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Review

Manure Valorization Using Black Soldier Fly Larvae: A Review of Current Systems, Production Characteristics, Utilized Feed Substrates, and Bioconversion and Nitrogen Conversion Efficiencies

by
Florian Grassauer
*,
Jannatul Ferdous
and
Nathan Pelletier
Food Systems PRISM Lab, University of British Columbia Okanagan, 3247 University Way, Kelowna, BC V1V1V7, Canada
*
Author to whom correspondence should be addressed.
Sustainability 2023, 15(16), 12177; https://doi.org/10.3390/su151612177
Submission received: 7 July 2023 / Revised: 1 August 2023 / Accepted: 7 August 2023 / Published: 9 August 2023
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Abstract

:
The growing demand for animal products leads to mounting environmental impacts from the livestock sector. In light of the desired transition from linear to circular nutrient flows and an increasing number of formal commitments toward reducing environmental impacts from livestock production, manure valorization using insects (particularly black soldier fly larvae; BSFL) gains increasing importance. Based on the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) methodology, this paper identified 75 BSFL production systems utilizing various types of manure as feed substrates. The review highlights considerable differences in system design regarding the different production steps and their specific characteristics. These differences lead to a wide spectrum of rearing performances, which were measured by a suite of indicators, including dry matter reduction (DMR), waste reduction index (WRI), feed conversion efficiency (FCE), bioconversion rate (BCR), and nitrogen reduction. The results further show that, to date, most manure-valorizing BSFL production systems operate at the micro-scale level. However, specific reduction targets for manure-related emissions will likely necessitate large-scale systems at the farm or industrial level, and further research should thus focus on the comprehensive assessment of potential environmental benefits of manure valorization using BSFL.

1. Introduction

Agriculture faces the twin challenges of feeding a growing population and simultaneously preserving the environment for future generations [1,2]. Within this context, the increasing demand for animal products creates both considerable pressures and opportunities. Key among these is the ever-increasing volume of livestock manure originating from animal production systems [3]. Although generally recognized (and utilized) as valuable fertilizer in order to cycle nutrients back into cropping systems, poorly managed livestock manure or the production of manure in excess of the regional assimilatory capacity may also create severe environmental impacts [4,5,6]. For example, inefficient storage, poor management, and excessive application of manure can lead to eutrophication via surface runoff or leaching of phosphorous (P) and nitrogen (N) [7]. In current livestock production systems, emissions to air, soil, and water from manure management and subsequent field application contribute a significant share to overall life-cycle emissions, especially greenhouse gas emissions, as shown for the egg industry by Turner et al. [8], for dairy farms by Grassauer et al. [9], or beef-producing farms by Grassauer et al. [10].
In addition, while feed utilization efficiencies differ between livestock species and age groups, much of the feed provided to livestock is bypassed as undigested chemical energy and nutrients [11]. Regarding N use efficiency (i.e., the ratio between the N in animal products and the dietary N intake), Hristov et al. [12,13] reported 14% for fattening cattle, Huhtanen and Hristov [14] indicated a range from 14 to 45% for dairy cows, Millet et al. [15] estimated a value of 46% for fattening pigs from 8 to 100 kg, and Musigwa et al. [16] reported values of 60% for broilers on a high-protein diet versus 63% for broilers on a low-protein diet. However, life-cycle N use efficiency, which also takes losses occurring up- or downstream of the farm (i.e., the production system) into account, is even lower in livestock supply chains [17]. For feed energy efficiency, results for different livestock species depend on the definition of the indicator, which may differ among scholars. For example, Phuong et al. [18] defined energy efficiency as the ratio between energy in animal products and digestible energy intake and calculated a value of 34% for dairy cows. On the other hand, Musigwa et al. [16] estimated the energy efficiency of broiler chicken as the metabolizable energy (i.e., the gross energy consumed minus animal excreta [19]) per gross energy and reported values of 73 and 74% for broilers on a high-protein and low-protein diet, respectively. Most of the bypassed nutrients and energy are respired back into the atmosphere as short-cycling carbon as well as methane (CH4), volatilized ammonia (NH3), and nitrous oxide (N2O) emissions when manure is stored and applied to agricultural land [2,3], contributing to both climate change and acidification impacts. For these reasons, a variety of alternative technologies for manure management have been developed, including solid–liquid separation [20], waste-to-energy pathways like gasification, and anaerobic digestion [21]).
A promising but comparatively unconsidered means of manure treatment is its utilization as a feed substrate for producing insects [7], which are able to convert low-value organic resources like manure into high-protein feed ingredients utilizable in animal nutrition [22] or as a raw ingredient for biodiesel production [23]. Indeed, some have proposed that insect production based on low-opportunity cost substrates offers a potential solution to the growing global demand for protein sources as food and feed [24,25]. This can reduce pressure on feed resources as well as emissions both from feed input supply chains and manure management [22,23,26]. Additionally, the frass (i.e., the residual material after insect digestion) can be used as fertilizer with lower mass, moisture, and nutrient contents compared to raw manure [7,27] or even as an additional feed input as demonstrated by Yildirim-Aksoy et al. [28], who utilized BSFL frass to increase the weight gain of farm-raised channel catfish. In this way, insects can potentially contribute to the transition from linear to circular nutrient flows in crop/livestock systems by upcycling nutrients that are currently inefficiently utilized [22]. Further, this manure valorization pathway is expected to reduce the environmental burdens of livestock production systems by providing high-protein feed ingredients, which can be used to partially substitute conventional feed ingredients, whose production and provision is a central contributor to environmental impacts in livestock production systems [8,29].
The black soldier fly (BSF), Hermetia illucens, is currently the most suitable insect species for manure valorization as the larvae can digest a wide range of substrates due to its superior array of digestive enzymes compared to other fly species [7]. The BSF belongs to the family Stratiomyidae of the order Diptera and is originally native to the Americas, from Argentina to the central USA [30]. Due to its broad temperature tolerance and widespread human-caused distribution, the BSF is now prevalent in temperate and tropical regions throughout the world [7,30,31]. Oviposition occurs between 27.5 and 37.5 °C, with optimal temperatures being reported as 32 °C or higher [32]. Eggs usually hatch within 102–105 h at 24 °C, and larvae mature within 22–24 days under optimal conditions [33,34]. At the prepupae stage, the larvae stop feeding and empty their guts for pupation. This stage is characterized by a fat larvae body with maximal stored energy, making it the appropriate stage for food or feedstuff collection [30]. Black soldier fly larvae (BSFL) are considered a valuable feed ingredient for the aquaculture and monogastric livestock sectors [35,36] because they contain high levels of protein and fats [25,37]. They can be included in feeds at a rate of 10–15% dry matter and are usually used to substitute soybean or fish meal [30].
BSFL can potentially be reared on different types of manure (e.g., dairy, swine, or poultry manure) [38,39,40,41,42]. Generally, the type of feeding substrate has a significant impact on the larvae’s consumption rate, development time, and weight [43,44] as the efficiency of converting the organic matter and its contained nutrients into body weight and protein heavily depends on the residual energy content of the feed substrate [45] and generally increases as a function of substrate gross energy and nutrient contents [46]. Therefore, parameters on the bioconversion and nitrogen conversion efficiency of BSFL production systems are of pivotal importance in determining the suitability of different feed substrate types and the overall environmental sustainability and economic viability of BSFL production [22].
To date, BSFL production systems that utilize manure as a feed substrate are only described in a limited number of studies compared to systems that use animal feed, co-products from plant and animal product processing, or food waste [22] but will likely gain more importance as an increasing number of binding pledges towards reducing GHG emissions in combination with specific reduction targets from manure and fertilizer-related emissions is enacted in jurisdictions worldwide [47]. Further, the increasing number of related studies reports a growing variety of utilized feed substrates and BSFL-rearing procedures differing in production characteristics, system designs, and management practices [48]. Therefore, this review provides an overview of current BSFL production systems that utilize manure or mixtures of manure and other waste products or by-products in order to inform future systems design and to contribute to a more comprehensive understanding of the efficiency of such systems depending on different factors, such as the utilized feed substrate. The review focuses on the production characteristics of different production steps in BSFL production, assesses the wide variety of utilized feed substrates, and presents key performance parameters on the bioconversion and nitrogen conversion efficiencies exhibited by those systems by answering the following research questions (RQs):
  • RQ1: What are the production characteristics of current manure-valorizing BSFL production systems regarding different production steps, the production scale, the utilized BSFL strain, the geographical context, and optimal rearing parameters?
  • RQ2: Which feed substrates (i.e., manure or mixtures of different types of manure or with other waste products or co-products) are currently utilized in BSFL production, what is their nutritional composition, and how are those feed substrates prepared before rearing?
  • RQ3: Which efficiencies do those systems exhibit in terms of various reported performance parameters regarding nitrogen converstion and bioconversion, depending on the utilized feed substrate?

2. Materials and Methods

In order to identify current BSFL production systems across the globe, a systematic review of peer-reviewed original research articles was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) methodology [49,50], as presented in Figure 1.

2.1. Search Strategy

The literature review was initiated by a keyword search utilizing the Web of Science Core Collection, implementing a temporal scope from 2010 to 2022 and using the following keyword combinations: (“Hermetia illucens” OR “black soldier fly”) AND (“insect production” OR “insect farming”) AND (“manure” OR “manure valorization” OR “manure-fed” OR “chicken manure” OR “poultry manure” OR “cattle manure” OR “dairy manure” OR “pig manure” OR “swine manure”). In the next step, the reference sections of the identified records of the initial keyword search (n = 106) were screened for additional relevant articles using the search term “manure”. This procedure yielded another 60 papers, equalling a total of 166 records to be checked for duplicates in the next step, which resulted in the exclusion of seven records.

2.2. Screening Criteria

Titles, keywords, and abstracts of the remaining 159 records were then screened against the following criteria: (1) articles had to be written in English, (2) only original research articles (i.e., no review articles, book reviews, short communications, or technical notes) were considered, (3) articles had to describe a BSFL production system, and (4) the BSFL production system had to use manure as feed substrate. Although review articles were not included, reference lists of review articles were screened for additional research articles as described in Section 2.1. Accordingly, 115 records that did not meet one or more of these criteria were excluded. The remaining 44 records were subsequently sought for retrieval by institutional means, whereby one article could not be accessed and was hence also excluded. Then, 43 peer-reviewed original research articles were subjected to full-text screening, which led to the exclusion of another 13 documents due to non-compliance with one or more of the following eligibility criteria: (1) the focus of the study was not on the BSFL production system; (2) no data regarding the BSFL production system were provided (i.e., the BSFL production system was only briefly mentioned and not described in detail).

2.3. Extraction and Synthesis of Data

The final sample resulted in 30 documents describing a total of 75 BSFL production systems that were reviewed for specific characteristics regarding different production steps, the scale of production, and the utilized feed substrate. Additionally, the documents were screened for data and indicators on the nitrogen conversion and bioconversion efficiencies of the described systems.
More specifically, to answer RQ1, information was collated regarding (1) certain rearing parameters (e.g., temperature and relative humidity) for the different production steps (i.e., egg production, larvae nursing, and larvae rearing), (2) the scale of production, (3) the utilized BSFL strain, and (4) the geographical context of the production system.
To answer RQ2, the available data regarding the utilized feed substrates were tabulated. This included identifying the different feed components (in the case of mixtures), the nutritional composition of the feed substrate, and the preparation steps prior to rearing.
For RQ3, the data extraction aimed at different indicators that describe the nitrogen conversion and bioconversion efficiency of the reviewed production systems. Documents that did not report these indicator results were additionally screened for the necessary data to calculate the individual indicators.

3. Results and Discussion

3.1. Production Characteristics of BSFL Production Systems

3.1.1. General System Description

Rearing insects on livestock manure is a relatively novel pathway of valorizing bypassed, undigested chemical energy and nutrients that has attracted increasing scholarly interest over the last two decades [4]. This novelty is also reflected by the production scales of the 75 reviewed BSFL production systems. The vast majority of systems (n = 66) are operated at the micro-scale (i.e., in a laboratory setting). Another four systems were operated on a small scale, i.e., 10,000 larvae per batch [51] and 9.6 kg DM BSFL output per day connected to a poultry farm with 130 broilers [46]. One study did not specify the scale of production [52], and the remaining four systems operated on an industrial [26,53] or pre-industrial scale [54].
The distribution of the reviewed BSFL production systems among different jurisdictions is displayed in Figure 2A. The bulk of the production systems operate in China (42 of 75 systems), followed by the US (n = 9), the Netherlands (n = 7), Switzerland (n = 6), Indonesia (n = 4), Germany (n = 2), Italy, Kenya, South Korea, Thailand, and Ghana and Mali defined as West Africa (n = 1 each).
Figure 2B shows the utilized BSFL strains across the reviewed BSFL production systems. In 48 of the 75 systems, no specific BSFL strain was mentioned. BSFL systems that did specify a certain strain most commonly (n = 17) used the Wuhan strain, which originates from a temperate region close to Wuhan, China [41]. Other utilized strains originate from the Coastal Plain Experiment Station at the University of Georgia, which is maintained at the Texas AgriLife Experiment Station, Stephenville, TX (Texas strain) [55]; from the Guangdong Insect Institution, China (Guangzhou strain) [41]; or from Africa, Australia, Europe, and Southeast Asia [56]. Zhou et al. [41], who compared the development of three BSFL strains reared on chicken, pig, and dairy manure, found high phenotypic plasticity among the different strains and identified significant differences in larval development, final larvae weight, and protein content. They identified climatic variation as the mean driver of this phenotypic plasticity and suggested that BSF should be sourced from similar climate regions to obtain the best development results [41]. To further harness the potential of the vast genetic diversity and the variety of unique regional gene pools, more differentiated BSF breeding strategies will be necessary for future research [57].

3.1.2. Egg Production System

The egg production system comprises the housing and maintenance of an adult fly colony under controlled conditions in order to produce sufficient amounts of eggs that can be used in larvae-rearing systems to (1) produce BSFL products such as BSFL oil or BSFL meal and (2) restock and maintain the adult colony [4,58]. Overall, 17 of the 75 reviewed BSFL production systems did not specify a separate egg production system, meaning they depend on natural inoculation from local wild BSF populations or purchased eggs or young larvae from other facilities [59]. While systems with natural oviposition are rather cheap and easy to implement [58], all of the reviewed systems that mentioned a method of egg production (58 of 75) rely on an adult colony (n = 53) or purchased eggs (n = 5). Different cages were used for adult fly housing, from simple wooden or metal frames with wire mesh on each side, greenhouses, and plastic boxes to sophisticated net systems sold under registered trademarks. If colony sizes were reported in the literature, most of the numbers were estimates and ranged from a few thousand flies [46] to large populations housed in walkable double-net systems [56].
As mentioned, keeping an adult fly colony for controlled breeding is more labour- and cost-intensive than relying on natural inoculation from wild BSF populations. However, it also offers several advantages, such as stable larvae production rates, no seasonal shifts, and reproducible production yields [58]. To ensure these advantages, adult colonies are usually kept under a controlled climate in terms of temperature and relative humidity. A total of 43 of the 75 systems reported a temperature with a range of 25–28 °C and a mean of 27 °C, whereas 37 systems indicated a relative humidity ranging from 50 to 70% with a mean of 62%. One system from West Africa (Ghana and Mali) also mentioned keeping the adults inside a poultry barn in net cages and moving them outside to promote mating and oviposition whenever weather conditions allow for exposure to sunlight [46,60]. Shumo et al. [61], who described a BSFL production system located in Kenya, even kept their adult colony outside permanently due to the suitable climate. In geographic regions without a suitable climate to house the adult colonies outside, climate control was reported to be ensured by keeping the colonies in greenhouses.
Although adult BSFs do not require any feed within their lifespan of about 14 days [46], using an oviposition substrate to promote egg laying was found to be common practice among described egg production systems. A total of 24 of the 75 systems described specific oviposition substrates, including chicken manure, residues from larvae rearing, spent grain, or the Gainesville House Fly Diet, a specialized insect-rearing diet consisting of 50% wheat bran, 30% alfalfa, and 20% corn [62]. In addition to the oviposition substrate, some systems also described the use of a specific oviposition medium (most commonly corrugated cardboard), which is placed on top of the oviposition substrate and is usually used by the female flies for egg laying [56,61]. Such mediums can then be manually retrieved to harvest and transfer the egg clusters [40,63].
The complete suite of extracted data regarding the 53 described egg production systems relying on adult colonies (i.e., adult fly housing, temperature, relative humidity, and oviposition substrate) is presented in Table S1 in the Supplementary Material.

3.1.3. Larvae Nursing System

After harvesting, the BSF eggs are often transferred to a larvae nursing system. In total, 55 of the 75 reviewed production systems described a separate larvae nursing system. Larvae nursing plays an important role in ensuring the optimal growth, survival, and overall production efficiency of the larvae for the initial time period after hatching [4,56] and is also operated under a controlled climate. Bosch et al. [48] highlighted that this pre-trial rearing of neonates influences larval and prepupal weight, development time, and possibly protein and fat contents of the finished product.
Nursing systems usually utilize specialized nursing substrates ad libitum to ensure the optimal development of the neonates [64]. Reported nursing substrates were usually of higher nutritional quality than the subsequently used rearing substrates and included standard poultry feed, standard colony diets, such as the Gainesville House Fly Diet, and wheat bran. The nursing diet is usually placed in plastic containers with egg clusters on top [65]. These containers should be dimensioned in a way that the required nursing substrate thickness is between 5 and 10 cm [66] to maintain the desired substrate temperature, which, in turn, influences larval development [48]. Therefore, in addition to managing the desired ambient temperature and relative humidity, Bosch et al. [48] also highlighted the necessity to monitor the substrate temperature, which can significantly deviate from the ambient temperature. If the substrate temperature rises to a certain value above the ambient temperature, reducing substrate layer thickness or substrate ventilation could be necessary [48].
As mentioned, the rearing containers are placed in a controlled climate for a certain period of time. A total of 55 of the 75 systems reported a desired temperature with a range of 26–30 °C and a mean of 28 °C, whereas 49 systems indicated a relative humidity ranging from 60 to 80% with a mean of 66%. Temperatures and relative humidity in the nursing system are kept at slightly higher levels than in the egg production systems, which is intuitive since the eggs and neonates require higher temperatures and humidity than the adult flies for optimal development [65,67]. Depending on the climate at the BSFL production systems’ location, different means of climate control were reported in the literature. Production systems located in cold and temperate climates (Cfb and Dwa, respectively, according to Köppen climate classification [68]) in Tianjin, China, Switzerland, and the Netherlands, used climate chambers or cabinets [37,52,56,64], whereas production systems in subtropical climate (Cfa) of Wuhan, China mainly operated their larvae nursing systems in greenhouses [41,53,69,70,71]. Other reported means of climate control in larvae nursing were incubation chambers [72,73] and Rheem Environmental Chambers [40,51].
The larvae nursing is concluded after a certain time period (i.e., nursing period), after which the larvae are transferred to the rearing system. A total of 49 of the 75 reviewed systems reported the duration of the nursing period, which ranged from one to 13 days, with a mean of six days. The nursing period is influenced by the maintained climate, which can promote or impede the larvae’s metabolism, and the quality of the nursing substrate, which also influences growth potential and efficiency [74].
Detailed data on the 55 described larvae nursing systems, including the utilized nursing substrate, the temperature and humidity, the reported means of climate control, and the duration of the nursing period, can be found in Table S2 in the Supplementary Material.

3.1.4. Larvae Rearing System

Similarly to the larvae nursing stage (see Section 3.1.3), BSFL rearing occurs in different types of containers and under a controlled climate. The rearing containers are usually made of plastic, metal, glass, or cement. They are typically open but are sometimes covered with gauze to help maintain humidity levels [75] or mesh to keep potential predators and competitors out of the rearing containers [46]. Depending on the systems’ production scale, the size of the rearing container differs considerably. For example, Wang et al. [76] described a micro-scale production system, which uses Petri dishes for individual larvae rearing. In contrast, Xiao et al. [53] reported an industrial-scale production system with one ton of fresh chicken manure and one million BSFL as inputs per batch, which utilized a cement pool (3 × 4 × 0.2 m) as a rearing container. Regarding the controlled climate, 71 of the 75 reviewed systems reported a desired temperature with a range of 26–30 °C and a mean of 28 °C, whereas 69 systems indicated a relative humidity ranging from 50 to 85% with a mean of 66%. Thus, compared to the larvae nursing systems (see Section 3.1.3), the desired ambient temperature and relative humidity of larvae rearing stages are similar despite the higher number of reported values.
Regarding development time, the reported systems showed a wide range of values. The development time is usually measured in days and spans from the beginning of the rearing trial (i.e., the inoculation of the feeding/rearing substrate with larvae) to the termination point at the desired larval development stage [48]. The reported range of the 75 reviewed systems is 8 to 214 days, with a mean value of 70 days and a median of 18 days. The huge difference between the mean and median can be explained by three systems described by Oonincx et al. [37], which exhibited development times of 144, 144, and 214 days for BSFL reared on chicken, pig, and cattle manure, respectively. Those values are 5.5 and 8.2 times higher than the next-highest value of 26 days reported by Julita et al. [77]. Oonincx et al. [37] attributed those high development times to three causes: First, the poor dietary quality of the different manure types, which were dried and ground prior to rehydration and larval bioconversion. This procedure destroys heat labile B vitamins [78] and reduces microbial populations of certain bacteria, such as Bacillus natto, which are essential for larval development [79,80,81]. Second, the rearing systems described in Oonincx et al. [37] used neonates without the crucial preceding larvae nursing stage (see Section 3.1.3), which has a significant influence on the development time [37,48]. Third, the utilized feeding regime, which distributed the total amount of feed substrate over a longer period of time compared to other studies, indicates that the feed substrate was restricted in this study [37]. The shortest development time was reported by Roffeis et al. [46], who harvested the BSFL after eight days, independently of the larval development stage. Other systems described by Parodi et al. [6] harvested the BSFL at the emergence of the first prepupae after 8.6 days, which shows that the ideal larval development stage can be reached after a significantly shorter time compared to the median of the reported values (18 days) if rearing conditions are optimal.
The rearing system-related data extracted from the literature regarding temperature and relative humidity, utilized rearing devices, and development time can be found in Table S3 in the Supplementary Material.

3.1.5. Larvae Harvesting and Processing

After the development time, BSFL are harvested. Although the larval development stage at harvest was reported in only about half of the reviewed literature (i.e., in 39 of 75 systems), Sandrock et al. [56] mentioned the sixth instar stage (i.e., prepupal stage) as the optimal development stage for harvest. This prepupal stage is characterized by the highest larval biomass [73], fat, and protein contents [40,77], which are accumulated during late instars to serve as an energy reserve for the pupation period and adult life stage [64,82]. Prepupae can be identified by a melanized cuticle compared to a white cuticle found in larvae at earlier development stages [37]. Moreover, at the prepupal stage, larvae stop feeding and show migratory behaviour away from the feed substrates and searching for suitable pupation sites [76,83]. Accordingly, 38 of the 39 BSFL production systems, which reported a harvest stage, aimed at the prepupal stage and employed different points of rearing termination. The most common termination point was when the first prepupae emerged (n = 27 systems). Other systems harvested the BSFL after a defined share of larvae turned into prepupae, e.g., 40% in Miranda et al. [51] or 100% in Lalander et al. [84], or just collected individual prepupae detected during a series of multiple checks over the entire rearing period [40,54]. On the other hand, Gold et al. [64] and Roffeis et al. [46] reported a termination point after nine and eight days of rearing, respectively, independently of the larval development. Gold et al. [64] intended to harvest the BSFL before the appearance of prepupae, arguing that prepupae are less suitable for animal feed as they are richer in chitin [64,85].
Further processing can be split into several different processing steps, including separation from the feed substrate and residual frass, purging, cleaning, and killing/drying. Due to most of the reviewed systems operating on a micro- or laboratory scale, 44 of the 46 systems that did report a separation technique indicated a manual harvest of the larvae, usually with forceps. However, there are also system concepts that exploit the natural migratory behaviour of the larvae before the pupation stage by providing ramps that lead the larvae away from the feed substrate and toward suitable pupation site decoys (e.g., plastic pipes) where the larvae can be collected easily [30]. Purging was only reported for 4 of 75 systems and is defined as a post-rearing treatment period during which larvae are deprived of their rearing substrate for a certain time to allow them to empty their guts [46], which can reduce the risk of biological hazards if the BSFL are intended to serve as livestock feed. The reported purging periods lasted for 12–48 h and either provided a different N-free substrate (e.g., in Parodi et al. [6]) or no substrate in order to partially starve the larvae (e.g., in Wang et al. [52]). A total of 39 systems further reported a cleaning step that involved using a simple water rinse to remove any excess material on the larvae, and 51 systems specified a distinct killing/drying step, using either drying chambers, microwave ovens, or freezing. The technology utilized for the killing/drying step was shown to influence the physicochemical characteristics and microbial loads of BSFL. On the one hand, heat treatment is less expensive and exhibits a higher drying efficiency compared to freeze-drying. However, on the other hand, freeze-drying was shown to aid in a superior quality of the dried products regarding nutritional composition as it reduces water activity, inhibiting microbial activity and enzymatic reactions that would potentially degrade or even spoil the product [86].
Extracted data from the literature regarding larvae harvesting and further processing can also be found in Table S3 in the Supplementary Material.

3.2. Utilized Feed Substrates

The 75 reviewed BSFL production systems utilized a multitude of different feed substrates for rearing, which either consisted of a single manure type (n = 49), a mixture of multiple manure types (n = 12), or a mixture of manure and other waste products or by-products (n = 14). The different manure types originated from chicken (i.e., broiler production and laying hens), cattle (i.e., manure from beef cattle and dairy cows), pigs, horses, and sheep. The utilized waste products and by-products encompassed canola straw [72,73], soybean curd residues [70], vegetable waste [77], and brewery waste [46,60]. Additionally, there were occasions when minimal amounts of other substances were added to the feed substrate (i.e., coarse chabazite [54] and ammonium chloride [6]) or when inoculation with different strains of Bacillus and Paenibacillus was performed [69].

3.2.1. Nutritional Composition

In order to compare the nutritional composition of the different substrates and substrate mixtures, the feed substrates were clustered into different feed substrate groups regarding their respective main ingredients. Accordingly, feed substrates and substrate mixtures that contain ≥ 50% dry matter of a certain manure type were assigned to a group labelled with the respective manure type. Feed substrates and mixtures that contain ≥ 50% dry matter of waste products or by-products were subsumed into another group. This procedure yielded six different feed substrate groups: (1) chicken manure (i.e., substrates containing ≥ 50% dry matter of chicken manure; n = 33), (2) cattle manure (n = 18), (3) pig manure (n = 16), (4) horse manure (n = 2), (5) sheep manure (n = 2), and (6) others (i.e., substrates containing more than ≥50% dry matter of waste products or by-products; n = 4). Figure 3 depicts the boxplots of the nutritional composition of the different feed substrate groups in terms of their dry matter (DM), total organic carbon (TOC), nitrogen (N), and phosphorous (P) contents.
The DM (in %) differed considerably among the feed substrate groups, with a total range of 13–91% across all groups. The highest mean DM contents were found in the four BSFL production systems that utilized horse and sheep manure as the main ingredient, with values of 89.5 and 90.2%, respectively. These four systems were evaluated by Julita et al. [77] and used horse and sheep manure as a sole ingredient or mixed it with vegetable waste at a ratio of 50:50. The lowest mean DM contents were exhibited by feed substrates that contained ≥ 50% dry matter of waste or by-products. These were soybean curd residues [70] and fresh brewery waste [46,60], which have low DM contents of 17.7 and 40%, respectively (Figure 3A). The DM contents in the other groups largely overlapped with mean values of 33.6% for chicken manure, 24.3% for cattle manure, and 27.3% for pig manure.
Figure 3B presents the ranges of TOC contents (in % of DM) across the different feed substrate groups. Substrates of the chicken manure group showed the lowest TOC contents with a mean value of 37.2%, followed by the pig manure group, for which only one study reported the TOC content at a level of 44.8% [87], and the cattle manure group with a mean value of 46.5% TOC. The highest values were found in the “others” group (mean = 51%), for which numbers of three of four systems were reported [70]. For the horse and sheep manure groups, no TOC values were reported.
The N contents showed the lowest variation among the different substrate groups, with an overall range from 1.6 to 7.4% per DM. The highest mean values were found in the chicken manure group (4.2% N per DM) followed by the others group (3.2% N per DM), the cattle and pig manure groups (2.5% N per DM), the sheep manure group (2.4% N per DM), and the horse manure group (1.9% N per DM) (Figure 3C). This is intuitive as (1) chicken and pigs are usually fed large shares of concentrates with higher N content compared to ruminants (e.g., cattle and sheep), and (2) chickens exhibit a higher share of N excretion per intake compared to pigs and cattle [3].
The ranges of P contents of the different substrate groups are depicted in Figure 3D and show a considerable variation among the groups. Mean values ranged from 2.2% in the pig manure group to 0.4% in the others group. The chicken manure group was quite similar to the pig manure group, with a mean value of 2% P. The cattle manure group showed a mean value of 0.8% P, and the other groups ranged even lower, with mean values of 0.7 (horse manure), 0.5 (sheep manure), and 0.4% P (others).
The numerical data on the dry matter, TOC, and nutrient contents, along with a description and the different shares of ingredients of the utilized feed substrates, can be found in Table S4 in the Supplementary Material.

3.2.2. Preparation Steps

Bosch et al. [22] highlighted the importance of substrate preparation prior to rearing to create a homogeneous distribution of the contained nutrients and a texture that enables efficient digestion by the larvae. However, only 37 of the 75 BSFL production systems (i.e., 12 studies) described at least one substrate preparation step. For single-ingredient substrates, the most reported preparation step was the homogenization of manure. This was either performed by grinding [37], blending [64], or manual mixing with bare hands [40,51]. In multi-ingredient feed substrates, ingredient mixing was the most reported preparation step [69,70,71,72,73,88]. Other reported preparation steps were grinding [54]; milling and sieving fibre-rich ingredients prior to mixing (e.g., canola straw in Elsayed et al. [72,73]); inoculation with bacteria strains [69]; mixing with ammonium chloride [6]; and mixing with tap water to achieve the desired moisture content [37,54,61]. Some studies also reported manure drying right after collection as a means to store substrates over longer time periods prior to rearing [54,72,73].
The full list of feed substrate preparation steps reported in the reviewed BSFL production studies is shown in Table S5 in the Supplementary Material.

3.3. Bioconversion Indicators

3.3.1. Dry Matter Reduction

Dry matter reduction (DMR) is a commonly used indicator to determine the efficiency of BSFL production systems and is defined as the ratio of the consumed feed substrate and the total provided feed substrate [89]. It is calculated as follows:
DMR (%) = (1 − (W − R)/W) × 100,
where W is the initial amount of feed substrate, and R is the residual amount of substrate after completion of the larvae rearing [70,73].
A total of 58 of the 75 reviewed BSFL production systems provided values for or the necessary data to calculate the DMR, ranging from 12.7 to 75.5%, with a mean of 43.5%. The comparison of the different feed substrate groups shown in Figure 4A reveals no significant differences. However, Zhou et al. [41] found higher DMRs using chicken manure compared to cattle manure and related it to the fact that chicken manure contains higher values of nutrients. Contradicting results were, however, reported by Miranda et al. [40], who found higher DMRs in treatments with cattle manure than with chicken manure despite the superior nutritional composition of the chicken manure. This indicates that other parameters, such as the utilized BSFL strain, also critically influence the DMR [56]. The lowest value (12.7%) was reported by Gold et al. [64], who used fresh cattle manure with a very high moisture content (87%) and hence very inferior nutrient contents (e.g., 1.77% N). On the other hand, Bortolini et al. [54], who reported a DMR of 75.7%, utilized an optimized feed substrate composition consisting of 34.5% chicken manure, 7.2% coarse chabazite, and 58.3% water. This DMR is considerably higher than the reported mean of 43.5% and indicates that optimizing substrate composition maximized larval performance in terms of dry matter reduction [54,89]. Due to the low nutrient contents of different manure types, it has to be noted that systems that use feed substrates with higher nutrient contents can exhibit higher DMRs. For example, Mahmood et al. [90] reported a DMR of 89.66% for a BSFL production system utilizing kitchen biowaste.

3.3.2. Waste Reduction Index

The waste reduction index (WRI) was established by Diener et al. [39] as a further development of the DM reduction indicator as it also takes the required time for a given DM reduction into account. Accordingly, the WRI indicates the substrate consumption per development time and is defined as:
WRI = ((W − R)/W)/t × 100,
where W is the initial amount of feed substrate, and R is the residual amount of substrate after the development time t [39].
As indicated in Figure 4B, a total of 26 BSFL production systems of four different substrate groups provided either values for the WRI or the necessary input data to recalculate the WRI. The mean WRI over all different substrate groups was 2.5, and the highest mean was observed in the pig manure group, followed by the chicken and cattle manure groups. For the other group, only one value (3.2) was provided by Roffeis et al. [46,60], who utilized a mixture of fresh brewery waste and chicken manure. Overall, the WRI exhibited a range of 0.2 to 6.4. The lowest values were reported in the production systems described by Oonincx et al. [37], who used chicken, cattle, and pig manure as feeding substrates. The low values of those systems are caused by the extremely high reported development times of 144 days for chicken and pig manure and 214 days for cattle manure. Peng et al. [91] examined the effect of feed substrate accumulation thickness on the biotransformation of BSFL in fresh pig manure and tested it for 10, 15, and 20 cm. The highest WRI (6.4) was observed at 15 cm, which led to an optimal balance of oxygen concentration and substrate temperature [91]. On the other hand, the low accumulation thickness of the manure also led to a comparatively high surface area that fostered the evaporation of the fresh pig manure, which helps to explain the high WRIs [91]. Another factor influencing the WRI seems to be the nutrient contents of the feed substrates as Naser El Deen et al. [92] reported a WRI of 7.9 for a system based on fast food waste with a N content of 2.9%, which is superior compared to most manure types considered in this study.

3.3.3. Feed Conversion Efficiency

Feed conversion efficiency (FCE) is a widely known performance indicator of livestock production systems and describes the efficiency of turning ingested feed into desirable food products, such as larval body weight [93]. Although used under different terminology (e.g., “efficiency of conversion of ingested food to body substance (ECI)” by Waldbauer [94] or “conversion efficiency of the digested feed (CED) by Elsayed et al. [73]), the indicator is defined as the weight of desired product divided by the weight of the ingested feed [95]. In livestock production systems that consider an animal’s body (or parts thereof) as the desirable product (e.g., insect or meat production), the weight of the desired product is usually determined by the animal’s weight gain in a certain system. Accordingly, FCE in BSFL production systems can be calculated as follows [94]:
FCE (%) = (Weight gain)/(Ingested feed) × 100
Despite its key importance in determining the economic and environmental efficiency of livestock production systems [95], FCEs or the necessary data to recalculate it were provided for only 22 of 75 reviewed BSFL production systems. Thirteen FCEs were reported from the chicken manure group, while two values were reported from the cattle manure group, and seven values were reported from the pig manure group (Figure 4C). Across all groups, the lowest reported FCE was 2.9%, and the highest was 60.8% (mean = 23.8%). The lowest three values (i.e., 2.9, 3.4, and 4.5%) were reported by Oonincx et al. [37] and can also be related to the high reported development times of 144 days in systems that used chicken and pig manure and 214 days for the system that utilized cattle manure. This is because a longer development time means a higher share of ingested energy and nutrients are allocated to basal metabolism instead of body weight gain [37]. Comparing the three different feed substrate groups, there were lower FCE values found in the cattle manure group (mean = 16.9%) than in the chicken group (mean = 18.7%) and, especially, the pig manure group (mean = 35.2%). The lower values in the cattle manure group could be related to lower nutrient contents and lower relative amounts of easily available carbon as cattle manure contains comparatively high amounts of slowly digestible long-chain fibre compounds, such as cellulose, lignocellulose, and lignin [75,84,96].

3.3.4. Bioconversion Rate

The bioconversion rate or biomass conversion ratio (BCR) relates the mass of produced insects to the mass of provided feed substrate [40]:
BCR (%) = (Produced insect mass)/(Provided feed)
Among the different methodological descriptions reported in the reviewed papers, an inconsistency was found regarding calculating the produced insect mass. Whereas BCR is most commonly estimated using the total amount of produced insects as the denominator, Gold et al. [64] reported a modified equation, subtracting the initial larval weight at the start of the rearing from the total amount of produced insects after rearing. In this way, Gold et al. [64] only consider the larval weight gain throughout the rearing process, leading to slightly lower BCRs but a better reflection of the efficiency of producing living biomass from the feeding substrate of the actual rearing system. Considering the large variety of larvae nursing systems described in Section 3.1.3, which yield different larvae qualities and quantities, this aspect becomes increasingly important.
Among the 48 BCRs that could be retrieved from the literature, the lowest BCRs were found for the horse and sheep manure groups (Figure 4D). More specifically, the lowest values were reported for two systems that utilized 100% horse and sheep manure and exhibited BCRs of 1.6 and 0.9%, respectively, which can be explained by the low nutrient contents (e.g., 1.6 and 2.1% nitrogen for horse and sheep manure, respectively) [77]. Julita et al. [77] also described two other systems that used a mixture of 50% horse/sheep manure and 50% vegetable waste, which increased the overall substrate nutrient contents (i.e., 2.2 and 2.6% nitrogen for horse and sheep manure, respectively) and the BCRs to 2.1 and 1.8%, respectively. The BCRs exhibited by BSFL production systems for the other feed substrate groups do not differ significantly and are within a range of 1.8 to 17.2%, with a mean of 8.6%. Mahmood et al. [90] reported a mean BCR of 12.9% in a BSFL production system based on kitchen biowaste, which can be related to the superior nutrient content of kitchen biowaste compared to the different manure types. The reason BCR values are considerably lower than FCE values is the fact that the BCR considers the total amount of provided feed substrate as the numerator, whereas the FCE only accounts for the ingested feed substrate.
The numerical data on DMR, WRI, FCE, and BCR extracted or recalculated from the literature can be found in Table S6 in the Supplementary Material.

3.4. Nitrogen Reduction

The nitrogen reduction percentage is an indicator that compares the nitrogen contents of the feed substrate and the residual frass, with the difference being the N reduction [41]. The indicator is calculated as follows:
N red. (%) = (1 − (N1 − N2)/N1) × 100,
where N1 is the nitrogen content in the feed substrate before rearing, and N2 is the nitrogen content of the residual frass after rearing [41].
Twenty-nine of the reviewed BSFL production systems reported values for the N reduction or the necessary data to recalculate it. The overall range across all feed substrate groups was 22.1–82.1%, with a mean value of 50%. The values are comparable to the findings of Zhang et al. [97], who described a BSFL production system utilizing different mixtures of bioflocs and wheat bran and reported a mean N reduction of 49%. Similarly to the DMR (see Section 3.3.1), no considerable differences could be found across the feed substrate groups (Figure 5). A reported shortcoming of this indicator is that it does not differentiate between N that is converted into larval protein after ingestion and N that is lost in the valorization process either directly from the feed substrate (i.e., manure) or via microbial-related fermentation processes in the larvae guts [87]. This issue was recently addressed by Parodi et al. [6], who conducted BSFL-rearing trials on pig manure mixed with NH4Cl in two different treatments and constructed a complete NH3-N mass balance of the rearing process using the stable 15N ammonium isotope in NH4Cl as a tracer to quantify the incorporation of NH3-N into larval protein. The results indicated that, of the overall N reduction of 46 and 48%, only 27 and 25% were attributable to larval protein gain, whereas the remaining 19 and 23% were losses [6].
The numerical data on N reduction extracted or recalculated from the literature can also be found in Table S6 in the Supplementary Material.

4. Conclusions

This review identified 75 BSFL production systems across heterogeneous geographical contexts in different climate zones utilizing various livestock manure or manure/waste/by-product mixtures as feed substrates to be valorized by multiple different BSFL strains with their unique phenotypic plasticity. The review also highlighted considerable differences in production system design regarding the different production steps, their specific characteristics, and feed substrate preparation. These differences lead to a wide spectrum of rearing performances, which can be measured by a suite of indicators depending on the goals of the respective systems. Regarding bioconversion efficiency, BSFL production systems are commonly evaluated in terms of dry matter reduction (DMR), waste reduction index (WRI), feed conversion efficiency (FCE), and bioconversion rate (BCR), whereas the nitrogen reduction indicator was frequently used to determine the nitrogen efficiency of reviewed systems.
Although the feed substrate and especially its nutrient contents were shown to have considerable influence on the rearing performance, contradicting results were also reported, highlighting the importance of different parameters such as the utilized BSFL strain as well as an optimal system design, including larvae nursing, feed preparation, and climate control. Based on the results of this review, an optimal BSFL production system utilizing livestock manure should consider the following production steps and characteristics:
  • Establishing an adult BSF colony from a strain that suits the intended type of fed manure. The adults should be restocked and adequately housed at a temperature of ~27 °C and a relative humidity between 50 and 70% to produce a sustained supply of eggs.
  • After hatching, the neonates should be subjected to a separate larvae nursing step with a high-quality feed substrate (e.g., standard poultry feed). This step requires a slightly higher temperature and humidity (i.e., ~28 °C and 60–80%, respectively) and should be concluded after around six days.
  • Larvae rearing can occur under the same climate characteristics and should utilize a homogenized feed substrate with adequate water content. The rearing step should be concluded with the emergence of the first sixth instar-stage larvae.
  • After harvesting, the BSFL should be further processed according to their desired use. In case of subsequent use as livestock feed, an additional purging period after harvesting (between 24 and 48 h) is highly recommended to reduce the risk of biological hazards.
The review results further show that, to date, the vast majority of BSFL production systems that valorize livestock manure are operated at the micro-scale level (i.e., in laboratory settings). However, the increasing worldwide number of legally binding commitments toward reducing environmental impacts (e.g., greenhouse gas emissions) from livestock production and the potentially beneficial contribution of manure valorization using BSFL will likely necessitate large-scale systems at the farm or industrial level. Thus, further research should focus on the comprehensive assessment of the potential environmental impacts of manure valorization using BSFL compared to conventional manure application and other alternative scenarios, such as gasification or anaerobic digestion. Remaining knowledge gaps regarding assessing biological and chemical hazards associated with rearing feed inputs (i.e., BSFL) on manure and their potential impacts on animal and human health also merit further attention.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/su151612177/s1. Table S1: Adult fly housing, temperature, relative humidity, and oviposition substrate of the 53 described egg production systems relying on adult colonies; Table S2: Nursing substrate, temperature, relative humidity, means of climate control, and nursing period of the 55 described larvae nursing systems; Table S3: Harvest stage, temperature and relative humidity, utilized rearing devices, development time, and harvesting process steps of the 75 reviewed larvae rearing systems; Table S4: Components and nutritional composition of the feed substrates used in the 75 reviewed BSFL production systems; Table S5: General feed substrate composition and preparation steps reported in the reviewed BSFL production studies; Table S6: Dry matter reduction, waste reduction index, feed conversion efficiency, bioconversion rate, and nitrogen reduction of the reviewed BSFL production systems.

Author Contributions

Conceptualization, F.G. and J.F.; methodology, F.G. and J.F.; investigation, F.G. and J.F.; writing—original draft preparation, F.G.; writing—review and editing, N.P.; visualization, F.G.; supervision, N.P.; funding acquisition, N.P. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by funds from the Natural Sciences and Engineering Research Council of Canada (NSERC) and Egg Farmers of Canada (EFC) through the Industrial Research Chair in Sustainability.

Institutional Review Board Statement

Not appliable.

Informed Consent Statement

Not appliable.

Data Availability Statement

Not appliable.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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Figure 1. Flowchart of the systematic review to identify relevant peer-reviewed original research articles according to the PRISMA methodology [49,50].
Figure 1. Flowchart of the systematic review to identify relevant peer-reviewed original research articles according to the PRISMA methodology [49,50].
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Figure 2. (A) Geographical context and (B) utilized BSFL strains of the 75 reviewed BSFL production systems.
Figure 2. (A) Geographical context and (B) utilized BSFL strains of the 75 reviewed BSFL production systems.
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Figure 3. Boxplots of the nutritional composition of the different feed substrate groups (i.e. (A) dry matter (DM) content, (B) total organic carbon (TOC) content, (C) nitrogen (N) content, and (D) phosphorous (P) content). Feed substrates of the groups “chicken manure”, “cattle manure”, “pig manure”, “horse manure”, and “sheep manure” contain ≥ 50% dry matter of the respective manure type, whereas feed substrates from the group “others” contain ≥ 50% dry matter of waste products or by-products. Symbol ° shows the individual data points, and × indicates the mean value.
Figure 3. Boxplots of the nutritional composition of the different feed substrate groups (i.e. (A) dry matter (DM) content, (B) total organic carbon (TOC) content, (C) nitrogen (N) content, and (D) phosphorous (P) content). Feed substrates of the groups “chicken manure”, “cattle manure”, “pig manure”, “horse manure”, and “sheep manure” contain ≥ 50% dry matter of the respective manure type, whereas feed substrates from the group “others” contain ≥ 50% dry matter of waste products or by-products. Symbol ° shows the individual data points, and × indicates the mean value.
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Figure 4. Boxplots of the (A) dry matter reduction (DMR), (B) waste reduction index (WRI), (C) feed conversion efficiency (FCE), and (D) biomass conversion ratio (BCR) of the reviewed BSFL production systems differentiated by feed substrate group. Feed substrates of the groups “chicken manure”, “cattle manure”, “pig manure”, “horse manure”, and “sheep manure” contain ≥ 50% dry matter of the respective manure type, whereas feed substrates from the group “others” contain ≥ 50% dry matter of waste products or by-products. Symbol ° shows the individual data points, and × indicates the mean value.
Figure 4. Boxplots of the (A) dry matter reduction (DMR), (B) waste reduction index (WRI), (C) feed conversion efficiency (FCE), and (D) biomass conversion ratio (BCR) of the reviewed BSFL production systems differentiated by feed substrate group. Feed substrates of the groups “chicken manure”, “cattle manure”, “pig manure”, “horse manure”, and “sheep manure” contain ≥ 50% dry matter of the respective manure type, whereas feed substrates from the group “others” contain ≥ 50% dry matter of waste products or by-products. Symbol ° shows the individual data points, and × indicates the mean value.
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Figure 5. Boxplots of the nitrogen reduction of the reviewed BSFL production systems differentiated by feed substrate group. Feed substrates of the groups “chicken manure”, “cattle manure”, “pig manure”, “horse manure”, and “sheep manure” contain ≥ 50% dry matter of the respective manure type, whereas feed substrates from the group “others” contain ≥ 50% dry matter of waste products or by-products. Symbol ° shows the individual data points, and × indicates the mean value.
Figure 5. Boxplots of the nitrogen reduction of the reviewed BSFL production systems differentiated by feed substrate group. Feed substrates of the groups “chicken manure”, “cattle manure”, “pig manure”, “horse manure”, and “sheep manure” contain ≥ 50% dry matter of the respective manure type, whereas feed substrates from the group “others” contain ≥ 50% dry matter of waste products or by-products. Symbol ° shows the individual data points, and × indicates the mean value.
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Grassauer, F.; Ferdous, J.; Pelletier, N. Manure Valorization Using Black Soldier Fly Larvae: A Review of Current Systems, Production Characteristics, Utilized Feed Substrates, and Bioconversion and Nitrogen Conversion Efficiencies. Sustainability 2023, 15, 12177. https://doi.org/10.3390/su151612177

AMA Style

Grassauer F, Ferdous J, Pelletier N. Manure Valorization Using Black Soldier Fly Larvae: A Review of Current Systems, Production Characteristics, Utilized Feed Substrates, and Bioconversion and Nitrogen Conversion Efficiencies. Sustainability. 2023; 15(16):12177. https://doi.org/10.3390/su151612177

Chicago/Turabian Style

Grassauer, Florian, Jannatul Ferdous, and Nathan Pelletier. 2023. "Manure Valorization Using Black Soldier Fly Larvae: A Review of Current Systems, Production Characteristics, Utilized Feed Substrates, and Bioconversion and Nitrogen Conversion Efficiencies" Sustainability 15, no. 16: 12177. https://doi.org/10.3390/su151612177

APA Style

Grassauer, F., Ferdous, J., & Pelletier, N. (2023). Manure Valorization Using Black Soldier Fly Larvae: A Review of Current Systems, Production Characteristics, Utilized Feed Substrates, and Bioconversion and Nitrogen Conversion Efficiencies. Sustainability, 15(16), 12177. https://doi.org/10.3390/su151612177

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