1. Introduction
Entomophagy, meaning consumption of insects, has been practiced by humans on every inhabited continent, not only historically [
1,
2,
3], but also up until the present day [
4,
5,
6,
7]. Insects play a more prominent role in the cuisines of some contemporary cultures [
8], while in others they are seen as taboo or at least unappetizing [
9]. Over the past century, however, starting perhaps with Holt’s [
10] essay, “Why Not Eat Insects?”, discussion of the role insects should play in modern, urban, and/or Western food culture has increased [
11]. Consumers without longstanding traditions of entomophagy are displaying a growing awareness that insects are edible and have benefits over other foods, and are showing greater interest in trying edible insect dishes [
12,
13,
14,
15], either out of curiosity [
16], ecological concerns [
17], or other reasons [
18]. Interest in entomophagy has reached a point where the supply of insects cannot keep pace with the demand [
13,
19], and some edible species are already under threat of overexploitation [
6]. International conferences have been held [
6,
20,
21,
22] and cookbooks published on the subject [
23,
24,
25,
26]. Particular attention has been paid to the potential of edible insects as a solution to present or looming food crises [
27,
28,
29], in particular fears of global food insecurity due to climate change and/or rising populations [
30,
31].
Besides being delicious when prepared properly, insects are rich sources of proteins, good fats, and certain trace elements. Their greatest advantage over other animal meats, which underlies their frequent championing as saviors in a food-insecure world, is their lower environmental impact. Insects have a lower feed-to-protein conversion ratio than cattle or swine [
32] and even poultry according to some sources [
31], and produce fewer greenhouse gases and lower ammonia emissions than any conventional livestock [
31,
33,
34]. Industrial-scale insect farms need less water and land space than pasture [
35], can have a lower water footprint per gram of protein than any conventional livestock or even milk and eggs [
36,
37], and some insect species can even consume organic waste and side-streams [
29,
31]. Thus insect rearing can operate in developing countries that need low-tech and low-capital investment, yet can still be done with high technology and automated methods to produce consistent, safe, high-quality products [
20]. Insects can also improve the environmental footprint of vertebrate meats indirectly, through their use as feed [
38,
39]. Rearing insects on human-inedible wastes and feeding them to larger food animals (whose wastes can even be fed to the insects in a partly closed circle of food energy) can boost the protein content of these animals [
40] and is more environmentally friendly and efficient than growing fields of grains or other feeds, which use land and resources that could otherwise be used to grow food for humans [
31].
One known problem with industrializing edible insects today, however, is the relative dearth of insects to choose from. While thousands of species are consumed worldwide [
29], all but a dozen or so are wild caught by more traditional societies and cannot at this time be farmed, with consequences for regular supply and for conservation [
41,
42]. The species commonly sold and consumed in the West, such as house crickets and mealworms, are thus not necessarily the most sustainable species nor those with the most desirable organoleptic properties such as taste and texture. Several authors have noted that, if done improperly, entomophagy can be environmentally destructive rather than helpful [
27,
41]. Insects that are difficult to rear or harvest and thus in lower supply would also be more expensive, lowering their desirability among most consumers; and of course the issue of flavor in food acceptance cannot be understated. Rearing insects on otherwise inedible organic wastes would greatly lower their environmental footprint and boost their utility, in particular for developing world consumers. An added benefit is the recycling of the waste itself, as the management of organic wastes such as manure, leachates, and food waste is both costly and a growing environmental concern [
43]. Rearing edible insects on wastes would solve two problems at once [
44], but popular species like cricket and mealworm cannot be reared easily on most waste, especially animal products. A need exists, therefore, to identify and refocus attention on species with superior cultivation properties than extant edible insect species, but which can still be used either as feed or food.
The black soldier fly,
Hermetia illucens, is a true fly (Diptera) of the family Stratiomyidae. Though originally native to the Americas, it now occurs worldwide in tropical and temperate regions [
45,
46], and its lack of hardiness to the cold precludes its invasion of nonnative regions such as Northern Europe [
47]. Adults consume nothing but water, do not approach humans, do not bite or sting, and do not vector or disseminate any specific diseases [
46,
48]. Black soldier fly larvae (BSFL) are reported as feeding on an immense variety of organic material, and have already been used in small-scale waste management purposes using substrates such as manure [
49,
50], rice straw [
51], food waste [
52], distillers’ grains [
53], fecal sludge [
54,
55], animal offal, kitchen waste, and so on [
56]. The diversity of substrates they can process and the efficiency with which they do so may be the highest among the flies [
57]. BSFL are also edible, and have been studied as such. Their feed conversion ratios are known to be superior to both crickets and mealworms, and, compared to those two, BSFL survival rate and nitrogen and phosphorus compositions do not vary as highly with diet [
32]. They are not thought to be toxic [
58]. BSFL accumulate lipids from their diet for use as energy by the non-feeding adult, to the point that they can be converted to biodiesel [
59,
60,
61,
62]. What they do not consume, combined with their nitrogen-rich frass, can be used as fertilizer [
52,
63]. Their larval development time of over three weeks is longer than that of flies such as house and carrion flies (<5 days), meaning a single larva will consume a larger amount of substrate and produce larger pupae [
46]. Additionally, when BSFL are at the pre-pupa stage, they will instinctively leave the substrate and move to a high, clean place, a behavior called “self-harvesting” that removes an otherwise labor-intensive step from their farming [
45,
64]. All these benefits make BSFL practical to rear and a suitable tool to valorize wastes, plus possibly a sustainable animal feed or human food source. Here we review the literature on the black soldier fly to evaluate its suitability for use in human food systems.
3. Discussion
Black soldier fly is indeed one of the nearly 2000 species of insects already consumed by humans in entomophagous cultures, but is neither popular nor common, with contemporary consumption limited to one ethnic group that is increasingly abandoning the practice [
162,
165]. This matches reports for insects around the world: entomophagy is primarily practiced by more rural and traditional cultures (“primitive” people) rather than urbanites, and is decreasing in popularity among these people over time as urbanization and Westernization take over [
13,
33,
170].
H. illuscen’s tendency to colonize unpalatable and biohazardous wastes such as manure likely explains why it is not consumed as widely as it is geographically located, as care would be needed to clean the prepupae sufficiently. This saprophagy also means that most people’s image of BSFL, if they have any, would be as maggots that infest highly inedible dung and waste, meaning that, by the anthropological law of contagion (“once in contact, always in contact”), the larvae will always be seen as highly inedible, even if they were reared on a non-waste substrate and sterilized before cooking [
171,
172]. This issue affects insects in general, but for a known saprophage the effect is arguably rational, as they really might be pathogenic to eat. Research has confirmed that, for Western and non-Western consumers alike, insects associated with waste are seen as the most disgusting and least potentially edible, even if consumers know the insect dishes presented to them are safe to eat [
173]. These factors, combined with the odor and taste issues associated with waste, similarly explain why the ubiquitous house fly (Muscidae) and blow fly (Calliphoridae) maggots are not typically consumed. The exception that proves the rule is the Sabah case, where the BSFL consumed are those found infesting the same food (
tapai feedstock made of cassava or rice) with which they are eaten. By the same law of contagion, the flies are seen as similarly edible as the
tapai. BSFL here are consuming a food-quality substrate, which normalizes their edibility (and would also allow for the legal use of these larvae as feed under U.S. law). A good parallel would be
Piophila casei (Diptera: Piophilidae), the cheese skippers, which colonize human food as well as old human cadavers [
174]. Though not reared directly for human consumption, other than another ambiguous record in Ramos-Elorduy 1997 [
162,
163], and never consumed off the dead, they are an example of edible entomology in the form of
casu marzu, a Sardinian cheese fermented to the point of decomposition and colonized by these maggots, which are only ever consumed along with the cheese (a practice that skirts EU food laws) [
158]. For both the cheese skipper in Sardinia and the black soldier fly in Sabah, the larvae are only ever eaten with the same food item on which they were found. The same larvae harvested off of waste would not be consumed.
Regardless, one must conclude that humans can and do eat BSFL in some situations. Whether BSFL should be an insect of choice for commercial insect rearing for human food is the main question raised by our review. Nutritionally, BSFL are acceptable for human feeding. The main concern from studies on BSFL as fish or poultry feed was reduced performance when used as the sole food source due to low palatability or nutritive content relative to other diets: many, though not all [
82], studies recommended BSFL be used only as a partial meal replacement [
175]. This concern is somewhat moot in humans: as omnivores, the idea of using BSFL or any other insect (or any other animal or plant organism, for that matter) as a sole source of human nutrition is not seriously considered. BSFL have one of the least healthful fatty acid profiles compared to other insects, based on our current opinions of which fatty acids are considered healthful. Interest in lowering rates of human cardiovascular disease would suggest BSFL as an unfavorable insect food relative to others due to this high saturated fat content, although one makes an assumption about future human food preferences in predicting that consumers will be choosy over which insects they eat. Defatting the insects may be essential for the commercial preparation and marketing of BSFL as a healthful alternative to animal meat, although this adds a step and cost to the processing of the insect that would need to be factored into environmental and economic analyses of BSFL rearing practicality. The importance of the substrate in determining the fatty acid profile in BSFL means some of the most desired waste biomass inputs, such as fish offal, may naturally mitigate the fatty acid problem. More data correlating substrate type to nutrients in the larvae are needed. From a sensory perspective alone, studies have found that lower (more healthful) ratios of monounsaturated to polyunsaturated fats beyond a certain threshold are associated with negative odor, texture, and flavor profiles [
176,
177,
178,
179]. Thus, though perhaps less nutritionally favorable, BSFL might be tastier than other insects. The high levels of saturated fats in mammal meat, poultry skin, and dairy products have not stopped these foods from being accepted in human diets. Note also that the high amounts of medium-chain saturated fatty acids and low amounts of polyunsaturated fatty acids found in BSFL, while not ideal for human health, are ideal for biodiesel fuel production, suggesting that BSFL reared on waste may be even better suited as fuel than food [
100]. Research on commercial-scale biofuel production from waste-fed saprophagous insects and its economic and environmental sustainability are a worthy topic for further exploration.
Regarding flavor and mouthfeel, the texture of BSFL is not significantly different from other larvae, but at this time no sensory profile tests have been done on BSFL-derived food. The issues of flavor and texture do not get the attention they deserve in entomophagy texts: the assumption that insects will be accepted as meat substitutes once the taboos of eating insects are overcome ignores the problem that insects do not taste or feel like meat [
156,
173,
180]. BSFL in particular are most frequently compared to fish meal and oil, albeit with an earthier flavor. Note that one need not always think of what extant foods a novel food tastes like, and instead should consider that an insect tastes like an insect and prepare/market it accordingly [
156]. The texture issue is more prominent in insects with hard exoskeletons like crickets, but appears to be less important in the soft-skinned BSFL. Fish meal is not a major ingredient in human cuisine, but pureed fish is used to make fish balls in East Asia and Scandinavia, and such
surimi-type products (“textured insect protein”) might indeed be a successful way to prepare BSFL or other insects for human consumers, assuming the flavor is acceptable. The advantage this formulation has is that it hides the insect origin. Many have reported, to the point of it becoming a consensus, that the best way to convince people in cultures unused to entomophagy to add insects into their diet is to disguise the insect as much as possible, with grinding the insects to a powder being the ideal method [
14,
15,
181]. Powdered/ground insects can be easily added to baked goods and processed meats [
3,
182]. This should also work to introduce a typically unappetizing insect to people who eat other insects readily, as different entomophagous cultures are not united in their food choices, but see different types of insects as delicacies or disgusting [
25]. People surveyed also seem to prefer meat products that are part-insect, part-conventional livestock meats as opposed to all insect or all vegetable meat alternatives [
183]. Insect meal has various uses, such as fortifying baked goods for extra protein (a ratio as high as 50/50 grain: insect meal has the same baking performance as pure flour), formulation into protein bars, or use in ground animal meat substitutes [
184]. More creative ways to process insects are currently being researched, which can shape the direction of the industry greatly [
33,
182]. For the more adventurous, dried BSFL could be a snack item suitable for eating like peanuts and salted crackers as an accompaniment to beer or other light alcohols, like fried grasshoppers in Mexico (
chapulines) [
185] or, indeed, like raw BSFL in Sabah [
164]. This use of insects as a snack rather than a vertebrate protein substitute for main courses does not meet any environmentalist goals, however, but just adds insects to the diet for novelty without any nobler reason [
156]; not that there is anything wrong with that [
186].
Under the paradigm of insects as an alternative protein to mitigate the effects of climate change or rising populations,
H. illuscen’s advantages might reasonably put it as the insect of choice among the pantheon of 1 million species: not only does it not compete with humans or livestock for food, have specialized diets, or require significant environmental manipulation [
187], but also it provides an economic and ecological service in processing the waste substrates that it feeds on. No other insect comes close to closing so many material flow loops and creating nearly self-sustaining food production cycles as BSFL, effectively making BSFL rearing on wastes a self-financing form of pollution reduction [
188,
189], although it is not yet known what are the best ratios of insects to substrate and what conditions will provide the optimal mix of larval production and waste recycling. BSFL thus show strong promise as part of a sustainable system with hydroponics or composting and aquaculture or poultry farming [
93,
190,
191], particularly in situations where food choices would be extremely limited, such as space travel [
190,
192] or the most pessimistic global food insecurity crises envisioned by population growth extrapolation [
30]. Pilot projects to this end are already underway, such as the “Insect-based Feed and Fertilizer Production” project co-run by the Swiss Research Institute of Organic Agriculture and the University of Ghana [
191]. However, the present legal restrictions on using waste-fed BSFL as livestock feed in the USA and EU mean BSFL cannot presently be legally used to close nutrient loops, but rather to recycle the nutrients from wastes into another form, such as compost or biodiesel. BSFL’s use as feed or food hinges on changes in these regulations, which in turn depend on positive results to safety testing.
Saprophagy has economic and ecological advantages but a cultural disadvantage: the idea of eating an insect that feeds on waste, like a cockroach or blowfly, simply comes with too much of a taboo [
173]. Beyond preconceived expectations of bad flavors, people may still feel consuming insects that fed on animal biosolids is hazardous to one’s health, and the extant laws reflect these concerns. Though the flies have a strong record of reducing microbial and chemical contamination from their substrates, and microbial issues can be dealt with during insect production and processing [
124], the possibility of something unpleasant remaining in their gut between self-harvest and final processing exists. While manure is not considered a reservoir for prions that cause diseases such as bovine spongiform encephalitis or scrapie, there is currently no data on the fate of prions in slaughterhouse wastes processed by BSFL [
193]. Insects are definitively not biological vectors or amplifiers of prions [
114,
194,
195], but experiments with the corpse fly
Sarcophaga carnaria fed brains from scrapie-infected hamsters found that healthy hamsters can become infected after eating these fly larvae [
195]. Evidence of absence would be more comforting to consumers and regulatory agents than absence of evidence, so this should be a priority research topic before BSFL fed slaughterhouse biomass can be legally fed to other organisms. Pending such data, the European Food Safety Authority recommends insects used as animal or human feed not be fed manure or certain ruminant meat substrates, some of which are already excluded from the food chain due to their risk of transmitting prion diseases. They also note that thermal treatment can deactivate prions as well [
114].
Beyond manure and feces, reports exist of BSFL colonizing human cadavers in advanced stages of decay [
196,
197,
198,
199], and pig cadavers as early as a week [
200]. It is hard enough to convince people to eat grasshoppers, which, as entomophagy promoters love to argue, are farm-raised and eat the same food as cows do. To eat an insect whose diet includes garbage, dung, and even the dead may be too difficult a pill to swallow, even though other saprophagous arthropods—crabs and lobsters—are readily consumed. Insect foods, including BSFL, are already associated with rurality and primitiveness [
33,
164]. The risk is that BSFL, perhaps more than insects in general, will be labeled a “starvation food” [
201] or “food of attrition” [
156]: something not eaten for its own organoleptic properties, but because humanity has no alternative. Global warming and overpopulation are thus depicted as societal crimes whose punishment is reducing humanity to eating things that most people would otherwise find objectionable [
202]. Unfortunately, this pessimistic view is exactly how BSFL and other insects have been primarily marketed for human consumption in the West: with a focus on their sustainable production rather than flavor or cost, which are the greater factors driving what people choose to eat [
14,
154,
186].
Such marketing of insects as sustainable is itself problematic, as other protein alternatives to livestock exist that are even more sustainable. This includes soy and other vegan protein sources, as well as future foods such as algae and lab-reared meat [
17,
203]. Plant proteins have a lower carbon footprint than BSFL and are better for human cardiovascular health due to their superior fatty acid profiles. However, BSFL have an edge over plant proteins in terms of the greatly reduced land and water requirements for their rearing, as well as their ability to recycle wastes. BSFL are no substitute for plants sensu lato in the human diet, but per gram protein may prove to be more sustainable to produce than plant protein due to the low input costs. Of all extant protein production industries (other than hunting and fishing), BSFL rearing could prove to be the most sustainable. It absolutely has a place in the future, both as a waste recycler and as animal feed. The biggest obstacle may be a regulatory/legal one: extant laws on BSFL as animal feed explicitly forbid the use of “wastes” as substrate for BSFL feeding, which immediately places limitations on BSFL rearing. Luckily, these laws (themselves less than two years old at the time of this paper’s publication) can and do change following the efforts of lobbyists armed with new research results. The biggest such research questions remaining are just how much protein and fat is produced per kilogram waste fed into a BSFL bioreactor per insect, how can BSFL be safely decontaminated if reared on a waste substrate, and whether their fatty acid profiles or palatability issues compromise their economic value as a feed substitute.