percentage of prepupae = 36.4 ± 5.6% − Survival rate = 87.0 ± 5.6% − Length (larvae, prepupae) = ~16.8 mm, ~17.6 mm − Weight (larvae, prepupae) = ~16.9 mg, ~17.5 mg − Highest percentage (~43%) of lauric acid (C12) − Supported growth and best nutritional profile of BSF larvae − High total amino acid content (38.33 ± 2.39%)	[47]
	SCG, 2 weeks		− Material reduction = 63.4 ± 3.3% − Percentage of prepupae = 36.5 ± 5.8% − Survival rate = 98.6 ± 1.3% − Length (larvae, prepupae) = ~16.7 mm, ~17.4 mm − Weight (larvae, prepupae) = ~16.8 mg, ~17.2 mg − Significantly higher crude protein than the other diets (~65% dry weight, while others are ~40%) − Highest composition of C16:0 (palmitic acid, 24.85%) and C18:2n-6 (linoleic acid, 23.30%) compared to those fed with sweet potato (17.45%, 12.40%, respectively) or dough (15.21%, 18.92%, respectively). − Highest total amino acid content (39.49 ± 2.57%)
	Dough, 2 weeks		− Material reduction = 92.6 ± 12.2% (best material reduction) − Percentage of prepupae = 15.1 ± 1.2% (lowest percentage of prepupae among sweet potatoes and dough). − Survival rate = 83.3 ± 2.9% − Length (larvae, prepupae) = ~18.5 mm, ~19.5 mm (significantly larger/heavier BSF larvae). − Weight (larvae, prepupae) = ~18.5 mg, ~19.5 mg − Lowest total amino acid content (30.33 ± 0.18%)
11.	Fruit and vegetable pulp residue (apple 12%, pineapple 12%, carrot 25%, tomato 44%, guava 5%, beetroot 1.5%, celery 0.5%) mixed with 0% fermented SCG	Larvae kept in plastic containers with diameter 24.5 cm × height 12.5 cm, with 28–34 °C, 70–90% RH, light:dark = 13 h: 11 h. Feeding rate = 200 mg/larvae/day.	− Survival rate = ~85% − Duration of prepupation = ~10 days − Weight (larvae, prepupae) = 121 mg, 64 mg − Substrate reduction rate = ~90% − Highest waste reduction efficiency and feed conversion rate, similar to 20% fermented SCG. Served as the control.	[62]
	Pulp with 20% fermented SCG		− Survival rate = ~95% − Duration of prepupation = ~15 days − Weight (larvae, prepupae) = 116 mg, 90 mg − Substrate reduction rate = ~85% − Short rearing time, high survival rate, and high substrate reduction rate. Supported the largest prepupae size. − Recommended for rearing BSF larvae.
	Pulp with 40% fermented SCG		− Survival rate = ~92% − Duration of prepupation = ~21 days − Weight (larvae, prepupae) = 136 mg, 91 mg − Substrate reduction rate = ~65% − Largest prepupae size, high survival rate, but with long prepupation duration and not optimum reduction rate.
	Pulp with 60% fermented SCG		− Duration of prepupation = 25–35 days − Weight (larvae, prepupae) = 139 mg, 81 mg − Substrate reduction rate = ~68% − Large prepupae size, passable reduction rate, but long prepupation duration.
	Pulp with 80% fermented SCG		− Survival rate = ~80% − Duration of prepupation = 30–35 days (long development time) − Weight (larvae, prepupae) = 102 mg, 79 mg − Substrate reduction rate = ~55%
	Pulp with 100% fermented SCG		− Survival rate = ~65% − Duration of prepupation = 45–53 days − Weight (larvae, prepupae) = 117 mg, 74 mg − Substrate reduction rate = ~30% − Very long development time, low rate of substrate reduction, lightest prepupae weight.
12.	Fresh SCG (aged < 1 month, 50% water, incorporated into soil)	BSF larvae grown in the first chamber (275 × 250 × 210 cm3, 25–28 °C, 60% RH) for 3–5 days. After that, they will be grown in the second chamber (275 × 80 × 250 cm3, 28 ± 1.5 °C, 40% RH, 24 h dark photoperiod) for 12 days. Growing of radish and tomato = 30 days	Inhibited plant growth (radish and tomato, 30 days) and development; reduced slug herbivory (Arion atar, Deroceras laeve, Derocerus reticulatum, and Lehmannia marginata). Height of radish plant = ~9 cm Radish leaf consumed by slug ≤ 5% Height of tomato plant = ~7 cm Area of tomato leaf consumed by slug (SCG mixed with soil or layered on top of the soil) = 0 mm2, <1 mm2	[37]
	SCG (aged 7 months, 1 cm top dressing)		Promoted growth, while simultaneously reduced slug herbivory through repellent and host quality effects. Height of radish plant = ~10 cm Radish leaf consumed by slug ≤ 5% Height of tomato plant = ~8 cm Area of tomato leaf consumed by slug (SCG mixed with soil or layered on top of the soil) = 0 mm2, <3 mm2
	SCG (aged 14 months, incorporated into soil)		Promoted plant growth, while having no effect on slug herbivory. Height of radish plant = ~13 cm Radish leaf consumed by slug (SCG mixed with soil, or layered on top of the soil) = 10–80% Height of tomato plant = ~15 cm Area of tomato leaf consumed by slug (SCG mixed with soil or layered on top of the soil) = 10 mm2, 35 mm2
	SCG-derived BSF frass (incorporated into soil, or 1 cm top dressing)		Reduced development of plants, yellowing, reduced height. Height of radish plant = ~5 cm Radish leaf consumed by slug (SCG mixed with soil or layered on top of the soil) = not available Height of tomato plant = ~2.5 cm Area of tomato leaf consumed by slug (SCG mixed with soil or layered on top of the soil) = not available

3.2. Utilization of Coffee-Reared BSF Larvae in Fisheries

To explore the impacts of SCG on the growth of BSF larvae as a sustainable fish feed, Table 2 tabulates the particularly recent developments. Similar to Table 1, in Table 2, there is some leading research on the use of (1) coffee silverskin enriched with algae (Schizochytrium sp.) and (2) a mixture of SCG with other sources of nutrients (carbohydrate, protein, fibers). Those various feeds are then utilized to grow BSF larvae that will be further consumed by zebrafish (Danio rerio) or rainbow trout fish (Oncorhynchus mykiss). The effects observed in the fish fed with SCG-derived BSF larvae are detailed as follows:

Zarantoniello et al. [65] explored the use of coffee silverskin enriched with 10% Schizochytrium sp. algae to rear BSF larvae. The coffee silverskin-based BSF larvae are then used as a substitution for the zebrafish (Danio rerio) meal at various ratios. At 0% and 25% substitution rates of fish meal using coffee silverskin-based BSF larvae, the zebrafish show no significant change in their responses. This trend is continued up to the substitution level of 50%, which is the most balanced rate (in terms of fish growth and sustainability). Therefore, we can conclude that (to some extent) the BSF-based replacements provide comparable performance to the control fish meal diet. However, at higher levels of meal substitution (75 and 100%), negative effects are detected, such as severe hepatic steatosis, microbiota modification, increased lipid content, elevated stress, and immune responses. Based on the aforementioned results, their study demonstrates the potential of coffee silverskin-based BSF larvae as a promising partial substitution for fish meal, although there are some limits at high substitution levels.

On yet another use of coffee silverskin enriched with Schizochytrium sp. microalgae for rearing BSF larvae, Milanović et al. explored the dynamic profile of the antibiotic resistance (AR) genes in zebrafishes that are fed with them [66]. The study employed quantitative Polymerase Chain Reaction (qPCR) to assess the detection of various AR genes. It is shown by the researchers that genes like erm(B), tet(K), tet(M), tet(O), and tet(S) are present. On the other hand, mecA, vanA, vanB, and aac-aph genes are not detected. Amusingly, in zebrafish (at both juvenile and reproductive stages), the AR genes such as erm(A), erm(C), vanB, and aac-aph are never detected, whereas erm(B), tet(M), and tet(S) are widespread.

Rodrigues et al. investigated the use of fish discards and coffee silverskin enriched with Schizochytrium sp. for rearing BSF larvae [67]. It was found that those substrates significantly improved the lipid profile of BSF larvae, enhancing the content of omega-3 fatty acids, which is crucial nutrition for fish health (and also human health). Upon using fish discards, there is approximately a 40% improvement in the lipid profile and essential fatty acid profile. In addition, the practice of combining fish discards with coffee silverskin enriched with Schizochytrium sp. leads to high levels of eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) detection in BSF larvae.

Chemello et al. assessed the physiological responses of zebrafish fed with BSF larvae reared on coffee silverskin enriched with 10% Schizochytrium sp. algae [48]. They were then used as a substitute for fish meal at different levels (0, 20, 50, 75, and 100%). At lower replacement levels (0, 20, and 50%), there are no physiological issues observed in the zebrafish, which is an indication that the larvae are a viable component of the diet. However, at higher substitution levels (75 and 100%), there are significant impacts on fish stress response, oocyte maturation stages, spawning, and hatching success. This study provides critical insights into the feasibility of using BSF larvae as a fish meal substitute, highlighting the importance of moderation in substitution levels to avoid adverse effects on fish health.

The study by Osimani et al. explored the effects of feeding zebrafish with BSF larvae and BSF frass reared on coffee by- products [68]. Variability in viable bacterial counts based on the substrate used are shown in the zebrafish. When they are fed with larvae reared on coffee by-products, Danio rerio exhibited a higher occurrence of Lactobacillaceae and Leuconostoccaceae, low bacterial richness and evenness, and a higher abundance of Clostridia, influenced by bioactive compounds from the coffee by-products. As an interesting finding, the core fish microbiota remained stable despite these changes. On the other hand, the zebrafishes fed with larvae that are reared on a mixture of vegetables showed the highest bacterial richness and evenness in larvae and frass. They also showed higher abundance of Enterobacteriaceae, as well as a stable core microbiota.

In a recent study by Ratti et al., Oncorhynchus mykiss (rainbow trout) were fed with different proportions of BSF meal for six weeks [49]. The control group receives a regular BSF meal, while the test groups are fed 3% and 20% BSF prepupae meals. The findings reveal that the fishes accept the BSF-based diet well, with no adverse effects on fish growth, gut and liver health, or marketable characteristics. Interestingly, the group fed with 20% BSF prepupae meal demonstrated an increase in immuno-related gene expression, with a slight reduction in fillet redness and yellowness.

Table 2. Recent studies on the effects of coffee-reared BSF larvae as feed for fishe.

No.	Name of Rearing Substrate	Rearing Conditions	Produced BSF Fed to	Results	Reference
1.	BSF reared on coffee silverskin enriched with 10% Schizochytrium sp.	BSF as substitution of fish meal (0, 25, 50, and 75%)	Zebrafish (Danio rerio)	At 0% (baseline) and 25%, zebrafishes show standard responses based on the control diet. The 50% substitution gives the best compromise between sustainability and proper fish growth. However, at 75% and 100% substitution, severe hepatic steatosis was observed, along with microbiota modification, increased lipid content, fatty acid modification, and higher expression of stress and immune response markers.	[65]
2.	BSF reared on coffee silverskin with 10% Schizochytrium sp. microalgae	BSF as substitution of fish meal (0, 25, 50, 75, and 100%) for 6 months	Zebrafish (Danio rerio)	This study employed qPCR to assess the dynamics of antibiotic resistance (AR) genes in fish feed, including those with insect meal ingredients. Resistant genes studied: macrolide-lincosamide-streptogramin B (MLSB) [erm(A), erm(B), erm(C)], vancomycin (vanA, vanB), tetracyclines [tet(M), tet(O), tet(S), tet(K)], β-lactams (mecA, blaZ), and aminoglycosides [aac-aph]. Findings in diet samples: Detected: erm(B), tet(K), tet(M), tet(O), and tet(S). Not Detected: mecA, vanA, vanB, and aac-aph. Findings in zebrafish (juvenile and reproductive stages): Never Detected: erm(A), erm(C), vanB, and aac-aph. Widespread: erm(B), tet(M), and tet(S).	[66]
		0% BSF larvae		erm(A), erm(C), vanB, aac-aph not detected in zebrafish at any stage.
3.	Marine-based substrates		Zebrafish	− Significantly improves the lipid profile of BSF larvae. − Enhanced omega-3 fatty acids profile.	[67]
	Fish discards			− Improvement of approximately 40% in the lipid profile. − Increase in essential fatty acids.
	Fish discards with coffee silverskin with Schyzochytrium sp.			− High levels of EPA and DHA recorded. − Still reliant on marine-based bioresources
	Coffee silverskin enriched with 10% of Schizochytrium sp.	100% fish meal replacement		Affected fish stress response, oocytes maturation stages, spawning, and hatching success.
4.	Coffee silverskin enriched with 10% of Schizochytrium sp.	0% fish meal replacement	Zebrafish	No impairment observed in zebrafish physiological responses	[48]
		20% fish meal replacement
		50% fish meal replacement
		75% fish meal replacement		Affected fish stress response, oocytes maturation stages, spawning, and hatching success.
		100% fish meal replacement
5.	Coffee by-products	BSF larvae and frass	Zebrafish (Danio rerio)	Zebrafishes fed with BSF larvae reared on coffee by products show: − Variability in viable counts based on substrate. − Highest occurrence of Lactobacillaceae and Leuconostoccaceae. − Low bacterial richness/evenness. − Higher abundance of Clostridia in zebrafish influenced by bioactive compounds from coffee by-products. − Core fish microbiota remained stable.	[68]
	Mixture of vegetables			Zebrafishes fed by BSF larvae reared on mixture of vegetable show: − Highest bacterial richness/evenness in larvae and frass of BSF. − Low bacterial richness/evenness. − Higher abundance of Enterobacteriaceae in zebrafish, possibly influenced by bioactive compounds (chlorogenic and caffeic acids) in the substrate. − Core fish microbiota remained stable.
6.	BSF meal (control)	Fed 6 weeks	Oncorhynchus mykiss	Well accepted; no impairment in fish growth, gut and liver health, or marketable characteristics.	[49]
	3% BSF prepupae meal	Fed 6 weeks
	20% BSF prepupae meal	Fed 6 weeks		Well accepted; increased immuno-related gene expression and slight reduction of fillet redness and yellowness.

Table 2. Recent studies on the effects of coffee-reared BSF larvae as feed for fishe.

No.	Name of Rearing Substrate	Rearing Conditions	Produced BSF Fed to	Results	Reference
1.	BSF reared on coffee silverskin enriched with 10% Schizochytrium sp.	BSF as substitution of fish meal (0, 25, 50, and 75%)	Zebrafish (Danio rerio)	At 0% (baseline) and 25%, zebrafishes show standard responses based on the control diet. The 50% substitution gives the best compromise between sustainability and proper fish growth. However, at 75% and 100% substitution, severe hepatic steatosis was observed, along with microbiota modification, increased lipid content, fatty acid modification, and higher expression of stress and immune response markers.	[65]
2.	BSF reared on coffee silverskin with 10% Schizochytrium sp. microalgae	BSF as substitution of fish meal (0, 25, 50, 75, and 100%) for 6 months	Zebrafish (Danio rerio)	This study employed qPCR to assess the dynamics of antibiotic resistance (AR) genes in fish feed, including those with insect meal ingredients. Resistant genes studied: macrolide-lincosamide-streptogramin B (MLSB) [erm(A), erm(B), erm(C)], vancomycin (vanA, vanB), tetracyclines [tet(M), tet(O), tet(S), tet(K)], β-lactams (mecA, blaZ), and aminoglycosides [aac-aph]. Findings in diet samples: Detected: erm(B), tet(K), tet(M), tet(O), and tet(S). Not Detected: mecA, vanA, vanB, and aac-aph. Findings in zebrafish (juvenile and reproductive stages): Never Detected: erm(A), erm(C), vanB, and aac-aph. Widespread: erm(B), tet(M), and tet(S).	[66]
		0% BSF larvae		erm(A), erm(C), vanB, aac-aph not detected in zebrafish at any stage.
3.	Marine-based substrates		Zebrafish	− Significantly improves the lipid profile of BSF larvae. − Enhanced omega-3 fatty acids profile.	[67]
	Fish discards			− Improvement of approximately 40% in the lipid profile. − Increase in essential fatty acids.
	Fish discards with coffee silverskin with Schyzochytrium sp.			− High levels of EPA and DHA recorded. − Still reliant on marine-based bioresources
	Coffee silverskin enriched with 10% of Schizochytrium sp.	100% fish meal replacement		Affected fish stress response, oocytes maturation stages, spawning, and hatching success.
4.	Coffee silverskin enriched with 10% of Schizochytrium sp.	0% fish meal replacement	Zebrafish	No impairment observed in zebrafish physiological responses	[48]
		20% fish meal replacement
		50% fish meal replacement
		75% fish meal replacement		Affected fish stress response, oocytes maturation stages, spawning, and hatching success.
		100% fish meal replacement
5.	Coffee by-products	BSF larvae and frass	Zebrafish (Danio rerio)	Zebrafishes fed with BSF larvae reared on coffee by products show: − Variability in viable counts based on substrate. − Highest occurrence of Lactobacillaceae and Leuconostoccaceae. − Low bacterial richness/evenness. − Higher abundance of Clostridia in zebrafish influenced by bioactive compounds from coffee by-products. − Core fish microbiota remained stable.	[68]
	Mixture of vegetables			Zebrafishes fed by BSF larvae reared on mixture of vegetable show: − Highest bacterial richness/evenness in larvae and frass of BSF. − Low bacterial richness/evenness. − Higher abundance of Enterobacteriaceae in zebrafish, possibly influenced by bioactive compounds (chlorogenic and caffeic acids) in the substrate. − Core fish microbiota remained stable.
6.	BSF meal (control)	Fed 6 weeks	Oncorhynchus mykiss	Well accepted; no impairment in fish growth, gut and liver health, or marketable characteristics.	[49]
	3% BSF prepupae meal	Fed 6 weeks
	20% BSF prepupae meal	Fed 6 weeks		Well accepted; increased immuno-related gene expression and slight reduction of fillet redness and yellowness.

3.3. Bibliometric Analysis of the Effects of Feeding SCG to BSF

In order to illustrate the landscape of research on feeding SCG to the cultivation of BSF, a bibliometric analysis is conducted. The author keywords from the 18 core papers are entangled in an orderly fashion, as shown in Figure 2, as a result of the VOSViewer software (version 1.6.17). There are four clusters that can be observed, as follows:

• BSF reared with SCG for aquaculture (red)
• (Bio)chemical analysis related to BSF and SCG (green)
• BSF and bioconversion (blue)
• SCG and other substrates (yellow)

Figure 2. The bibliometric visualization of the research on the effects of SCG to the BSF cultivation.

Figure 2. The bibliometric visualization of the research on the effects of SCG to the BSF cultivation.

The details of the members of the aforementioned clusters and their strength (weight) are detailed in

Table 3. All keywords from the 18 key papers in this study, as visualized in Figure 2.

Cluster 1	Weight	Cluster 2	Weight	Cluster 3	Weight	Cluster 4	Weight
zebrafish	9	coffee silverskin	13	black soldier fly	28	bioconversion rate	9
edible insects	8	Hermetia illucens	13	frass	14	brewer’s spent grains	6
microbiota	8	microalgae	13	insect farming	7	protein conversion	6
alternative proteins	5	bioaccumulation	6	bioconversion	5	spent coffee grounds	6
fatty acids	5	chemical hazard	6	circular agriculture	5	substrate mass reduction	6
reproduction	5	Hermetia illucens prepupae	6	integrated pest management	5	upcycling	6
Schizochytrium sp.	5	potentially toxic elements	6	repellence	5	fermented substrate	3
aquaculture	4	antibiotic resistance genes	5	systemic defenses	5	growth performances	3
circular economy	4	fa profile	5	coffee pulp	4	SCG	3
fish feed	4	principal component analysis	5	npk	4
insect meal	4	rearing substrates	5	prepupae	4
Isochrysis galbana	4	relative macromolecular composition	5	spent coffee	4
polyunsaturated fatty acids	4	food chain by-products	3	sustainable protein	3
qPCR	4	prepupal fatty acids profile	3	waste management	3
Schizochytrium limacinum	4	waste valorization	3	caffeine	2
tetracyclines	4

.

The mapping of the keywords in Figure 2 resulted from the bibliometric analysis of the keywords generated by the authors (“author keywords”) of the 18 core papers on the usage of SCG or related coffee parts for the rearing of BSF larvae. There are 55 keywords that are correlated with each other, with 162 links and a total link strength of 166. They are clustered together, with the minimum cluster size optimized to be 8.

3.4. Bibliometric Analysis of a Single Keyword: “Black Soldier Fly”

The bibliometric analysis conducted via VOSViewer software allows us to specifically assess the multiple connections of one keyword of interest. That particular keyword is “spent coffee ground”. This is quite a niche keyword for BSF cultivation that might have plenty of room for innovation in the future. Based on the data in Table 3, the keyword “spent coffee ground” is placed in cluster 4 (yellow), with a weight of 6. The connections to the single keyword “spent coffee ground” based on VOSViewer analysis for the 18 core papers are shown in Figure 3 and detailed in

Table 4. Network analysis for the terms associated with the keyword “spent coffee ground” obtained from Figure 3.

No.	First Node	Second Node	Cluster for the First Node	Cluster for the Second Node	Link Strength
1.	spent coffee grounds	substrate mass reduction	4	4	1
2.	spent coffee grounds	upcycling	4	4	1
3.	black soldier fly	spent coffee grounds	3	4	1
4.	bioconversion rate	spent coffee grounds	4	4	1
5.	brewer’s spent grains	spent coffee grounds	4	4	1
6.	protein conversion	spent coffee grounds	4	4	1

. Please kindly note that a gray ellipse is intentionally placed to cover most of the keywords not related to the connection stemming from the keyword “spent coffee ground”.

Based on Figure 3 and Table 4, it can be concluded that spent coffee grounds in the cultivation of BSF larvae are clearly connected with the keyword “black soldier fly”, which enables the “substrate mass reduction” with a specific “bioconversion rate” for the beneficial process of “upcycling” organic wastes such as “brewer’s spent grains” (among other resources) to obtain “protein conversion”. The portion highlighted in pale yellow in Figure 3 is the area of the gap in the research on BSF cultivation using SCG and/or other coffee parts. It is clearly seen that there is indeed plenty of room for improvement and innovation in this research area. To name a few interesting topics, there are “food chain by-products”, “circular agriculture”, “antibiotic resistance genes”, “alternative proteins”, “aquaculture”, and “circular economy”.

4. Conclusions

This study reports the recent development of the utilization of SCG (and/or coffee parts, mixed with or without other organic materials) for the cultivation of BSF larvae. As coffee contains caffeine as an alkaloid that hinders the growth of some plants or the BSF larvae themselves, the right composition or modification of SCG is intriguing to be explored. The recent usage of SCG-derived or coffee-fed BSF larvae in aquaculture and fisheries is also reported here, along with the limitations of substitution levels and the related consequences for the fishes. Bibliometric analyses are also performed to supplement the mapping of the recent advances in the cultivation and application of BSF larvae using SCG and/or coffee parts.