It is estimated that by 2030, USA’s agricultural production and industrial processing of food will generate between 145 and 602 gigatons of organic waste annually (Perlack et al. 2005; Turhollow et al. 2014). Assuming a population of 359.4 million (Colby and Ortman 2017), this amounts to approximately 4.5 kg per day per person! Food wastes are often differentiated as either pre- or post-consumer waste, with the former including waste streams derived from losses incurred during growth, harvest, transport, processing, and storage (Parfitt et al. 2010). Conversely, post-consumer wastes are derived from losses incurred at the consumer level, including over- or inappropriate purchasing, storage, preparation, portioning, and cooking (Parfitt et al. 2010). While post-consumer food waste is certainly a global concern, this review treats only pre-consumer organic wastes, as they are often less covered in reviews of insect bioconversion (Surendra et al. 2016; Wang and Shelomi 2017; Diener et al. 2011; Čičková et al. 2015), do not have the same regulatory and health concerns (Codex Alimentarius Commission 2014), and are more chemically and physically diverse (Parfitt et al. 2010). Specifically, pre-consumer organic wastes are by-products in the food supply chain based on materials not designated for human consumption, and they include (1) non-marketable but edible food (damaged and misshapen); (2) food spoilage at production sites; (3) by-products from primary food processing, including stems, leaves, hulls, seeds, skins, and pulps generated from cleaning, de-hulling, pounding, grinding, packaging, soaking, winnowing, drying, sieving, and milling; (4) by-products from secondary food processing—the cuttings, crumbs, and remains generated from mixing, cooking, frying, molding, cutting, and extrusion (Parfitt et al. 2010); and (5) non-food post-harvest by-products associated with orchard and field crops—the chips, slash, wood, fibers, and stovers (Hoogwijk et al. 2003) (Fig. 1).
Each combination of crop and its method of production, processing, packaging, storage, and distribution generates a unique set of pre-consumer organic wastes. For example, residuals from pre-consumer processing of fruit and vegetables for juice can include leaves, peels, pulps, and seeds (Rezzadori et al. 2012), each with different chemical and physical properties. With over 6000 crop species in production globally (Hanelt 2001), and a wide range of processed goods, the diversity of organic waste streams is immense (Colby and Ortman 2017). Despite growing legal restrictions, some pre-consumer organic wastes are still disposed in landfills and considered a problem rather than an economic opportunity (Lou and Nair 2009). Disposal of pre-consumer organic wastes in compost and landfilling operations generate considerable greenhouse gas emissions and other environmental pollutants (Eriksson et al. 2015; Schott et al. 2016). Therefore, developing innovative ways to use pre-consumer organic wastes is important for reasons of material efficiency and product development as well as pollution prevention and economic gain. Currently, about 3.73 billion hectares, a staggering ~ 75% of the planets arable land!, is dedicated to livestock grazing (Foley et al. 2011), and the demand for meat is expected to grow 58% by 2050 (McLeod 2011). Consequently, there is a dire need for alternative sources of proteins and fats to meet the growing human demand, and use of insect biomass represents an opportunity to meet this growing demand. The potential of using insects to produce proteins and fats is of particular interest when tied directly to development of more sustainable waste management practices. Moreover, pre-consumer organic wastes can be consumed as a feedstock by insects, which “bioconvert” the waste into valuable products (Wang and Shelomi 2017; Smetana et al. 2016; Oonincx and De Boer 2012; Vantomme et al. 2012).
The production of pre-consumer organic wastes may be considered a waste problem, but they also represent potentially significant resources and business opportunities due to their richness in nutrients and active compounds (Brar et al. 2013). An illustrative example of this type of transformation is how whey protein from cheese production represented a major problem for the diary industries up until the 1980s, with farmers paying for disposal or reuse as fertilizer. In recent years, the protein powder industry has recognized the value of whey and is now willing to pay for this high-value protein source. Moreover, novel markets and industries may emerge through innovative utilization of existing organic “waste products” and in the process eliminate waste streams and create jobs and industries. Other examples include use of organic wastes as substrate for mushroom production, compost, energy production, or fillers in animal feed (e.g., insect biomass) (Surendra et al. 2016; Lou and Nair 2009; Kusch et al. 2015; Kabongo 2013; Lim et al. 2016; California Biomass Collaborative 2012; Zweigle 2010).
Similar to conventional livestock production, the insects themselves can be commercialized as bulk biomass to be added to animal feed or human food, and/or specific compounds can be extracted from their biomass for industrial, pharmaceutical, or energy (biofuel) purposes, such as proteins and fats (Surendra et al. 2016; Wang and Shelomi 2017; Kagata and Ohgushi 2012). In addition, the left-over material [insect molts and feces (frass) and left-over waste material] may be processed and commercialized as high-value soil amendments. Current insect bioconversion facilities have the capacity to accept as much as 250 tons of food waste per day (www.agriprotein.com), so development and adoption of insect-based waste management solutions is not a thing of the future but unfolding and gaining momentum. A crucial aspect of large-scale use of insects as bioconverters of pre-consumer organic wastes is their “bioconversion rate,” which is a quantitative measure of the input:output ratio (Oonincx et al. 2015; Wilkinson 2011; Lundy and Parrella 2015). The bioconversion rate can be measured based on a number of variables, including energy, protein, and fat, and a low bioconversion rate implies high efficiency. In livestock nutrition, it is common to calculate the bioconversion rate based on the nutrient or energy content of feed material compared to the nutrient or energy content of meat or milk produced (Wilkinson 2011). Such a calculation is partially incomplete, as considerable energy, fertilizer, labor, and other inputs often were used to produce and process the feed materials. We are unaware of any direct comparisons of bioconversion rates of insects and typical livestock animals. That is, to accurately compare their conversion rates, the exact same feed material should be given to insects and, for instance, cows or chicken, and their growth in biomass as well as their production (eggs and milk) should be quantified. Without such true comparisons, it is difficult to accurately compare bioconversion rates. Regarding conversion rates of insects versus traditional livestock, it is also important to emphasize that entire insect bodies can typically be used, while only the meat from vertebrate livestock is commercialized. Thus, the proportion of usable biomass (compared to bines, hides, internal organs, etc. in vertebrate livestock) is generally markedly higher for insects. Finally, the protein content of insects, such as houseflies (Musca domestica), mealworms (Tenebrio molitor), and crickets (Acheta domesticus), is typically 40–70% (Makkar et al. 2014). For comparison, the protein content of a whole chicken or cow is typically ~ 55% and ~ 40%, respectively (Van Huis 2013). Thus, from a bioconversion standpoint, there are strong arguments for focusing on insects as bioconverters of our current and future pre-consumer organic wastes.
In this review, we argue that development, use, and commercialization of tailored/customized insect-microbial systems to specific pre-consumer organic wastes are at the brink of becoming a serious and profitable business sector and also an accepted research discipline. Moreover, we show that insects (and their gut microbials) can and will play a major role in the development of sustainable management plans for pre-consumer organic wastes. We review this exciting area from the perspectives and applications of evolutionary and ecological theory to insect breeding.
Natural selection may be defined as the process, in which variable and heritable fitness-promoting traits are selected for within a population of a given species to increase the fitness of individuals in the following generations (Endler 1986). In nature, complex community interactions drive natural selection, and these interactions are underpinned by spatio-temporal dynamics of the given environment. Consequently, “artificial selection” of insects is defined as deliberate anthropogenic control and manipulation of selection forces to promote a particular evolutionary outcome (optimization of an insect population to serve as bioconverter of a specific organic waste product) (Zeder 2012; Meyer et al. 2012). While modern phenotypes (observable traits) of only a few insect species are regarded as the outcome of artificial selection (i.e., domesticated honey bees (Apis mellifera L.), flightless mulberry silkworm (Bombyx mori L.), and resinous lac bug [Kerria lacca (Kerr)] (Melillo 2013)), the potential of artificial selection to improve insect lineages has been discussed for decades (Hoy 1976). In addition, this endeavor is greatly facilitated by copious research and development in the mass rearing of insects, (Ortiz et al. 2016) with notable examples including production of sterile insects and natural enemies for biocontrol, (Dyck et al. 2006) production of medically important species for research, and insect biomass for animal and human consumption (Wang and Shelomi 2017; Salomone et al. 2017). However, the recent recognition of insects as potential bioconverters of pre-consumer organic wastes is a new and exciting area. Moreover, progress in use of insects for bioconversion of wastes will benefit, if mass rearing insects is viewed through a particular lens, (Jensen et al. 2017) in which evolutionary processes and gut microbe-host interactions play major roles.
The “ideal insect bioconverter”
As decomposers and herbivores, the diversity of insect species includes groups that are highly specialized in their ability to thrive on different organic substrates and under specialized environmental conditions (Futuyma and Agrawal 2009). Moreover, some natural host substrates resemble pre-consumer organic wastes, in terms of moisture content, digestibility, and nutritional composition (Smetana et al. 2016). In addition, insect functional diversity (the behavioral and the ecological services they provide) can be exploited to substitute mechanical and/or chemical steps in conventional waste processing,(Li et al. 2015) such as using beetles larvae maceration to feed around and remove the seeds. Insect species that exhibit innate biological compatibility with target pre-consumer organic wastes, and/or possess an exploitable functional service, can then be further improved via artificial selection (targeted breeding). In this way, specific insect species with distinct traits (i.e., physiological, microbial, behavioral) can be bred to function as the “ideal insect bioconverters” for a target waste stream.
Here, we consider candidate “ideal insect bioconverters,” as those that possess as many of the traits listed in Table 1 as possible. Certainly, no incipient bioconverter species or population will possess all these traits initially, but a strain of insects subjected to targeted breeding may ultimately gain a unique potential for bioconversion of a particular waste stream at a large scale (Jensen et al. 2017). Considering the sizeable literature on insects undergoing rapid adaptation in nature, including adapting to new foods, (Carroll and Loye 2012; Carroll et al. 1998) ecological communities, (Strauss et al. 2006) pesticides, (Tabashnik 1994) and experimental evolution in the laboratory, (Beldade et al. 2005) it is reasonable to predict targeted breeding programs could rather rapidly and cost-effectively yield new and significantly improved bioconverters in manageable and economically practicable time frames.
Insect species currently used as bioconverters
At present, only a handful of insect species are used for bioconversion of organic wastes, with the most represented species being (Anankware et al. 2015; Van Huis et al. 2013) crickets, locusts Locusta migratoria, black soldier flies Hermetia illucens, green bottle flies Lucilia sericata, and several mealworm species, including the yellow mealworms Tenebrio molitor (see Table 2 for an extended list). Research on the growth performance and feeding conversion of these species suggests they alone are not sufficient to fully capitalize on the high diversity of unique organic wastes available for bioconversion. For instance, the most utilized bioconverter, the black soldier fly (Fig. 2), has a well-documented capacity to break down wastes, (Surendra et al. 2016; Barry 2004; Diener et al. 2009; Nguyen et al. 2015) which evolved in the context of feeding on nutrient-rich decaying biomass. However, studies have shown that black soldier flies are only marginally suited for bioconversion of low-nutrient fruit and vegetable pulps (Smetana et al. 2016). Similarly, research has shown markedly different performance in feeding efficiency and growth rates of three mealworm species, which were reared on four different organic waste diets of variable starch and protein composition (Van Broekhoven et al. 2015). The authors concluded that certain diets may be unsuitable for mealworms due to a lack of essential nutrients, and that mealworms reared on high-starch diets (49.8% starch; 10.7% crude protein; 1.8% crude fat) had the lowest growth and waste conversion rates.
The role of gut symbionts
An important consideration in the pursuit of ideal insect bioconverters is the prospect of incorporating modern invertebrate microbiome research into targeted breeding programs of ideal insect bioconverters. Studies have shown that invertebrate symbiont interactions are hyper-diverse and critical in facilitating host exploitation of food resources, (Gibson and Hunter 2010; Ceja-Navarro et al. 2015) and that gut symbiont community structures correlate with the chemical composition of the host’s food source (Engel and Moran 2013). For instance, in multiple insect species [including fruit flies (Drosophila spp.), Indianmeal moth (Plodia interpunctella), gypsy moth (Lymantria dispar), and German cockroach (Blattella germanica)], there is a relationship between body protein content and the host’s bacterial diversity (Chandler et al. 2011; Montagna et al. 2016; Mason and Raffa 2014; Pérez-Cobas et al. 2015). While insects are generally considered to be less symbiont rich compared to other animals, such as vertebrates, polyphagous insect species have higher symbiont species richness compared to specialists (Gibson and Hunter 2010). One hypothesis possibly explaining the difference in gut symbiont diversity suggests diverse diets do not require particular symbionts, and therefore, polyphagous hosts benefit from the diversified metabolic capabilities provided by a wider array of symbionts (Montagna et al. 2016). From the perspective of developing ideal bioconverters, monitoring the microbial diversity developing within insect-to-waste pairings will be of high value in the pursuit of optimizing insects as bioconverters.
Experiments discerning how direct manipulations of a host’s gut symbiont community alter host performance and efficiency in bioconverting biomass may yield valuable insight into the bioconversion potential of particular interactions (Scheuring and Yu 2012; Mueller and Sachs 2015). Several strategies may be deployed for direct manipulation of gut microbe-host interactions. First, facultative gut symbionts can be transferred horizontally between target bioconverters, to aid in modulating immunity or accessibility of essential amino acids (Łukasik et al. 2015). Second, organic wastes may be inoculated with beneficial companion bacteria. This practice is already used in part to induce oviposition in black soldier fly, where bioconverted substrate is added to fresh media to make an attractant for gravid females to lay eggs (Nakamura et al. 2016). Likewise, agar inoculated with the bacteria isolated from black soldier fly leads to higher rates of female oviposition, (Zheng et al. 2013). suggesting volatiles emitted from the microbiota of conspecifics mediate oviposition. While these techniques are not a direct manipulation of the gut symbionts per se, cues from the bacteria inform female flies of substrates with microbial communities favorable for larval growth. For example, when chicken manure is inoculated with black soldier fly companion bacteria, the adult body length of flies increases, while the development time from hatching to 90% reaching the prepupual stage is reduced by ~ 5 days (29.00 ± 1.00 days vs. 34.33 ± 3.51 days), (Yu et al. 2011) both valuable improvements for insect bioconversion enterprises. Finally, as interest in bioconversion advances, a bioconverter symbiont community may be manipulated by inclusion of genetically modified symbionts added for custom-made bioconversion applications. To our knowledge, this final strategy has not yet been used in insects used as bioconverters of pre-consumer organic wastes. However, the strategy has been used to reduce transmission of diseases by biting insects, (Taracena et al. 2015) as well as to introduce transgenic gut symbionts to an entire termite colony from only a few initially inoculated individuals (Husseneder and Grace 2005). One could imagine how engineered microbes, perhaps capable of synthesizing more complete amino acid profiles, may assist and add value to insect’s bioconverting nutrient-deficient pre-consumer wastes, such as almond hulls or tomato pomace. In summary, insect-based bioconversion of pre-consumer organic wastes will benefit from comprehensive strategies, those using microbial surveillance and direct manipulations, that incorporate both the health and composition of insect-symbiont relationships. Furthermore, knowledge derived from livestock breeding and other disciplines will be of tremendous value in this effort.
A detailed review by Makkar et al. cites numerous studies of the chemical constituents of insect meals derived from various pre-consumer organic wastes, and lists the insect meals’ nutritional value when consumed by different animal species (Makkar et al. 2014). In addition, many life cycle assessments and protocols have been developed for these insect species for use as animal feed or secondary products (i.e., pharmaceuticals, lubricants, biodiesels) (Ortiz et al. 2016; Jensen et al. 2017; Anankware et al. 2015). Table 2 includes a compiled review of organic wastes and bioconversion outputs for the most commonly cited bioconverting species, as well as other less commonly cited insects.