Punita kumari1, A K Singh2 and S K Rajak3
1: TVO, Animal and Fisheries Resources Department, Government of Bihar, India.
2: Assistant Professor, FVAS, BHU, Mirzapur UP India
3: SMS, KVK Parsauni, DRPCAU, PUSA, Bihar, India
Introduction
The food production system of the world is rapidly changing due to growth in human population, urbanization, nutritional preferences, environmental concerns and growing income. Demand for animal sourced food (ASF) is increasing both quantitatively and qualitatively. The predicted demand for meat (pork, chicken, beef etc.) and milk in 2050 will be 70 and 58% percent higher compared to 2010 with the bulk of the demand coming from developing countries (FAO 2011a). However, livestock farming occupies about 70% of all agricultural land (Steinfeld et al., 2006), consume 8% of water used by humans (FAO, 2009), contribute 14.5% to greenhouse gas emissions (Gerber et al., 2012) and causing much higher water footprint than plant-based foods (Mekonnen and Hoekstra, 2012). Livestock production requires intensive resources for its sustenance which is difficult to maintain from available natural resources. Soybean meal and fish meal constitute the main protein component for the livestock production but low availability of land for soya cultivation and overexploitation of marine resources threatens fish meal production. Therefore, the price of these two feed ingredients has increased a lot during the last 5 years which the increases the livestock production cost and is a major concern for the owners.
Insects have been proposed as an alternative high-quality protein feed for livestock. Insect production on a commercial scale may be a promising strategy for global feed security because , insects grow and reproduce rapidly, with very low investment of resources in the form of space and time (Oonincx and De Boer, 2012).Further there is lower emission of greenhouse gases (Oonincx et al., 2010) and ammonia than cattle or pigs and their production requires low capital investment (FAO, 2013). Insects are also more efficient in converting feed to protein (Veldcamp et al., 2012) Insects as food and feed can have significant impact on food-feed security if they are produced in high number with proper management and strategy. Veldcamp et al. (2012) demonstrated production of insects on large scale and use them as an alternative protein rich feed in pigs and poultry diets. Many countries in the world has started to produce insects and use them for livestock feeding, like in Thailand 20,000 insect farms produce an average of 7,500 metric tons in a year for home consumption (Hanboonsong et al., 2013). Agriprotein Technologies, Australia is producing two tons maggots as protein source per week but target is 100 t of larvae per day. Based on available information this paper mainly focuses on insects for feeding animals and addressing nutritional quality, nutritive value, functional properties, animal performance, risk profile of insects and future research needed.
Insect species
More than 2000 edible insect species have been reported in the literature, most of them from tropical countries. The insect species reported to have the greatest potential as feed on an industrial scale are the black soldier fly (Hermetiaillucens), the common housefly (Muscadomestica) and the meal worm (Tenebriomolitor) Veldcamp and Bosch (2015). These three species have great potential to use and valorize organic waste of which 1.3 billion tons are annually produced globally (FAO, 2011b) with a potential value of US $ 750 billion (The Economist, 2014). Oher insects of importance include locusts-grasshoppers-crickets and silkworm (Table 1). Several review papers and reports have been published on insects as human food/animal feed (Veldcamp et al., 2012; Makkar et al., 2014; EFSA Scientific Committee, 2015) reviewed.
Table 1. Order and species and stage of insects used as food and feed for humans and livestock
| Order | Scientific name | Common name | Stage at which harvested for food/feed |
| Coleoptera | Tenebriomolitor | Mealworm | Larvae |
| Diptera | Hermetiaillucens | Black soldier fly | Larvae/pupae |
| Muscadomestica | House fly | Larvae/pupae | |
| Lepidoptera | Bombyxmori | Silk worm | Pupae |
| Orthoptera | Locustamigratoria | Grasshopper | Adult |
| Achetadomestica | House cricket | Adult |
Borroso et al. (2014)
Nutritional Composition
Most insect species dry matter content was around 40% with the exception of black soldier fly (26.8%). In processed insects (in dried and ground form) dry matter content was 90% (Veldkamp et al., 2012). The insects of different orders have different ranged of crude protein that may vary from 13 to 77% on DM basis. (Xioming et al., 2010). Feed of the insects may directly influence the nutritional composition Oonincx and Dierenfeld 2012; Rumpold and Schluter, 2013; Makkar et al., 2014; Micek et al., 2014; Sanchez_Muros et al., 2014). The black soldier fly larvae contain about (42.3%) and prepupae (38.1%) and highest for common housefly pupae (62.5% of DM) of CP as reported by Veldkamp et al. (2012). Yellow meal worm and house fly larvae were comparable for their crude protein content (median 49.3 and 50.8 % of DM). Soybean meal (defatted) which was mainly used as a protein source in animals feed has a protein content of 49-56% and contains around 3% fat on DM basis.
Insects are also considerable sources of fat. As per the available literature the crude fat (CF) values range between 5-50% in edible insects (Xioming et al., 2010; Makkar et al., 2014; Micek et al., 2014) yellow mealworm larvae and pupae contains about 36.1 and 33.8% CF, respectively whereas common housefly larvae and pupae had 20.6% and 15.5%. (Veldkamp and Bosch, 2015). Information on carbohydrate content in insects is scanty. Crude fiber content in different edible insects ranged from 0 to 86% on DM basis (Bukkens, 1997; Finke, 2005; Rumpold and Schluter, 2013; Makkar et al., 2014; Sanchez-Muros et al., 2014). Chitin is the principal carbohydrates present in the insects which may decrease insect protein digestibility (Defoliart, 2002). The Yellow mealworm larvae contains around 3.5% of total ash which is lower than those for common house fly (larvae = 11.2%; and pupae = 7.7%) and black soldier fly (larvae = 11.0%; prepupae = 14.7%). Locust meal and silk worm pupae meal contains about 57.3, 8.5, 6.6 and 63.3, 17.3 and 5.6%, of crude protein, ether extract and ash, respectively (Makkar et al., 2014). Similarly, silk warm pupae meal contains 60.7% protein, 25.7% fat and 5.8% ash.
Minerals
The mineral content g/kg DM of 32 species (mainly larvae) ranges between Ca (0.4-24.8), P (1.2-14.3), Mg (0.3-27.4) and in mg/kg DM for trace elements, Cu (9-265), Mn (3-39), Zn (21-390), Se (0.3-400) as reported by Finke (2005). Makkar et al. (2014) concluded about the status of major mineral and trace element content of black soldier fly (larvae), common house fly (maggot and pupae), mealworm (larvae), locust, house cricket (adults) and silk warm pupae meal and informed that insects contained higher levels of phosphorus than calcium. The availability of phosphorus was almost 100% in simple stomach animals from insects-based feed (Micek et al., 2014). Most insects may turn to be good sources iron, zinc, copper manganese and selenium (Barker et al., 1998; Belluco et al., 2013; Rampold and Schluter, 2013) but not for calcium (Finke, 2013). Makkar et al. (2014) reported that the Black soldier fly had the highest calcium phosphorus ratio (8.4) with other insects having lower ratios (0.29 to 1.28).
Vitamins
The literature for vitamin content in insects are very scanty and inadequate (Micek et al., 2014). Vitamin content insects as reported by Finke (2013) in black soldier fly (larvae) and common house fly (adult) were as follows: Retinol (<300 μg/kg), vitamin D2 (<2 μg/kg), Vitamin D3 (2.5 μg/kg), α-tocopherol (6-30 mg/kg), Vitamin C (<10-23 mg/kg), Thiamin, B1 (0.1-11 mg/kg), Riboflavin, B2 (16-77 mg/kg), Niacin B3 (34-91 mg/kg), Pantothenic acid B5 (27-45 mg/kg), Pyridoxine B6 (1.7-6.1 mg/kg), Folic acid (08-2.7 mg/kg), Biotin (0.35-068 mg/kg), vitamin B12 (5-237 μg/kg) and 625-1100 mg/kg Choline (Simunek et al., 2001).
Energy
Gross energy (MJ/kg DM) contents of black soldier fly, housefly maggot, housefly pupae, mealworm and locust meals were 22.1, 22.9, 24.3, 26.8 and 21.8, respectively. Soybean meal which represents two thirds of the total world output of protein feedstuffs including all other oil meals and fish meal (Oil World, 2010) has a gross energy value of 19.7 MJ/kg DM. Digestible and metabolizable energy values for insects are scarcely available in the literature and there is an urgent need to generate these information. .
Amino acids
Histidine, lysine and tryptophan are most frequent limiting amino acids in insects (Sanchez-Muros et al., 2014). Veldkamp et al. (2012) summarized in their report that proteins in black soldier fly, common housefly and mealworm were generally lower in arginine and cysteine (except mealworm larvae) and higher in methionine and tyrosine compared to soybean meal. First limiting amino acids were tryptophan and lysine in insect protein (Ramos Elorduy et al., 1997; Finke, 2005). Essential amino acids levels in silkworm pupae meal and black soldier fly larvae were higher than in soybean meal or FAO reference protein (Makkar et al., 2014).
The essential amino acid indices (EAAI) of black soldier fly, common house fly and mealworm would generally provide more of the essential amino acids than required for broilers and growing pigs (Veldkamp and Bosch, 2015). Chemical scores were also calculated for insect amino acids to assess their protein quality. The lowest score which indicates the first limiting amino acids in black soldier fly (larvae and prepupae), housefly larvae and yellow mealworm larvae were methionine or methionine+cytine in pigs and broilers (Veldkamp and Bosch, 2015). Further, lowest score in mealworm was also observed for arginine in broilers.
Fatty acids
It was observed that the insect meal possesses a lot of variation in fatty acids profile across different species (Lu et al., 1992; Borroso et al., 2014). It was reported that the fatty acid present in edible insect species mainly constitute palmitic, (8-38%), oleic (9-48%), linoleic (7-46%) and α-linolenic acid (15-38%) respectively (Womeni et al., 2009). Summarization of fatty acid data of six insect species (Pereira et al., 2003; Barroso et al.,2014; Makkar et al., 2014) revealed saturated, monounsaturated, polyunsaturated and omega 3 fatty acid levels of 22.2-67.1, 16.9-52.7, 7.5-32.1 and 0.7-24.7 %, respectively. Unsaturated (mono+poly) fatty acid levels were higher and saturated fatty acids were lower in all insect species except for black soldier fly. Silkworm pupae meal contains the highest Omega fatty acids whereas, the black soldier fly larvae contains the lowest (Bukkens, 2005). Fatty acid composition of diet influenced lipid content and composition in black soldier fly. Larvae that had been reared on cow manure had reported to have more saturated (37%) and monounsaturated fatty acids (32%) content however, were low in omega-3 fatty acids (0.2%). (St-Hilaire et al., 2007). Insect fatty acids are richer in polyunsaturated fatty acids (PUFA) (Kierończyk et al., 2018).
Digestibility
Literature on digestibility of selected insect species in pigs and poultry is very scanty. Monogastric animals have comparatively better digestibility and utilization of insect crude protein than the polygastric animals (Han et al., 2017). Digestibility of crude protein was similar where as crude fat digestibility was higher as reported after feeding black soldier fly larvae meal to the pig (33% of corn-based diet) in comparison to those fed soybean meal (25.5% based corn diet (Newton et al., 1977). Hwangbo et al. (2009) recorded digestibility of 98.5whereas Pretorius (2011) reported 69% for protein in broilers fed common housefly meal-based diets. Pretorius (2011) reported higher CP digestibility for housefly pupae meal than larvae meal however, the amino acid digestibility in both the diets were more than 90%. The lower protein digestibility (69%), attributed due to the indigestibility of chitin-N and/or ADF bound N. Further research on feeding value whole insects at different life stages as well as processed ones is essential for formulating insect-based diets for livestock.
Functional Properties of Insects
Chemically chitin is similar in structure to that of cellulose (β 1-4 N-acetyl-D-glucosamine). The black soldier fly larvae and yellow mealworm larvae were reported to contain about 5.4 and 2.8% Chitin, respectively (Finke, 2013). Non insect chitin or chitin derivatives can enhance immune response in kelp groupers (Harikrishnan et al., 2012), act as antibiotic/probiotic in rats and chicken (Khempaka et al., 2011) and had hypolipidaemic properties in broilers (Hossain and Blair, 2007). Further, the peptides produced by black soldier and house fly larvae thriving on manure or organic waste are antimicrobial and these peptides might be functional in in monogastric livestock (pigs and poultry). It is assumed that Chitin may support gut health; the chitin was reported to act as prebiotics in rainbow trout after feeding black solder fly larvae meal (Bruni et al., 2018).
Performance of Livestock
Insect meals can be used feed protein in the same way as more conventional protein sources (soybean meal, fish meal etc.) but may not be able to replace these protein sources completely. (Ravindran and Blair, 1993; Veldkamp et al., 2012; FAO, 2013, Makkar et al., 2014; Sanchez-Muros et al., 2014; Veldkamp and Bosch, 2015) reviewed studies based on the insect feeding in animals and reported that many developing countries mostly using organic waste and livestock manure as substrates for the insects.
Pigs
Black soldier larvae meal found to be a good source for protein, lipid and calcium content (Makkar et al., 2014) and was included in growing pig diets.Neumann et al. (2018) substituted black soldier fly (BSF) larvae (partially defatted) or algae meal (Spirulina platensis) to soybean meal in piglet and grower pig feed and reported no difference in the growth parameters and further, observed superior apparent N digestibility in the BSF diet. Altman et al. (2019) observed no negative effect on the resultant pork quality and sensory parameters with improved juiciness after replacing the soybean meal content of growing/finishing pigs diets with either 50 or 75 and 100% BSF meal (partially defatted; 61% CP and 14% lipid). They also recorded the feed supplemented with BSF larvae produced back fat with higher polyunsaturated fatty acid content. The Soybean-based diet supplemented with 10% maggot meal to replace fish meal (isonitrogenous and isocaloric) when fed to weaned pigs had no negative effect on body weight gain or feed conversion efficiency (Viroje and Malin, 1989). Jin et al. (2016) reported an increase in average daily gain, body weight, dry matter and protein digestibility in the pigs after replacing soybean with 6% replacement of mealworm in the diet of the pig. It was revealed that after providing pigs with diets that contained Tenebrio molitor larvae meal supplemented at the 10% of the diet results in improved apparent ileal digestibility of nutrients as well as essential and non-essential amino acids (Yoo et al., 2019).
Poultry
Soybean meal was replaced by black soldier fly and housefly pupae, fish meal by silk worm pupae meal and fish meal and soybean meal by Chinese grasshoppers in poultry (broiler/layer) diets (Ravindran and Blair, 1993; Wang et al., 2007). Ramos-Elorduy et al. (2002) could replace soybean meal up to 10% with dried yellow mealworm meal harvested from low nutritive organic waste products without any negative effects. House fly maggot meal at 10% and greater level in the diet decreased performance and intake (Bamgbose, 1999; Makkar et al., 2014) probably due to darker color of the meal (less appealing to chicken) as well as well as low chemical score for methionine. Methionine supplementation might improve performance. Teguia et al. (2002), Awoniyi et al. (2003) and Hwangbo et al. (2009) successfully replaced fish meal in broiler diets with common house fly larvae (54% CP) on iso-caloric (12.6 MJ) and iso-nitrogenous (20% CP) basis. Feeding diets with 10-15% maggot meal improved weight gain and carcass quality of broiler chickens (Hwangbo et al., 2009) compared to diets with 5 and 20% maggot meal. Replacing 25% of fishmeal in the diet is most efficient in terms of weekly weight gain and protein efficiency without influencing carcass characteristics (Awoniyi et al., 2003). Average daily gain, slaughter weight and feed intake increased in broilers when compared with corn-soy meal-based diets when maggot meal was supplemented in three phase feeding system (Pretorius, 2011).
Woods et al. (2019) showed a higher apparent digestibility for dry matter and organic matter after feeding H. illucens larvae to quail as compared to the control group. However, Bovera et al. (2018) reported 2% lower ileal digestibility coefficients of dry matter and organic matter in broilers fed the T. molitor diet than those fed the soybean diet. In laying hens, Cutrignelli et al. (2018) detected the reduced coefficients of the apparent ileal digestibility (AID) of dry and organic matter after fedding H. illucens meal diet. Broilers fed either 10% maggot meal or 10% fish meal diets had heavier carcasses and breast muscle portion than those on corn-soy based diet (Pretorius,2011). Kareem et al. (2018) revealed that excreta Enterobacteriaceae count was lower in birds fed with larvae meal supplemented diets than the control. A 25% larvae meal diet when fed to broiler resulted in significantly higher slaughter weight, feed intake and average daily gain than control diet containing fish meal (Pretorius, 2011). Teguia et al. (2002) concluded that it is economical to use maggot meal in replacement for fish meal in broiler diet. In layers maggot meal could replace 50% of the dietary fish meal without affecting egg production and shell strength (Agunbiade et al., 2007). Twenty four broiler feeding trials (Africa-17, Asia-4 and US-3) in which various levels of house fly maggot (larvae) meal were fed and twelve broiler studies (9 from India) in which silk worm pupae meal was fed were summarized and it was concluded that insect protein could replace soybean meal, groundnut cake and fish meal (Makkar et al.2014) .Weight gain, feed intake, feed conversion and slaughter parameters and meat quality was not affected by replacing fish meal up to 100% in broiler diets with silk worm/pupae meal (Ijaiya and Eko, 2009; Kumar et al., 1992).
Ruminants
Limited feeding experiments with insects as dietary protein supplement was reported in ruminants (Makkar et al., 2014). However, a study on silk worm pupae meal (non-defatted) indicated that it could replace 33% groundnut cake safely and economically (on weight basis) in fattening Jersey calf diets (Narang and Lal, 1985). It has been observed that after feeding insects to the cattle a higher growth rate and better feed conversion rate with low greenhouse was emitted (Oonincx et al., 2010)
Major Concerns
Further, information is required on the use of insects as food/feed source. Major of the experimental trial expressed that insect larvae can be fit for human/animal consumption as protein source. Some consumers are interested to consume food from animals that were fed insects as part of the diet but this should be mentioned on the food label. Further, studies on economics of feeding as well as awareness are required for the supplementation of insect as protein source in the animal diet. At the same time proper investigation of potential risk needs to studied at the time of evaluation of nutrient digestibility and nutritive value of insects (processed) for mono-gastric livestock and aqua animals. Potential beneficial functional properties of insect proteins need to be identified so as to create an added value to the insect protein. Further any harmful implications on the health and welfare of animals with the cost of production is required to validate the information and build some evidence for the safe and sustainable use of insect for animal feeding. Larvae of insects (black soldier fly, housefly and yellow mealworm) need to be processed for improving their shelf life and food safety but processing methods (freezing/freeze drying) are very expensive which needs to be economized by developing suitable processing technology.
Conclusion
Insects may be used as an alternative and economical protein source for the livestock without compromising the quality of the feed protein. Establishing legal regulatory framework for use of insects/insect meals as animal feed and improved risk assessment methodologies are also very important consideration which needs to be framed and figure out for attracting investment in commercial insect farming. In addition, development of insect value chain by sharing knowledge and creating awareness among stakeholders of the insect industry (organic side stream suppliers, insect farming and processing industries, animal feed industry, pig and poultry producers, retailers and consumers). To make use of insects as a feed ingredient in the monogastric livestock (pigs and poultry) feed chain, additional research on substrate needs per unit of insect biomass production in different species is required.
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