Are insects a solution for feeding ruminants? Legislation, scientific evidence, and future challenges

Abstract

Insects are promising alternatives to conventional protein and fat sources for ruminants. Legislation is more restrictive for the use of protein-rich insect meals than for insect oils. Insect meals seem to have lower in vitro digestibility than conventional plant meals. Insect products may modulate the ruminal environment (e.g., CH4 emissions and biohydrogenation). The growing interest of the scientific community on the inclusion of insect-derived products in ruminant diets is leading to a boost of research papers on this topic. Even though in absolute terms the increase in the number of published papers is limited—because limited is also the literature on this topic—the scientific production in 2022 equals the scientific production of the former 19 years (about 10 papers published in each above-mentioned time-period). The reason is that insect-derived products are considered not only promising but also sustainable feed ingredients, thanks to the ability of insects to successfully convert relatively low-value agri-food waste into high-quality proteins and fats. The insect crude protein content varies, according to insect stage and processing technology, from 7.5% to 91% (dry matter—DM—basis), while the crude fat values range between 46% and 64% (DM basis) (Finke and Oonincx, 2023). Moreover, their production is characterized by limited environmental footprint. A generalization of their use in ruminant farming could contribute to limit its impact and to move towards a Circular Economy model (Gasco et al., 2020). However, this requires that reality meets expectations. On this basis, in this review we provide information about the state-of-the-art on the use of insects in the nutrition of domestic ruminants, including an overview of the current legislation worldwide and the hitherto known effects of insect-derived products on nutrient digestibility, animal performance, and ruminal biohydrogenation (BH). Following the identified differences in legislative frameworks and the potential application of insect products, information will be provided by dividing them into protein-rich feedstuffs, lipid-rich products (differentiating full-fat meals and free oils), and other insect-derived ingredients for ruminant diets. A major obstacle to evaluating the inclusion of insect-derived products in ruminant diets is represented by the legislation on the potential risk of mad cow disease (Bovine Spongiform Encephalopathy; Renna et al., 2022a). Insect meals are classified as processed-animal-proteins (PAPs) and prohibition on the use currently applies in most high-income countries (e.g., European countries, Japan, and China; Figure 1); contrarily, developing and emergent regions usually lack specific legislation on this issue (Lähteenmäki-Uutela et al., 2017). For example, in different countries in the Americas, only the prohibition of meat meal, blood meal, bone meal, and mammalian offal as raw materials for ruminant feeding was found. At the same time, no explicit ban or authorization was found on the use of insect proteins for the processing, marketing, and use of animal feed (Lähteenmäki-Uutela et al., 2017). Current worldwide legislation framework on the use of insects as feed for ruminants. Under the European Union (EU) Law, insects, and their derived products—excluding live insects—that are intended to be used in animal feed are explicitly considered “animal by-products”. This qualification entails a number of obligations for producers, as defined in Regulation No 1069/2009 and its implementing Regulation No 142/2011—also known as the “EU animal by-products legislation” (IPIFF, 2022). It is promising that EU laws on the use of insects as feedstuffs for monogastrics have been updated in recent years and, since July 2017, it is permitted in aquaculture, and in April 2021, the Standing Committee on Plants, Animals, Food, and Feed approved it for poultry and pig as well. The Regulation No 2001/999 (Annex IV), as amended by Regulation No 2017/893 (Annex X) and Regulation No 2021/1925, allows insect PAPs from several species [namely, black soldier fly (Hermetia illucens L.), common housefly (Musca domestica L.), yellow mealworm (Tenebrio molitor L.), lesser mealworm (Alphitobius diaperinus Panzer), house cricket (Acheta domesticus L.), banded cricket (Gryllodes sigillatus Walker), field cricket (Grillus assimilis), and silkworm (Bombyx mori L.)] in aquaculture, poultry, and pig feeding, as part of the legislation on animal by-products). On a positive note, although the EU prohibits the use of insect-derived PAPs for ruminants, no restriction applies for insect oils. Despite these regional variations in the legal rules governing the use of insects as feed, a clear global interest exists among researchers and feed manufacturers in fostering innovation and research in this sector. In the near future, this may contribute, as occurred for monogastrics, to promote legislative changes that favor the use of insects in ruminant feeding worldwide. Insect meals are considered as promising alternatives to plant proteins commonly used as ruminant feedstuffs (e.g., soybean meal; SBM). As for monogastrics, the first available studies on this topic focused on full-fat insect meals and were conducted in vitro (Table 1). In animal nutrition research, in vitro methodologies allow decreasing the length and cost of experiments, the number of animals used as well as the total time of their use. Of course, information obtained in vivo is the most reliable and therefore in vitro studies are commonly used for preliminary testing, prior to conduct large in vivo trials. Diets containing insect-derived products compared to control diets: impact on nutrient digestibility and ruminal fermentation parameters In an in vitro trial with bovine, Jayanegara et al. (2017a) examined the potential of full-fat H. illucens larvae meals to substitute 50–100% of SBM, the most common protein-rich feed for ruminants, using a 60:40 forage-to-concentrate (F:C) diet as the incubation substrate. The high crude protein (CP) and ether extract (EE) contents of H. illucens larvae meal suggested a suitable use to substitute SBM but decreases in in vitro organic and dry matter digestibility (IVOMD and IVDMD, respectively) were found compared to SBM. Using cannulated sheep as inoculum donors, Renna et al. (2022b) investigated the in vitro effects of eight insect meals (for species of origin, see Table 1) on rumen fermentation characteristics. Consistent with Jayanegara et al. (2017a), Renna et al. (2022b) observed poor IVOMD for the insect meals, except for Blatta lateralis, compared to reference plant meals (i.e., soybean, sunflower, and rapeseed meals). Nevertheless, low inclusion levels of insects may help avoiding the depression of digestibility parameters, as suggested by Ahmed et al. (2021) after replacing 25% of SBM (≈10% of total diet) with insect meals obtained from A. domesticus, Brachytrupes portentosus, and Gryllus bimaculatus adults, and from B. mori pupae. None of them caused adverse effects on nutrient digestibility when incubated in vitro with rumen inoculum from cows. Full-fat insect meals are characterized by high EE and chitin contents, which may contribute to explain detrimental effects on nutrient digestibility, especially on structural carbohydrates, since the presence of high amounts of unsaturated lipids can be toxic for ruminal cellulolytic microbiota (Jayanegara et al., 2017a). Moreover, Jayanegara et al. (2017a) hypothesized that chitin, a complex polysaccharide naturally present in insect exoskeletons, might contribute to impair nutrient digestibility, being nondegradable by ruminal microbiota. However, a subsequent study by the same research team showed that lowering the chitin content in Gryllus assimilis did not improve its overall digestibility characteristics (Jayanegara et al., 2017b), suggesting a minor role of chitin on overall digestibility. Renna et al. (2022b) also found that B. lateralis had the highest chitin content among the tested full-fat insect meals, but it displayed the most promising results in terms of fermentation. These results would support that chitin is degradable to certain extent in the rumen (Fadel El-Seed et al., 2003). As mentioned above, a major reason for the expectations placed on insects as innovative feeds is their high protein content. To properly assess protein digestibility in ruminant species, it is necessary to evaluate the extents of ruminal protein degradation and of intestinal digestibility of nondegraded protein in the rumen. Dietary proteins that reach the rumen are largely degraded to ammonia-nitrogen (NH3-N), a source of nitrogen for ruminal microbial growth. However, due to the high cost of protein-rich feeds and the need to minimize nitrogen losses, there is high interest in using proteins that by-pass the rumen, and reach the small intestine, where they are absorbed and favor animal performance (Putri et al., 2019). Robles Jimenez et al. (2022a) evaluated the use of larvae meals from H. illucens, T. molitor, and Notonecta spp., reporting similar in vitro degradable protein contents with that of SBM (≈60%) and higher when compared to fish meal (19%). Ruminal degradation of SBM proteins has been well characterized, whereas information on protein fractions and protein degradation rate of insect meals is still very scant. Renna et al. (2022b) observed lower ruminal ammonia content when comparing the use of various full-fat insect meals and plant meals, consistent with a previous comparison between H. illucens larvae meal and SBM (Jayanegara et al., 2017a). Such result would be advantageous in ruminant nutrition provided that intestinal digestibility of nondegraded protein in the rumen is high. This latter parameter was estimated by Toral et al. (2022) in T. molitor, Zophobas morio Fabricius, and A. diaperinus larvae, and A. domesticus adults, focusing on nitrogen disappearance, rather than in CP, since a misleading value could be obtained with the use of the conventional nitrogen-to-protein conversion factor (Kp) of 6.25. It should be highlighted that, in insects, the classical CP analysis with the Kjeldahl methodology may lead to an overestimation of the real CP content by including part of the nitrogen embedded in chitin (Janssen et al., 2017). Taking this into consideration, Toral et al. (2022) observed high (>64%) in vitro intestinal digestibility of nondegraded nitrogen for tested insects, with no difference relative to SBM, except for a higher intestinal digestibility in T. molitor. The literature on the use of insect-derived products in vivo is limited to only one or two papers on each ruminant species. Astuti et al. (2019) published one of the first in vivo trials on this topic, evaluating the inclusion of cricket meal in rations destined to preweaning and postweaning goat kids. Feeding a milk replacer containing full-fat adult Gryllus bimaculatus meal revealed no negative effects on physiological parameters in goat kids, which showed higher nutrient intake, comparable final body weight, and average daily gain, but lower feed efficiency, relative to the group fed goat milk. Compared with artificial milk replacers, goat milk helps the transfer of immunity from mothers to kids, which could affect animal performance. In postweaning kids fed a 30:70 F:C diet, the inclusion of 15% and 30% cricket meal in the concentrate (replacing 50% and 100% of SBM respectively), showed encouraging results, with no negative effects on DM and nutrient intakes, average daily gain, feed efficiency, and rumen fermentation profiles. In the ovine, Robles-Jimenez et al. (2022b) evaluated in vivo the effects of including T. molitor meal in the diet of growing lambs, compared to SBM and fishmeal. While feed intake and nitrogen intake were not impaired by the protein source, insect meal, and fishmeal decreased DM and organic matter digestibility, and nitrogen retention relative to SBM. In dairy ewes, however, Robles-Jimenez et al. (2022c) found that replacing SBM by Notonecta spp. in the diet increased milk production (up to 60%), fat-corrected milk and fat-protein corrected milk (Figure 2). Diets containing insect-derived products compared to control diets: impact on dairy performance and major pathways of ruminal biohydrogenation of linoleic acid. Compared with controls: increase (P < 0.05); no significant change; decrease (P < 0.05). Abbreviations: ACD, Acheta domesticus; ALD, Alphitobius diaperinus; BL, Blatta lateralis; BM, Bombyx mori; FPCM, fat-protein corrected milk yield; GB, Gryllus bimaculatus; GS, Grylloides sigillatus; HI, Hermetia illucens; MD, Musca domestica; NTC, Notonecta spp.; TM Tenebrio molitor. Finally, in the bovine, Fukuda et al. (2022) investigated the effects of full-fat H. illucens larvae meal, compared to conventional protein sources (cottonseed and SBM), as the main protein source in beef steers consuming low-quality forages. The authors focused their attention on feed intake and digestion performance, reporting no depression of the overall digestibility or impairments in ruminal fermentation. However, feeding the insect meal decreased the intake of organic matter from roughages, relative to the use of vegetable meals. Research aimed at improving the technological processes to obtain insect meals is moving alongside with investigations on their inclusion in animal diets. Manufacturers have increased the production of defatted insect meals, which allow increasing protein concentration (Mishyna et al., 2021). Moreover, defatted meals have better stability during storage, due to reduced risk of lipid oxidation and rancidity. However, we are aware of only three reports—two in vitro (Mulianda et al., 2020; Phesatcha et al., 2022) and one in vivo (Rashmi et al., 2022) – on the inclusion of defatted insect meals in the diet of ruminants. Interestingly, Phesatcha et al. (2022) reported that replacing SBM by defatted cricket meal improved ruminal fermentation by enhancing DM degradability and reducing methane production and acetate:propionate ratio. Mulianda et al. (2020) suggested that defatting of black soldier fly meal, in particular by chemical means, improved its nutritional value. Moreover, Rashmi et al. (2022) replaced 10%, 20%, and 30% of SBM by defatted silkworm pupae meal in the diet of crossbred cattle, also with positive results. Indeed, indirect comparisons with the use of full-fat insect meals (Jayanegara et al., 2017a; Renna et al., 2022b) would suggest a greater overall digestibility of defatted silkworm, which may be included up to 30% into rations for cattle without impairments of rumen fermentation patterns and nutrient utilization (Rashmi et al., 2022). Because ruminant diets are usually characterized by low lipid contents, defatting insect meals might an for developing innovative and sustainable protein-rich sources for ruminants. As mentioned above, their high protein full-fat insect meals are also sources of with a high in terms of length and when these meals in ruminant it is to the effects on ruminal of In this of the full-fat insect meals examined by Renna et al. (2022b) were in which by ruminal It could be that the high EE and chitin content of insects domesticus, T. molitor, and might have the microbial in interest in the study of the use of full-fat insect meals to improve the of products, as milk and meat (Figure 2). full-fat insect meals, and especially obtained from H. illucens larvae, are in as which can have and effects (Jayanegara et al., 2017a; Astuti and 2020; Ahmed et al., 2021). a potential to methane production (up to was also observed in vitro by Phesatcha et al. (2022) using defatted adult bimaculatus meal, which was to a of ruminal (Table 2). may therefore explain the potential effects of insect-derived products, which In these first promising results would suggest that insects may be included in ruminant diets with the of reducing the environmental impact of No are the of lowering CH4 production on animal performance and feed efficiency, the role of methane emissions as an for the Diets insect-derived products compared to control diets: impact on total and CH4 and ruminal a major after defatting insects, they are intended for animal feed or for the of insect to ruminant diets is 1) to increase the of the to methane and to modulate ruminal to obtain dairy and meat products with a more for In terms of digestibility, diet with insect showed similar results to obtained with full-fat insect meals. Jayanegara et al. tested the in vitro effects of increasing levels of H. illucens larvae of the reporting a decrease in and Despite an increase in ammonia concentration and in rumen H. illucens decreased in a with significant effects with inclusion levels or higher than The same was also reported by et al. using increasing levels of B. mori and in a previous study by Jayanegara et al. tested the in vitro effects of the of of insect with different of are reported in Table 1). Interestingly, et al. (2020) showed effects in whereas Jayanegara et al. (2020) reported no between of insect and diet or 30:70 F:C on methane these studies suggest a promising potential to this and decrease the environmental impact of with vegetable (e.g., soybean and has been examined as a to the nutritional of meat and milk In this et al. (2022) compared the in vitro of from H. illucens, B. and A. domesticus in and linoleic respectively) and soybean in linoleic In the of detrimental effects on ruminal results that insect ruminal with results that were to their A. domesticus was identified as the most to soybean the of the without a towards the production of (Figure 2). These latter have been with effects on animal performance and studies investigated the potential role of chitin, from insect and obtained chitin as feed for the of ruminal methane emissions and the first et al. (2022) reported that can the ruminal environment by lowering and feed digestibility, and the acetate:propionate ratio. Even most ruminal are the above-mentioned effects on might the methane potential of as defined as (e.g., use as an to In an in vitro et al. (2019) observed that the of of chitin or from H. illucens to a 60:40 F:C diet caused a decrease in As a feed may also the ruminal of unsaturated Jayanegara et al. results from published in vitro trials using from at between and diet and reported an increase in the ruminal of (e.g., and which could be available for and However, et al. (2022) observed that from H. illucens at DM did not the of in vitro ruminal when used or in with DM of soybean, H. illucens, A. domesticus, or B. mori oils. The lack of effects on and derived from microbial that did not ruminal microbiota. research is to these effects of may be by their (e.g., species of and the (e.g., incubation time and diet or other Research on the use of insects in ruminant feeding is its first and, although results obtained are available are still In these nutritional are still to several legislative worldwide. a major research is in years to a nutritional of insect-derived products (i.e., full-fat and defatted meals, and other and specific levels of inclusion for ruminants, into the large variations in insect due to species and production This information is to diets and to detrimental effects on animal performance, for which the differences between ruminant species and production also be As a it would be to evaluate the use of insect products in diets for ruminants, into their and environmental impact on different farming Finally, the of insect-derived products and of the on which insects are should be considered prior to a on insects as in this should also be by the transfer of research to as a to a worldwide. 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