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From waste to feed: a review of recent knowledge on insects as producers of protein and fat for animal feeds
Journal Pre-proof From waste to feed: a review of recent knowledge on insects as producers of protein and fat for animal feeds Laura Gasco, Irene Biancarosa, Nina S. Liland PII:
S2452-2236(20)30020-1
DOI:
https://doi.org/10.1016/j.cogsc.2020.03.003
Reference:
COGSC 333
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Current Opinion in Green and Sustainable Chemistry
Received Date: 12 February 2020 Revised Date:
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Accepted Date: 6 March 2020
Please cite this article as: L. Gasco, I. Biancarosa, N.S. Liland, From waste to feed: a review of recent knowledge on insects as producers of protein and fat for animal feeds, Current Opinion in Green and Sustainable Chemistry, https://doi.org/10.1016/j.cogsc.2020.03.003. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Elsevier B.V. All rights reserved.
From waste to feed: a review of recent knowledge on insects as producers of protein and fat for animal feeds Laura Gasco1, Irene Biancarosa2,3, Nina S. Liland3
1 Department of Agricultural, Forest and Food Sciences, University of Turin, largo P. Braccini 2, 10095 Grugliasco, Torino, Italy 2 University of Bergen, Department of Biology, Thormøhlensgt. 53 A/B, P.O. Box 7803, 5020, Bergen, Norway 3 Institute of Marine Research, P.O. Box 1870 Nordnes, 5817 Bergen, Norway
Corresponding author: Laura Gasco, Department of Agricultural, Forest and Food Sciences, University of Turin, largo P. Braccini 2, 10095 Grugliasco, Torino, Italy. Email: [email protected]
Abstract The use of insect-derived products in animal feed is a field of growing interest. Applying the Circular economy principle, insects efficiently bioconvert organic waste into new products enabling advantages and value at different steps: reduction of waste management costs (landfilling, anaerobic digestion, incineration) lower resource use than other protein and fat productions, and value gain from the sale of insect-derived. After introducing the potential use of insects to upgrade food waste for animal feed purposes and briefly discussing the feed sector and the regulations that govern and limit the insect mass production and uses, this review presents the latest and most interesting research (from 2019) on the use of insect as feed.
Keywords: Insects, waste, circular economy, protein, compound feed,
Introduction: Food waste and animal feed– insects as part of the solution? Globally, about one third of all the food produced for human consumption is lost or wasted within the food supply chain [1]. This corresponds to approximately 1.3 billion tonnes of food getting wasted every year but also to a tremendous loss of resources that have been invested in producing food (e.g. waters, land, fossil fuels). At the same time, the compound feed industry exceeded one billion tonnes of production in 2018, generating a turnover of more than € 360 billion [2]. Within the European Union (EU), this represent about 165 million tonnes of production and € 49.3 billion of commercial feed purchases [3]. To meet the demand for food of animal origin from an increasing world population, the global compound feed market will likely continue to expand for years to come. Such an increase in the production of feed ingredients will add pressure to limited resources such as land, water and energy. An intensification of the feed sector will therefore require new strategies to maintain a sustainable production. In the last years, the concept of a “circular economy” has taken hold in most
countries to fight food waste: that is an economic system which maintains values of waste through its use and reuse [4], and this way of thinking is also becoming more popular among feed producers. Today, finding sustainable raw materials is a major obstacle and has become a priority among the feed stakeholders.
In contrast to a “circular economy”, a traditional “linear economy” historically follows the “take-makedispose” step-by step plan. In this context, food production follows a linear process through food producers, distributors and consumers, and the remain is finally discarded. Following specific countries regulations, some of these wastes could be used as animal feed but are more often sent to landfills. Regulations on animal feeds to ensure the food safety, are now more stringent, making the unformal “from table to animal” way of using waste no longer an option. By using our food waste to grow insect larvae, which can further be used in animal feeds, the nutrients and energy in the waste can be conserved. Many insect species can efficiently, and with low environmental impact, convert typical food waste like bread, cereals or other relatively lowvalue products into protein and fat [5]. In that way, insect production can become a stream of high-quality feed ingredients, already being used with success in animal feed formulations [6,7]. Finding sustainable ingredients to produce animal feeds is a major obstacle in animal production and has become a priority among the feed stakeholders, thus being the perfect market for insect ingredients. The possibility to use or to upgrade food waste for animal feed purposes using insects, is a perfect example of how a system based on the principles of circular economy can be constructed. The field of using insects as feed ingredients is very dynamic and fast-moving today, with a great amount of studies being published each year. While previous reviews focus on the complete historical literary knowledge on this field [6,7,8], this review focuses on only the very newest information published from 2019. A special emphasis is put on the use of insect raw materials produced on different organic waste streams for fish and non-ruminants feed formulations.
Feed for insects and insects as feed – European legislation The main aim of the food production chain is to produce nutritious and safe food for the consumers, which means to ensure “food safety”. When food comes from livestock animals, it is also necessary to provide nutritious and safe feed for the animals, that is to guarantee “feed safety”. Feed and Food safety regulations are therefore in place to ensure that feed and food stuff do not represent a danger to human health, animal health or the environment. Recently, the EU adopted the “Circular Economy package” where it defines which food, no longer intended for human consumption, is suitable for feed production. Within this context, in the EU, the use of catering or animal waste is forbidden, while in other countries different legislations are in force [9]. In the EU, insects are considered full-fledged “farmed animals”-i.e. animals that are kept for the production of food, feed or other derived products [(Reg (EU) 2017/893)]. Like other farmed animals, insects can only be fed on authorized substrates like “feed grade materials” (e.g. plant-based materials, vegetable and fruit residues, wheat bran, grass and brewery byproducts, hay, among others). However, outside EU, regulations on feeds for insects are less stringent. Research on the use of insect-based feed ingredients for farmed animals has developed rapidly in the last 5 years, leading to the authorization of insect processed animal protein (PAP) in feed for farmed fish in 2017 [Reg. (EU) 2017/893]. However, this regards only a few insect species: Black soldier fly (Hermetia illucens - BSF), Common housefly (Musca domestica - HF), Yellow mealworm (Tenebrio molitor - MW), Lesser Mealworm (Alphitobious diaperinus), House cricket (Acheta domesticus), Banded cricket (Gryllodes sigillatus) and Field cricket (Gryllus
assimilis). For other livestock (poultry, pigs) the “feed ban” [Reg .(EC) 999/2001] still limit the use of insect PAP but the rule could be soon relaxed [10]. There are no limitations on the use of fats derived from insects. In other countries such as Canada, BSF meals are also allowed for poultry. Moreover, in countries such as China or South Korea, no limitation applied. Under EU regulation, the “feed ban” do not apply to carnivorous fur producing animals that can be fed processed animals proteins, including insect-derived proteins.
Insects grown on waste material In the EU only selected types of waste materials of vegetable origin are allowed for use in insect production, leading to some concerns about sustainability, as products which could be used as animal feed or human food will have a higher environmental impact than when using organic side streams [11,12,13]. It has to be pointed out that technologies used to produce insects are still in their infancy, and there is large space for improvement, both regarding the type of substrate used to grow insects and the technology involved in an efficient large-scale production. Among the insect species assessed for aqua and livestock feeds, the most interesting are: the BSF [14,15,16], the HF [17] and the MW [18,19]. These species have a fast growth and are efficient at converting a variety of organic waste to protein and lipids. There are several studies showing how it is possible to be innovative with regards to the use of local waste, using campus restaurant food waste [20], fruit and vegetable waste from a wholesale market [21] or kitchen waste substrate [22] to produce insects. The concentrations in protein and other nutrients in the whole insect is affected by the general growth of the insects on a given media. Nevertheless, a general tendency seen is that the protein meal in itself won’t be affected in it’s quality, although the amount or ratio protein/fat might vary, A general tendency seen when growing insects is that the protein fraction of the insects will mainly stay the same, regardless of the substrate they grow on, while major changes are seen in the lipid fraction (fatty acid profile), mostly mirroring the lipid composition of the substrate [23,24]. As pointed out by Danieli and colleagues, it is essential to know the optimum dietary composition of the selected insect species, as a sub-optimal diet can lead to a prolonged production time as well as a less efficient nutrient retention.
Insect-based ingredients in compound feeds Among the ingredients used to produce compound feeds, those rich in proteins constitute the most important and expensive part of the diet. In particular, animal derived feedstuffs provides highly digestible proteins with great biological value. A wide array of studies, with an especially large increase in published studies the last few years, have proven the suitability of insects as a high-quality source of nutrients for animal feeds [5,6,7,9]. When formulating diets, the digestibility and nutritive value of ingredients is of primary importance to obtain diets able to cover animal requirements, and to optimize performances and costs. However, only a few published studies that deal with the determination of nutrient digestibility coefficients of insect meals in fish and livestock are available (Table 1). More abundant is the number of papers reporting results, in terms of digestibility, animal performance or parameters such as somatic indexes, whole body or fillet /meat composition, of diets containing different levels of insect meals (Table 2). By using insect ingredients, comparable animal growth and performance as other commonly used feed ingredients can be obtained. Attention must, however, be paid to cover the animal’s requirements of essential amino acids (EAA), as most insect species are low in some EAA (typically tryptophan and sulfur amino acids like methionine [6] which might need to be supplemented to the diets. Some species are also more tolerant to a higher inclusion of insect-based ingredients than others, so a species-specific approach should be taken into account when formulating diets.
Apart from insect-derived proteins, another interesting insect product for animal nutrition is the lipid fraction (recent results reported in Table 3). Some trials have substituted up to 100% of the lipid source in the control diet without changes in performance or digestibility. There are, however, some studies showing a negative effect from the lipid fraction of the insect ingredients [17]. This shows the importance of knowing more about the tolerance of each species to different insect ingredients in the diets. Although the growth of animals using insect ingredients is generally good, there are studies showing that insect meals or -fat in animal diets can influence the quality of derived-products (fillets, meat, eggs) in terms of proximate composition, fatty acid profile, or physical traits [25,26]. Nevertheless, not all results indicated an effect on quality [14], highlighting the need for more investigations research on the quality of products from insect-fed animals.
Insect ingredients with health-promoting properties There is substantial evidence that the use of diets with insect meals could have positive effects on animals’ immune system and microbiota [27] and recent results are reported in Table 4. The increased diversity in microbiota has been attributed to the content of chitin in insect meals, which is not digestible in most animals and promote growth of certain groups of bacteria, with positive effects on gut health. Insect chitin is also endorsed with immunostimulating effects [27]. The lipid component of insects has also been shown to have a positive effect on animal health, especially the high concentration of lauric acid in BSF [27]. In addition insect fat are a fast substrate for energy and promote less lipid storage in the liver [15]. Insect-derived-products have also been shown to have anti-microbial effects [28,29]. Conclusions The mass production of insects on waste can help to reduce the environmental impact of food waste as well as generate a sustainable novel feed ingredient for the animal-feed sector. Applied research shows promising results and insect-derived products are currently recognised as one of the most interesting and sustainable sources of nutrients. Insect-derived products also show potential as health enhancers, being a possible source of ingredients for feeds targeting specific challenges or life stages in animal production. Nevertheless, this industry is still in its infancy and further research and a clear legal framework is needed for the complete development of the sector.
Table1. Nutrient’ apparent digestibility coefficients (ADC) of insect meal as ingredient vs a Reference diet Animal (IBW, g) [digestib ility method]
Insect species and form
Mandarin fish (31.27 g) [sediment ation column] Nile tilapia (3.0 g) [Guelph system]
Full fat maggot meal
Atlantic salmon (300 g) [sediment ation columns] European sea bass (33 g) [Guelph system]
% Insect inclusion
Nutrient digestibility
General comments
Main ingredie nt of the REF diet
DM
CP
EE
GE
FM: 53%
69.76
83.93
80.28
69.56
68.46
82.59
78.61
71.99
95.8
85.4
90.6
82.1
ZMM
83.2
70.0
93.5
80.1
GAM
42.6
39.7
87.9
47.0
NCM
61.7
69.6
91.6
58.4
GPM
48.2
61.6
98.8
47.4
15 30
Full fat MWM
20
-
Influence of the level of inclusion on nutrient ADCs Higher CP and AA but lower EE digestibility compare to plant that of plant protein ingredients
[30]
Good digestibility of all meals, some interactions with chitin content.
[31]
BSFM
30
FM: 33.5%
87
89
97
88
Digestibility trial also performed against SBM and CPC. ADC of BSFM was generally over 75%, with DM & GE showing higher coefficients in BSFM than CPC and SBM. Mineral digestibility was generally higher in BSFM compared with CPC and SBM.
[32]
Full fat BSFM Defatted BSFM Full fat MWM Defatted MWM LM
20
FM: 45%
48.3 53.7 85.2 72.4 40.1
75.8 87.2 89.2 92.8 74.1
91.4 92.7 94.5 94.4 66.5
67.2 64.8 79.2 84.4 53.0
ADCs of all AA were assessed. The two MWM had the highest digestible total amino acid. Authors highlighted the importance of the defatting process to increase the nutritional value of insect meals
[33]
Abbreviation. REF: reference diet; DM: dry matter; CP: crude protein; EE: ether extract; GE: gross energy; AA: amino acid; FM: fishmeal; PBP: poultry by-products; CPC: corn protein concentrate; MWM: yellow mealworm meal; BSFM: black soldier fly meal; LM: locust meal; ZMM: Zophobas morio larvae meal; GAM: Gryllus assimilis meal; NCM: Nauphoeta cinerea meal; GPM: Gromphadorhina portentosa meal; SBM: soybean meal; ADC: apparent digestibility coefficient.
Table 2. Effects of dietary inclusion of insect meals on fish and livestock performances (whole cycle), nutrients digestibility and other parameters. Animal species (diets form) [IBW, g] {n° days}
Insect species and form
Atlantic salmon (Extruded) [1398 g] {114}
Partially defatted BSFM
Atlantic salmon (Steam pellet) [2800 g] {112}
BSFM
Insect composition (% DM)
CP
CL
52
12
58.65
12.37
% insec t inclu sion
CTRL diet: % of main protein substitute d
worsened 4.91; 9.85; 14.75
FM: 10 SPC: 25 CGM: 7.5; PPC: 8.8
10
FM: 10; CPC: 17.2; PBP: 18.5; BM: 15
20 30
Magree (Dry pellet) [18.0] {63}
Partially defatted BSFM
55.4
10.9
10; 20
WG; SGR; TGC; FCR; PER FM: 40
30
Sea trout (Extruded) [0.14 g] {60} Japanese seabass (Extruded)
Full fat MWM; full fat hydrolys ed MWM Defatted BSFM
vs CRTL diet with no insect meal
no differences FBW; WG;DGI; SGR; FI; FCR
29.6
20
FM: 30.6
61.42
1.77
4.8; 9.6
FM: 25
improved No effect on ADC of CP, CL, AA & FA. No effects on WBC for CP, CL & AA. FA WBC reflects that of diets. Small changes in fillet sensory quality. No differences in digestive enzyme activities -
WG; SGR; TGC; FC; FCR; PER WG; SGR; TGC; FC; FCR;PER FC
[14]
[32]
Linear decrease trend for FE, PER, NR and ER with the increase of BSFM dietary inclusion reflects the lower growth performance without differences in FI. Whole body ash linearly decreased with the increase of BSFM. No differences for all other WBC parameters. No differences for HSI & VSI. Increase in saturated FA and decrease in unsaturated FA. Plasmatic total lipid and triglycerides linearly decreased with the increase of BSFM. No differences for plasma glucose, cholesterol and total proteins.
[34]
SR; SGR; RGR; FCR; PER
Increase of VSI in fish fed MWM treatments. No differences for intestinal amylase, lipase and trypsin.
[35]
SR; FBW; WG; FI; FCR; SGR; PR; LR
No differences for somatic indexes No effect of diets on trypsin, lipase and amylase in the hepatopancreas.
[22]
FBW; DGI; FI; FE; PER; NI; NR; LI; LR; EI; ER
FI; FE; PER; NI; LI; LR; EI; ER
47.0
Other parameters recorded & comments
FBW; DGI, NR
[14.14] {56}
14.4; 19.2
Rainbow trout (Extruded) [5.01 g] {90}
Partially defatted MWM
Rainbow trout (Cold pellet) [137.3 g] {98} Rainbow trout (Extruded) [78.3 g] {154}
Full fat BSFP
67.1
13.6
39.00
41.86
Partially defatted MWM
-
Siberian sturgeon (Cold pellet) [24.2 g] {118}
Highly defatted BSFM
65.84
Climbing perch (Pellet) [2.2 g] {123} Nile tilapia (Commercial + spray) [2.1g] {49} African catfish (Pellet) [4.0] {60}
BSFP
FI (increased)
10.5; 21
FM: 42
SR; FBW; WG; SGR; FCR
-
5; 10; 20
FM: 20
SR; FBW; WG; SGR; FCR; PER; FI
Decrease in ADC of CP with the increase of MWM but values always higher than 97%. No differences for ADCs of DM, EE and GE Higher HSI in fish fed 20% of MWM. No differences for K and VSI. No effects on hepatic amino acid catabolic and lipogenic enzymes.
[19]
4.24
18.5
FM: 70
SR; FBW; WG; SGR; FCR; PER FCR; PER
Decrease in ADC of CP, but values always above 86% No differences in HSI, VSI and K. Increase of whole body EE content in fish fed 37.5% of BSFM
[37]
SR; FBW; WG; SGR; FCR SR; FBW; WG; SGR; FCR SR; FBW; WG; SGR; FCR; SR; FBW; WG; SGR; FCR; PER SR; FBW; WG; SGR; FI; PER; FCR SR; FI
Diets containing insect were also increasing reduced for CP and EE content BSFP protein can be better assimilated by climbing perch than FM BSFP % were substituted (sprayed) to a commercial diet.
[38]
14.9
FBW; WG; FC; SGR FM: 23
43.67
28.37
3
-
6; 9 Partially defatted BSFM
42.6
23.0
5.72
FM: 15
11.45 17.18
Nile tilapia (pellet) [2.08g]
FC
29 Full fat BSFP
MWM
-
[18]
FM: 25
6.1
FBW; SGR; FCR; FI; PER; PR; ER
Higher activity of intestinal lipase in fish fed 14.4% and 19.2% of BSFM than those of fish fed other diets. No effects on ADC. No differences in fish WBC. Higher FBW in fish fed 7.5% and 15% diets vs 5%. Phosphorous retention only improved in 7.5 & 15% diets. Diets also included PPC and WGM which increased with BSFP inclusion
5; 7.5; 15; 25
37.5 59.1
SR; FBW; WG; FCR; SGR; PR; LR
-
5, 10, 15, 20
SBM: 46.97
PER
PER, PR
FBW; WG; SGR; PER; FCR
Higher whole-body protein recorded in fish fed 11.45 BSFM inclusion. No differences for somatic indexes. Higher whole body protein content in fish fed 11.45% of BSFM than other treatments.
SR; FBW; WG; SGR; FI; PER; FCR FBW, WG, SGR, FCR, erythrocytes, HSI and WBC (DM & EE): linear effect when inclusion levels increased. Polynomial models and Plateau Linear Responses were applied to survival and productivity (kg
[36]
[39]
[40]
[41]
{42} Muscovy duck {50}
Partially defatted BSFM
56.71
10.70
3, 6, 9
CGM: 9
Broiler quails {29}
BSFM1 (reared on layer mash) BSFM2 (reared on 50:50 layer mash and fish offal) Defatted BSFM
36.04
36.38
10
SBM: 46
36.48
39.04
10
55.55
11.11
2.5; 5; 7.5; 10
Laying quails {42}
BSFM
54.75
15.64
10; 15
Weaning pigs {61}
BSFM
59.0
8.97
Jumbo quails {42}
5; 10
m−3) indicating maximum values of 11.68% and 10.68% of MWM inclusion, respectively. Higher levels decreased growth and performance and increased mortality. DFI; FCR FBW Three feeding periods. In the start phase, CP & EE digestibility linearly decreased (minimum at 9 of BSFM inclusion). In the two other phases, EE digestibility linearly increased (maximum at 9% of BSFM inclusion). Quadratic response to increasing BSFM in the grower period (minimum at 6% of BSFM inclusion). SR; FBW; WG; FI; FCR FBW; WG
Soy oil cake: 19.3; Full fat soya: 7.4 SBM: 35.9
SBM: 20 (phase I) 18.5 (phase II)
[42]
No differences in ADC for CP and Chitin. Higher ADC for DM, OM and GE for BSFM2 but lower ADC for EE if compared to CTRL diet. Higher ADC for GE in both BSFM diets.
[43]
FBW; WG; FI
Quadratic effect for WG and FI: regression indicated an optimum BSFM inclusion of 5.4%.
[44]
SR; FBW; FCR; Eggs production; Egg mass; Defected eggs
BSFM increased shell weight and percentage, and increased yolk colour. BSFM decrease CP and increased ash eggs content. No effect on eggs cholesterol content. Increase in saturated FA and decrease in polyunsaturated FA. No effects on sensory attributes (odor, aroma, taste) of both yolk and albumen. No effect on ADC od DM and OM. ADC CP: linear decrease in phase I. ADC EE: linear increase in both phases. ADFI in phase II showed a linear response to increasing BSFM levels with the maximum for the 10% of BSFM inclusion.
[45]
SR; FI; FCR
WG, ADG; ADFI; FCR
[16]
Abbreviations. AA: amino acids; ADC: apparent digestibility coefficient; ADFI: daily feed intake; ADG: average daily gain; BM: blood meal; BSFM: black soldier fly larvae meal; BSFP: black soldier fly prepupae meal; CGM: corn gluten meal; CL: crude lipid; CP: crude protein; CPC: corn protein concentrate; CTRL: control diet; DGI: daily growth index; DM: dry matter; DMI: dry matter intake; EE: ether extract; EI: energy intake; ER: energy retention; FA: fatty acids; FBW: final body weight; FC: feed consumption; FCR: feed conversion ratio; FE: feed efficiency; FI: feed intake; FM: fishmeal; GE: gross energy; HSI: hepatosomatic index; IBW: initial body weight; K: condition factor; LI: lipid intake; LR: lipid retention; NI: nitrogen intake; NR: nitrogen retention; OM: organic matter; PBP: poultry
by-product meal; PER: protein efficiency ration; PPC: Pea protein concentrate; PR: protein retention; RGR: relative growth rate; SGR: specific growth rate; SPC: soy protein concentrate; SR: survival rate; TGC: thermal growth coefficient; MWM: yellow mealworm larvae meal; VSI: viscerosomatic index: WBC: whole body composition; WG: weight gain; WGM: wheat gluten meal.
Table 3. Effects of dietary inclusion of insect oils/fat on fish and livestock performances (whole cycle), nutrients digestibility and other parameters Animal species [n° days]
Insec t speci es
% insect inclusion
CTRL diet: % of main lipid substituted
performances vs CTRL no insect oil/fat
decrease Broiler [30]
MWO
5
PF or PO
no differences WG; FI; FCR
Turkey [35]
BSFF
2.5 & 5
SBO: 5
WG; FI; FCR
Rabbits [41]
BSFF & MWO
0.75 & 1.5
SBO: 1.5
SR; FBW; ADG; ADFI; FCR, Morbidity
Digestibility and other parameters
improve d Reduction of relative weight of liver in MWO vs PF. No differences on Apparent ileal digestibility of CP, CF and AMEn. No influence on lipase and trypsin activity. MWO decreased the amylase activity vs PF. MWO decreased TG in blood vs PF. MWO decreased TG and total cholesterol in liver vs PF. In breast muscle, MWO influenced the content of SFA, MUFA and PUFA. No differences on apparent ileal digestibility of CP, EE and AMEn. 5% of BSFF decreased trypsin activity but without effects on digestibility. No influence of BSFF & MWO on digestibility of nutrients and energy.
[46]
[47]
[48]
Abbreviations. ADFI: daily feed intake; ADG: daily weight gain; AMEn: apparent metabolizable energy corrected to zero nitrogen balance; BSFF: Black soldier fly fat; CF: crude fat; CP: crude protein; CTRL: control diet; EE: ether extract; FBW: final body weight; FCR: feed conversion ratio; FI: feed intake; MUFA: monounsaturated fatty acids; PF: poultry fat; PO: palm oil: PUFA: polyunsaturated fatty acids; SBO: soybean oil; SFA: saturated fatty acids; SR: survival rate; TG: triglycerides; MWO: yellow mealworm oil; WG: weight gain.
Table 4. Effect of insect products on animals’ immune system, microbiota, blood parameters and intestinal structure. Animal (IBW - FBW, g) [days of trial]
Insect species form
Rainbow trout (201–275 g) [35] Rainbow Trout (66–220 g) [84]
BSFP or defatted-BSFM
% Insect inclusion in diet (main substituted ingredient % in CTRL diet) 30 (FM: 50)
Partially defatted BSFM
10, 20 & 30 (FM: 60)
Rainbow trout (137-300 g) [98] Rainbow trout (78–413) [154] Rainbow trout (115–270 g) [90] Seabass (5–17 g) [70] Seabream (105-238 g) [163] Sea trout (0.14–1.20 g) [60]
Full fat BSFP
10.5 & 21.0 (FM: 42)
Partially defatted MWM
5, 10 & 20 (FM: 20)
Full fat MWM
60 (FM: 70)
Siberian Sturgeon (640-1200 g) [60] Siberian sturgeon (24–150 g) [118] African catfish
and
Effects vs CRTL diet and comments
Increased diversity (higher abundance of phyla Firmicutes and Actinobacteria with lower abundance of Proteobacteria). The life-cycle stage of insect influenced the composition of gut bacteria Insect meal positively modified intestinal microbiota diversity. The beneficial lactic acid-and butyrate-producing bacteria where increased with possible positive repercussion on fish health. The probiotic effect was mainly attributed to fermentable insect chitin. Illumina high-throughput sequencing detected increased intestinal biodiversity with a reduction in Proteobacteria and an increase of the gut abundance of Mycoplasma Highest insect content lead to increase in genetic markers of stress and inflammation as well as an increase in liver lipids and shortening of intestinal folds in both insect groups No effects on hepatic amino acid catabolitc and lipogenic enzyme activity.
[20] [21, 49]
[36]
[19]
A differential shift in the dominant bacterial in the gut of each species was recorded with a more pronounced effect on gastrointestinal microbiota in saltwater than in freshwater species
[50]
50 (FM: 70) 50 (FM: 50) Full fat MWM; full fat hydrolysed MWM Full fat BSFM and MWM
20 (FM: 30.6)
No differences for liver ALT and AST.
[35]
15 (FM: 26)
[51]
Highly defatted BSFM
18.5 & 37.5 (FM: 70)
Changes in intestinal flora and structure of intestine with a reduction and an increase of the mucosa thickness for fish fed BSFM and MWM, respectively A different influence on the microbiota population was recorded for BSFM and MWM No influence on the liver and distal intestine histology. Alterations of the oxidative stress biomarkers were detected at 37.5% inclusion of BSFM meal.
Partially
5.72,
No differences for blood parameters and differential leucocyte counts.
[40]
11.45
&
[52]
(4-15g) [60]
defatted BSFM
17.18 (FM: 15)
Atlantic salmon (1400 – x g) [56] Japanese seabass (14-60g) [56]
Partially defatted BSFM
14.75 (FM: 10.5)
Defatted BSFM
4.8, 9.6, 14.4 & 19.2 (FM: 25)
Broiler [40]
Full fat MWM
5, 10 & 15 (SBM & CGM)
Broiler [35]
Partially defatted BSFM
5, 10 & 15 (SBM & CGM)
Turkey [35]
BSFF
2.5 & 5 (SBO: 5)
Lowest serum total protein, globulin, glucose, triglycerides, total bilirubin for fish fed 11.45% of BSFM. Lowest AST and ALT in fish fed 11.45% BSFM. Decrease in ALP activity in fish fed all BSFM diets. Similar MDA content vs CTRL Higher CAT in fish fed 11.45 and 17.18% of BSFM Lower SOD in all BSFM treatments. No alteration in gut health Decrease in triacylglycerol and in MDA. No influence on non-specific immune indexes. No alteration on hepatic and intestinal histomorphology. Up-regulation of hepatic lipoprotein lipase and hormone sensitive lipase and downregulation of fatty acid synthase genes (likely due to chitin) Decrease in the relative abundance of Firmicutes phylum and lower Firmicutes:Bacteroidetes ratios in birds fed 10 & 15% MWM. Increase in the relative abundance of Clostridium, Alistipes and Sutterella genera in MWM chickens. Decreased in the relative abundance of Ruminococcus genus in MWM groups. Higher mucin staining intensity in the intestinal villi of birds fed 5% MWM than the other MWM groups, and a mucin reduction in the intestinal villi of birds fed 10% MWM compared to CTRL. 5% of BSFM inclusion positively influenced either the cecal microbiota or the intestinal mucin dynamics in terms of preservation of physiological microbial populations, selection of potentially beneficial bacteria and increase in villi mucins. High inclusion levels (in particular the 15%) may have a negative influence in terms of partial reduction of the microbial complexity, reduction of potentially beneficial bacteria, selection of bacteria with mucolytic activity and decrease in villi mucins Total replacement of SO reduced proliferation of potentially pathogenic bacteria (Enterobacteriaceae spp) , MWO decreased interleukin-6 and tumour necrosis factor–alpha.
[53] [22]
[54]
[55]
[47]
In blood, 5% of BSFF increased total cholesterol, HDL and LDL while no effect on ALT, AST, TG, glucose, total protein and albumin were reported for BSFF groups Laying hens [168]
Partially defatted BSFM
7.3 & 14.6 (SBM: 26.5)
Muscovy ducks [50]
Partially defatted BSFM
3, 6 & 9 (CGM: 9)
No differences in TG and cholesterol in turkey meat (breast and leg). The highest level of BSFM inclusion reported a decrease in ileal villi height, and a reduced duodenal maltase and intestinal alkaline phosphatase activity. This group also showed the highest acetate and butyrate levels No effects on the intestinal morphometric indices (villus height, crypt depth & villus height-to-crypt depth. No influence on histological features of spleen, liver, thymus and Bursa of Fabricius
[56]
[42, 57]
and on haematological parameters. TG and cholesterol levels showed a linear decrease with the increase of BSFM inclusion. Jumbo quails [42]
Defatted BSFM
Rabbit [41] Piglets [61] Finishing pigs [46]
BSFF and MWO Partially defatted BSFM Full fat BSFP
2.5, 5, 7.5 & 10 (Soy oil cake: 19.3; Full fat soya: 7.4) 0.75 & 1.5 (SBO: 0.75 & 1.5) 5 & 10 (SBM) 4&8 (SBM: 16.98)
No linear nor quadratic effects for all the blood parameters, except for the Albumin/Globin ratio.
[44]
No negative effects on gut morphology, blood parameters
[48]
No negative effect blood profile, gut morphology or histological features.
[16]
Dietary inclusion of BSFMl may enhance mucosal immune homeostasis of pigs via altering bacterial composition and their metabolites
[58]
Abbreviations. ALP: Alkaline phosphatase; ALT: Alanine aminotransferase; AST: aspartate aminotransferase; BSFF: black soldier fly fat; BSFM: black soldier fly meal; BSFP: black soldier fly prepupae meal: CAT: Catalase; CGM: corn gluten meal; CTRL: control diet; FBW: final body weight; FM: fishmeal; HDL: high-density lipoprotein; IBW: initial body weight; LDL: low-density lipoprotein; MDA: Malondialdehyde; SBM: soybean meal; SBO: soybean oil; SOD: Superoxide dismutase; TG: triglycerides; MWM: yellow mealworm meal; MWO: yellow mealworm oil.
Conflict of interest statement Nothing declared.
Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author contributions All authors equally contributed to the conceptualization, writing, review and editing of this paper. XX Acknowledgements Authors thanks the SUSINCHAIN (SUStainable INsect CHAIN - GA n. 861976 - H2020_IA) project.
References Papers of particular interest, published within the period of review, have been highlighted as: * of special interest
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S2452-2236(20)30020-1
DOI:
https://doi.org/10.1016/j.cogsc.2020.03.003
Reference:
COGSC 333
To appear in:
Current Opinion in Green and Sustainable Chemistry
Received Date: 12 February 2020 Revised Date:
22 February 2020
Accepted Date: 6 March 2020
Please cite this article as: L. Gasco, I. Biancarosa, N.S. Liland, From waste to feed: a review of recent knowledge on insects as producers of protein and fat for animal feeds, Current Opinion in Green and Sustainable Chemistry, https://doi.org/10.1016/j.cogsc.2020.03.003. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Elsevier B.V. All rights reserved.
From waste to feed: a review of recent knowledge on insects as producers of protein and fat for animal feeds Laura Gasco1, Irene Biancarosa2,3, Nina S. Liland3
1 Department of Agricultural, Forest and Food Sciences, University of Turin, largo P. Braccini 2, 10095 Grugliasco, Torino, Italy 2 University of Bergen, Department of Biology, Thormøhlensgt. 53 A/B, P.O. Box 7803, 5020, Bergen, Norway 3 Institute of Marine Research, P.O. Box 1870 Nordnes, 5817 Bergen, Norway
Corresponding author: Laura Gasco, Department of Agricultural, Forest and Food Sciences, University of Turin, largo P. Braccini 2, 10095 Grugliasco, Torino, Italy. Email: [email protected]
Abstract The use of insect-derived products in animal feed is a field of growing interest. Applying the Circular economy principle, insects efficiently bioconvert organic waste into new products enabling advantages and value at different steps: reduction of waste management costs (landfilling, anaerobic digestion, incineration) lower resource use than other protein and fat productions, and value gain from the sale of insect-derived. After introducing the potential use of insects to upgrade food waste for animal feed purposes and briefly discussing the feed sector and the regulations that govern and limit the insect mass production and uses, this review presents the latest and most interesting research (from 2019) on the use of insect as feed.
Keywords: Insects, waste, circular economy, protein, compound feed,
Introduction: Food waste and animal feed– insects as part of the solution? Globally, about one third of all the food produced for human consumption is lost or wasted within the food supply chain [1]. This corresponds to approximately 1.3 billion tonnes of food getting wasted every year but also to a tremendous loss of resources that have been invested in producing food (e.g. waters, land, fossil fuels). At the same time, the compound feed industry exceeded one billion tonnes of production in 2018, generating a turnover of more than € 360 billion [2]. Within the European Union (EU), this represent about 165 million tonnes of production and € 49.3 billion of commercial feed purchases [3]. To meet the demand for food of animal origin from an increasing world population, the global compound feed market will likely continue to expand for years to come. Such an increase in the production of feed ingredients will add pressure to limited resources such as land, water and energy. An intensification of the feed sector will therefore require new strategies to maintain a sustainable production. In the last years, the concept of a “circular economy” has taken hold in most
countries to fight food waste: that is an economic system which maintains values of waste through its use and reuse [4], and this way of thinking is also becoming more popular among feed producers. Today, finding sustainable raw materials is a major obstacle and has become a priority among the feed stakeholders.
In contrast to a “circular economy”, a traditional “linear economy” historically follows the “take-makedispose” step-by step plan. In this context, food production follows a linear process through food producers, distributors and consumers, and the remain is finally discarded. Following specific countries regulations, some of these wastes could be used as animal feed but are more often sent to landfills. Regulations on animal feeds to ensure the food safety, are now more stringent, making the unformal “from table to animal” way of using waste no longer an option. By using our food waste to grow insect larvae, which can further be used in animal feeds, the nutrients and energy in the waste can be conserved. Many insect species can efficiently, and with low environmental impact, convert typical food waste like bread, cereals or other relatively lowvalue products into protein and fat [5]. In that way, insect production can become a stream of high-quality feed ingredients, already being used with success in animal feed formulations [6,7]. Finding sustainable ingredients to produce animal feeds is a major obstacle in animal production and has become a priority among the feed stakeholders, thus being the perfect market for insect ingredients. The possibility to use or to upgrade food waste for animal feed purposes using insects, is a perfect example of how a system based on the principles of circular economy can be constructed. The field of using insects as feed ingredients is very dynamic and fast-moving today, with a great amount of studies being published each year. While previous reviews focus on the complete historical literary knowledge on this field [6,7,8], this review focuses on only the very newest information published from 2019. A special emphasis is put on the use of insect raw materials produced on different organic waste streams for fish and non-ruminants feed formulations.
Feed for insects and insects as feed – European legislation The main aim of the food production chain is to produce nutritious and safe food for the consumers, which means to ensure “food safety”. When food comes from livestock animals, it is also necessary to provide nutritious and safe feed for the animals, that is to guarantee “feed safety”. Feed and Food safety regulations are therefore in place to ensure that feed and food stuff do not represent a danger to human health, animal health or the environment. Recently, the EU adopted the “Circular Economy package” where it defines which food, no longer intended for human consumption, is suitable for feed production. Within this context, in the EU, the use of catering or animal waste is forbidden, while in other countries different legislations are in force [9]. In the EU, insects are considered full-fledged “farmed animals”-i.e. animals that are kept for the production of food, feed or other derived products [(Reg (EU) 2017/893)]. Like other farmed animals, insects can only be fed on authorized substrates like “feed grade materials” (e.g. plant-based materials, vegetable and fruit residues, wheat bran, grass and brewery byproducts, hay, among others). However, outside EU, regulations on feeds for insects are less stringent. Research on the use of insect-based feed ingredients for farmed animals has developed rapidly in the last 5 years, leading to the authorization of insect processed animal protein (PAP) in feed for farmed fish in 2017 [Reg. (EU) 2017/893]. However, this regards only a few insect species: Black soldier fly (Hermetia illucens - BSF), Common housefly (Musca domestica - HF), Yellow mealworm (Tenebrio molitor - MW), Lesser Mealworm (Alphitobious diaperinus), House cricket (Acheta domesticus), Banded cricket (Gryllodes sigillatus) and Field cricket (Gryllus
assimilis). For other livestock (poultry, pigs) the “feed ban” [Reg .(EC) 999/2001] still limit the use of insect PAP but the rule could be soon relaxed [10]. There are no limitations on the use of fats derived from insects. In other countries such as Canada, BSF meals are also allowed for poultry. Moreover, in countries such as China or South Korea, no limitation applied. Under EU regulation, the “feed ban” do not apply to carnivorous fur producing animals that can be fed processed animals proteins, including insect-derived proteins.
Insects grown on waste material In the EU only selected types of waste materials of vegetable origin are allowed for use in insect production, leading to some concerns about sustainability, as products which could be used as animal feed or human food will have a higher environmental impact than when using organic side streams [11,12,13]. It has to be pointed out that technologies used to produce insects are still in their infancy, and there is large space for improvement, both regarding the type of substrate used to grow insects and the technology involved in an efficient large-scale production. Among the insect species assessed for aqua and livestock feeds, the most interesting are: the BSF [14,15,16], the HF [17] and the MW [18,19]. These species have a fast growth and are efficient at converting a variety of organic waste to protein and lipids. There are several studies showing how it is possible to be innovative with regards to the use of local waste, using campus restaurant food waste [20], fruit and vegetable waste from a wholesale market [21] or kitchen waste substrate [22] to produce insects. The concentrations in protein and other nutrients in the whole insect is affected by the general growth of the insects on a given media. Nevertheless, a general tendency seen is that the protein meal in itself won’t be affected in it’s quality, although the amount or ratio protein/fat might vary, A general tendency seen when growing insects is that the protein fraction of the insects will mainly stay the same, regardless of the substrate they grow on, while major changes are seen in the lipid fraction (fatty acid profile), mostly mirroring the lipid composition of the substrate [23,24]. As pointed out by Danieli and colleagues, it is essential to know the optimum dietary composition of the selected insect species, as a sub-optimal diet can lead to a prolonged production time as well as a less efficient nutrient retention.
Insect-based ingredients in compound feeds Among the ingredients used to produce compound feeds, those rich in proteins constitute the most important and expensive part of the diet. In particular, animal derived feedstuffs provides highly digestible proteins with great biological value. A wide array of studies, with an especially large increase in published studies the last few years, have proven the suitability of insects as a high-quality source of nutrients for animal feeds [5,6,7,9]. When formulating diets, the digestibility and nutritive value of ingredients is of primary importance to obtain diets able to cover animal requirements, and to optimize performances and costs. However, only a few published studies that deal with the determination of nutrient digestibility coefficients of insect meals in fish and livestock are available (Table 1). More abundant is the number of papers reporting results, in terms of digestibility, animal performance or parameters such as somatic indexes, whole body or fillet /meat composition, of diets containing different levels of insect meals (Table 2). By using insect ingredients, comparable animal growth and performance as other commonly used feed ingredients can be obtained. Attention must, however, be paid to cover the animal’s requirements of essential amino acids (EAA), as most insect species are low in some EAA (typically tryptophan and sulfur amino acids like methionine [6] which might need to be supplemented to the diets. Some species are also more tolerant to a higher inclusion of insect-based ingredients than others, so a species-specific approach should be taken into account when formulating diets.
Apart from insect-derived proteins, another interesting insect product for animal nutrition is the lipid fraction (recent results reported in Table 3). Some trials have substituted up to 100% of the lipid source in the control diet without changes in performance or digestibility. There are, however, some studies showing a negative effect from the lipid fraction of the insect ingredients [17]. This shows the importance of knowing more about the tolerance of each species to different insect ingredients in the diets. Although the growth of animals using insect ingredients is generally good, there are studies showing that insect meals or -fat in animal diets can influence the quality of derived-products (fillets, meat, eggs) in terms of proximate composition, fatty acid profile, or physical traits [25,26]. Nevertheless, not all results indicated an effect on quality [14], highlighting the need for more investigations research on the quality of products from insect-fed animals.
Insect ingredients with health-promoting properties There is substantial evidence that the use of diets with insect meals could have positive effects on animals’ immune system and microbiota [27] and recent results are reported in Table 4. The increased diversity in microbiota has been attributed to the content of chitin in insect meals, which is not digestible in most animals and promote growth of certain groups of bacteria, with positive effects on gut health. Insect chitin is also endorsed with immunostimulating effects [27]. The lipid component of insects has also been shown to have a positive effect on animal health, especially the high concentration of lauric acid in BSF [27]. In addition insect fat are a fast substrate for energy and promote less lipid storage in the liver [15]. Insect-derived-products have also been shown to have anti-microbial effects [28,29]. Conclusions The mass production of insects on waste can help to reduce the environmental impact of food waste as well as generate a sustainable novel feed ingredient for the animal-feed sector. Applied research shows promising results and insect-derived products are currently recognised as one of the most interesting and sustainable sources of nutrients. Insect-derived products also show potential as health enhancers, being a possible source of ingredients for feeds targeting specific challenges or life stages in animal production. Nevertheless, this industry is still in its infancy and further research and a clear legal framework is needed for the complete development of the sector.
Table1. Nutrient’ apparent digestibility coefficients (ADC) of insect meal as ingredient vs a Reference diet Animal (IBW, g) [digestib ility method]
Insect species and form
Mandarin fish (31.27 g) [sediment ation column] Nile tilapia (3.0 g) [Guelph system]
Full fat maggot meal
Atlantic salmon (300 g) [sediment ation columns] European sea bass (33 g) [Guelph system]
% Insect inclusion
Nutrient digestibility
General comments
Main ingredie nt of the REF diet
DM
CP
EE
GE
FM: 53%
69.76
83.93
80.28
69.56
68.46
82.59
78.61
71.99
95.8
85.4
90.6
82.1
ZMM
83.2
70.0
93.5
80.1
GAM
42.6
39.7
87.9
47.0
NCM
61.7
69.6
91.6
58.4
GPM
48.2
61.6
98.8
47.4
15 30
Full fat MWM
20
-
Influence of the level of inclusion on nutrient ADCs Higher CP and AA but lower EE digestibility compare to plant that of plant protein ingredients
[30]
Good digestibility of all meals, some interactions with chitin content.
[31]
BSFM
30
FM: 33.5%
87
89
97
88
Digestibility trial also performed against SBM and CPC. ADC of BSFM was generally over 75%, with DM & GE showing higher coefficients in BSFM than CPC and SBM. Mineral digestibility was generally higher in BSFM compared with CPC and SBM.
[32]
Full fat BSFM Defatted BSFM Full fat MWM Defatted MWM LM
20
FM: 45%
48.3 53.7 85.2 72.4 40.1
75.8 87.2 89.2 92.8 74.1
91.4 92.7 94.5 94.4 66.5
67.2 64.8 79.2 84.4 53.0
ADCs of all AA were assessed. The two MWM had the highest digestible total amino acid. Authors highlighted the importance of the defatting process to increase the nutritional value of insect meals
[33]
Abbreviation. REF: reference diet; DM: dry matter; CP: crude protein; EE: ether extract; GE: gross energy; AA: amino acid; FM: fishmeal; PBP: poultry by-products; CPC: corn protein concentrate; MWM: yellow mealworm meal; BSFM: black soldier fly meal; LM: locust meal; ZMM: Zophobas morio larvae meal; GAM: Gryllus assimilis meal; NCM: Nauphoeta cinerea meal; GPM: Gromphadorhina portentosa meal; SBM: soybean meal; ADC: apparent digestibility coefficient.
Table 2. Effects of dietary inclusion of insect meals on fish and livestock performances (whole cycle), nutrients digestibility and other parameters. Animal species (diets form) [IBW, g] {n° days}
Insect species and form
Atlantic salmon (Extruded) [1398 g] {114}
Partially defatted BSFM
Atlantic salmon (Steam pellet) [2800 g] {112}
BSFM
Insect composition (% DM)
CP
CL
52
12
58.65
12.37
% insec t inclu sion
CTRL diet: % of main protein substitute d
worsened 4.91; 9.85; 14.75
FM: 10 SPC: 25 CGM: 7.5; PPC: 8.8
10
FM: 10; CPC: 17.2; PBP: 18.5; BM: 15
20 30
Magree (Dry pellet) [18.0] {63}
Partially defatted BSFM
55.4
10.9
10; 20
WG; SGR; TGC; FCR; PER FM: 40
30
Sea trout (Extruded) [0.14 g] {60} Japanese seabass (Extruded)
Full fat MWM; full fat hydrolys ed MWM Defatted BSFM
vs CRTL diet with no insect meal
no differences FBW; WG;DGI; SGR; FI; FCR
29.6
20
FM: 30.6
61.42
1.77
4.8; 9.6
FM: 25
improved No effect on ADC of CP, CL, AA & FA. No effects on WBC for CP, CL & AA. FA WBC reflects that of diets. Small changes in fillet sensory quality. No differences in digestive enzyme activities -
WG; SGR; TGC; FC; FCR; PER WG; SGR; TGC; FC; FCR;PER FC
[14]
[32]
Linear decrease trend for FE, PER, NR and ER with the increase of BSFM dietary inclusion reflects the lower growth performance without differences in FI. Whole body ash linearly decreased with the increase of BSFM. No differences for all other WBC parameters. No differences for HSI & VSI. Increase in saturated FA and decrease in unsaturated FA. Plasmatic total lipid and triglycerides linearly decreased with the increase of BSFM. No differences for plasma glucose, cholesterol and total proteins.
[34]
SR; SGR; RGR; FCR; PER
Increase of VSI in fish fed MWM treatments. No differences for intestinal amylase, lipase and trypsin.
[35]
SR; FBW; WG; FI; FCR; SGR; PR; LR
No differences for somatic indexes No effect of diets on trypsin, lipase and amylase in the hepatopancreas.
[22]
FBW; DGI; FI; FE; PER; NI; NR; LI; LR; EI; ER
FI; FE; PER; NI; LI; LR; EI; ER
47.0
Other parameters recorded & comments
FBW; DGI, NR
[14.14] {56}
14.4; 19.2
Rainbow trout (Extruded) [5.01 g] {90}
Partially defatted MWM
Rainbow trout (Cold pellet) [137.3 g] {98} Rainbow trout (Extruded) [78.3 g] {154}
Full fat BSFP
67.1
13.6
39.00
41.86
Partially defatted MWM
-
Siberian sturgeon (Cold pellet) [24.2 g] {118}
Highly defatted BSFM
65.84
Climbing perch (Pellet) [2.2 g] {123} Nile tilapia (Commercial + spray) [2.1g] {49} African catfish (Pellet) [4.0] {60}
BSFP
FI (increased)
10.5; 21
FM: 42
SR; FBW; WG; SGR; FCR
-
5; 10; 20
FM: 20
SR; FBW; WG; SGR; FCR; PER; FI
Decrease in ADC of CP with the increase of MWM but values always higher than 97%. No differences for ADCs of DM, EE and GE Higher HSI in fish fed 20% of MWM. No differences for K and VSI. No effects on hepatic amino acid catabolic and lipogenic enzymes.
[19]
4.24
18.5
FM: 70
SR; FBW; WG; SGR; FCR; PER FCR; PER
Decrease in ADC of CP, but values always above 86% No differences in HSI, VSI and K. Increase of whole body EE content in fish fed 37.5% of BSFM
[37]
SR; FBW; WG; SGR; FCR SR; FBW; WG; SGR; FCR SR; FBW; WG; SGR; FCR; SR; FBW; WG; SGR; FCR; PER SR; FBW; WG; SGR; FI; PER; FCR SR; FI
Diets containing insect were also increasing reduced for CP and EE content BSFP protein can be better assimilated by climbing perch than FM BSFP % were substituted (sprayed) to a commercial diet.
[38]
14.9
FBW; WG; FC; SGR FM: 23
43.67
28.37
3
-
6; 9 Partially defatted BSFM
42.6
23.0
5.72
FM: 15
11.45 17.18
Nile tilapia (pellet) [2.08g]
FC
29 Full fat BSFP
MWM
-
[18]
FM: 25
6.1
FBW; SGR; FCR; FI; PER; PR; ER
Higher activity of intestinal lipase in fish fed 14.4% and 19.2% of BSFM than those of fish fed other diets. No effects on ADC. No differences in fish WBC. Higher FBW in fish fed 7.5% and 15% diets vs 5%. Phosphorous retention only improved in 7.5 & 15% diets. Diets also included PPC and WGM which increased with BSFP inclusion
5; 7.5; 15; 25
37.5 59.1
SR; FBW; WG; FCR; SGR; PR; LR
-
5, 10, 15, 20
SBM: 46.97
PER
PER, PR
FBW; WG; SGR; PER; FCR
Higher whole-body protein recorded in fish fed 11.45 BSFM inclusion. No differences for somatic indexes. Higher whole body protein content in fish fed 11.45% of BSFM than other treatments.
SR; FBW; WG; SGR; FI; PER; FCR FBW, WG, SGR, FCR, erythrocytes, HSI and WBC (DM & EE): linear effect when inclusion levels increased. Polynomial models and Plateau Linear Responses were applied to survival and productivity (kg
[36]
[39]
[40]
[41]
{42} Muscovy duck {50}
Partially defatted BSFM
56.71
10.70
3, 6, 9
CGM: 9
Broiler quails {29}
BSFM1 (reared on layer mash) BSFM2 (reared on 50:50 layer mash and fish offal) Defatted BSFM
36.04
36.38
10
SBM: 46
36.48
39.04
10
55.55
11.11
2.5; 5; 7.5; 10
Laying quails {42}
BSFM
54.75
15.64
10; 15
Weaning pigs {61}
BSFM
59.0
8.97
Jumbo quails {42}
5; 10
m−3) indicating maximum values of 11.68% and 10.68% of MWM inclusion, respectively. Higher levels decreased growth and performance and increased mortality. DFI; FCR FBW Three feeding periods. In the start phase, CP & EE digestibility linearly decreased (minimum at 9 of BSFM inclusion). In the two other phases, EE digestibility linearly increased (maximum at 9% of BSFM inclusion). Quadratic response to increasing BSFM in the grower period (minimum at 6% of BSFM inclusion). SR; FBW; WG; FI; FCR FBW; WG
Soy oil cake: 19.3; Full fat soya: 7.4 SBM: 35.9
SBM: 20 (phase I) 18.5 (phase II)
[42]
No differences in ADC for CP and Chitin. Higher ADC for DM, OM and GE for BSFM2 but lower ADC for EE if compared to CTRL diet. Higher ADC for GE in both BSFM diets.
[43]
FBW; WG; FI
Quadratic effect for WG and FI: regression indicated an optimum BSFM inclusion of 5.4%.
[44]
SR; FBW; FCR; Eggs production; Egg mass; Defected eggs
BSFM increased shell weight and percentage, and increased yolk colour. BSFM decrease CP and increased ash eggs content. No effect on eggs cholesterol content. Increase in saturated FA and decrease in polyunsaturated FA. No effects on sensory attributes (odor, aroma, taste) of both yolk and albumen. No effect on ADC od DM and OM. ADC CP: linear decrease in phase I. ADC EE: linear increase in both phases. ADFI in phase II showed a linear response to increasing BSFM levels with the maximum for the 10% of BSFM inclusion.
[45]
SR; FI; FCR
WG, ADG; ADFI; FCR
[16]
Abbreviations. AA: amino acids; ADC: apparent digestibility coefficient; ADFI: daily feed intake; ADG: average daily gain; BM: blood meal; BSFM: black soldier fly larvae meal; BSFP: black soldier fly prepupae meal; CGM: corn gluten meal; CL: crude lipid; CP: crude protein; CPC: corn protein concentrate; CTRL: control diet; DGI: daily growth index; DM: dry matter; DMI: dry matter intake; EE: ether extract; EI: energy intake; ER: energy retention; FA: fatty acids; FBW: final body weight; FC: feed consumption; FCR: feed conversion ratio; FE: feed efficiency; FI: feed intake; FM: fishmeal; GE: gross energy; HSI: hepatosomatic index; IBW: initial body weight; K: condition factor; LI: lipid intake; LR: lipid retention; NI: nitrogen intake; NR: nitrogen retention; OM: organic matter; PBP: poultry
by-product meal; PER: protein efficiency ration; PPC: Pea protein concentrate; PR: protein retention; RGR: relative growth rate; SGR: specific growth rate; SPC: soy protein concentrate; SR: survival rate; TGC: thermal growth coefficient; MWM: yellow mealworm larvae meal; VSI: viscerosomatic index: WBC: whole body composition; WG: weight gain; WGM: wheat gluten meal.
Table 3. Effects of dietary inclusion of insect oils/fat on fish and livestock performances (whole cycle), nutrients digestibility and other parameters Animal species [n° days]
Insec t speci es
% insect inclusion
CTRL diet: % of main lipid substituted
performances vs CTRL no insect oil/fat
decrease Broiler [30]
MWO
5
PF or PO
no differences WG; FI; FCR
Turkey [35]
BSFF
2.5 & 5
SBO: 5
WG; FI; FCR
Rabbits [41]
BSFF & MWO
0.75 & 1.5
SBO: 1.5
SR; FBW; ADG; ADFI; FCR, Morbidity
Digestibility and other parameters
improve d Reduction of relative weight of liver in MWO vs PF. No differences on Apparent ileal digestibility of CP, CF and AMEn. No influence on lipase and trypsin activity. MWO decreased the amylase activity vs PF. MWO decreased TG in blood vs PF. MWO decreased TG and total cholesterol in liver vs PF. In breast muscle, MWO influenced the content of SFA, MUFA and PUFA. No differences on apparent ileal digestibility of CP, EE and AMEn. 5% of BSFF decreased trypsin activity but without effects on digestibility. No influence of BSFF & MWO on digestibility of nutrients and energy.
[46]
[47]
[48]
Abbreviations. ADFI: daily feed intake; ADG: daily weight gain; AMEn: apparent metabolizable energy corrected to zero nitrogen balance; BSFF: Black soldier fly fat; CF: crude fat; CP: crude protein; CTRL: control diet; EE: ether extract; FBW: final body weight; FCR: feed conversion ratio; FI: feed intake; MUFA: monounsaturated fatty acids; PF: poultry fat; PO: palm oil: PUFA: polyunsaturated fatty acids; SBO: soybean oil; SFA: saturated fatty acids; SR: survival rate; TG: triglycerides; MWO: yellow mealworm oil; WG: weight gain.
Table 4. Effect of insect products on animals’ immune system, microbiota, blood parameters and intestinal structure. Animal (IBW - FBW, g) [days of trial]
Insect species form
Rainbow trout (201–275 g) [35] Rainbow Trout (66–220 g) [84]
BSFP or defatted-BSFM
% Insect inclusion in diet (main substituted ingredient % in CTRL diet) 30 (FM: 50)
Partially defatted BSFM
10, 20 & 30 (FM: 60)
Rainbow trout (137-300 g) [98] Rainbow trout (78–413) [154] Rainbow trout (115–270 g) [90] Seabass (5–17 g) [70] Seabream (105-238 g) [163] Sea trout (0.14–1.20 g) [60]
Full fat BSFP
10.5 & 21.0 (FM: 42)
Partially defatted MWM
5, 10 & 20 (FM: 20)
Full fat MWM
60 (FM: 70)
Siberian Sturgeon (640-1200 g) [60] Siberian sturgeon (24–150 g) [118] African catfish
and
Effects vs CRTL diet and comments
Increased diversity (higher abundance of phyla Firmicutes and Actinobacteria with lower abundance of Proteobacteria). The life-cycle stage of insect influenced the composition of gut bacteria Insect meal positively modified intestinal microbiota diversity. The beneficial lactic acid-and butyrate-producing bacteria where increased with possible positive repercussion on fish health. The probiotic effect was mainly attributed to fermentable insect chitin. Illumina high-throughput sequencing detected increased intestinal biodiversity with a reduction in Proteobacteria and an increase of the gut abundance of Mycoplasma Highest insect content lead to increase in genetic markers of stress and inflammation as well as an increase in liver lipids and shortening of intestinal folds in both insect groups No effects on hepatic amino acid catabolitc and lipogenic enzyme activity.
[20] [21, 49]
[36]
[19]
A differential shift in the dominant bacterial in the gut of each species was recorded with a more pronounced effect on gastrointestinal microbiota in saltwater than in freshwater species
[50]
50 (FM: 70) 50 (FM: 50) Full fat MWM; full fat hydrolysed MWM Full fat BSFM and MWM
20 (FM: 30.6)
No differences for liver ALT and AST.
[35]
15 (FM: 26)
[51]
Highly defatted BSFM
18.5 & 37.5 (FM: 70)
Changes in intestinal flora and structure of intestine with a reduction and an increase of the mucosa thickness for fish fed BSFM and MWM, respectively A different influence on the microbiota population was recorded for BSFM and MWM No influence on the liver and distal intestine histology. Alterations of the oxidative stress biomarkers were detected at 37.5% inclusion of BSFM meal.
Partially
5.72,
No differences for blood parameters and differential leucocyte counts.
[40]
11.45
&
[52]
(4-15g) [60]
defatted BSFM
17.18 (FM: 15)
Atlantic salmon (1400 – x g) [56] Japanese seabass (14-60g) [56]
Partially defatted BSFM
14.75 (FM: 10.5)
Defatted BSFM
4.8, 9.6, 14.4 & 19.2 (FM: 25)
Broiler [40]
Full fat MWM
5, 10 & 15 (SBM & CGM)
Broiler [35]
Partially defatted BSFM
5, 10 & 15 (SBM & CGM)
Turkey [35]
BSFF
2.5 & 5 (SBO: 5)
Lowest serum total protein, globulin, glucose, triglycerides, total bilirubin for fish fed 11.45% of BSFM. Lowest AST and ALT in fish fed 11.45% BSFM. Decrease in ALP activity in fish fed all BSFM diets. Similar MDA content vs CTRL Higher CAT in fish fed 11.45 and 17.18% of BSFM Lower SOD in all BSFM treatments. No alteration in gut health Decrease in triacylglycerol and in MDA. No influence on non-specific immune indexes. No alteration on hepatic and intestinal histomorphology. Up-regulation of hepatic lipoprotein lipase and hormone sensitive lipase and downregulation of fatty acid synthase genes (likely due to chitin) Decrease in the relative abundance of Firmicutes phylum and lower Firmicutes:Bacteroidetes ratios in birds fed 10 & 15% MWM. Increase in the relative abundance of Clostridium, Alistipes and Sutterella genera in MWM chickens. Decreased in the relative abundance of Ruminococcus genus in MWM groups. Higher mucin staining intensity in the intestinal villi of birds fed 5% MWM than the other MWM groups, and a mucin reduction in the intestinal villi of birds fed 10% MWM compared to CTRL. 5% of BSFM inclusion positively influenced either the cecal microbiota or the intestinal mucin dynamics in terms of preservation of physiological microbial populations, selection of potentially beneficial bacteria and increase in villi mucins. High inclusion levels (in particular the 15%) may have a negative influence in terms of partial reduction of the microbial complexity, reduction of potentially beneficial bacteria, selection of bacteria with mucolytic activity and decrease in villi mucins Total replacement of SO reduced proliferation of potentially pathogenic bacteria (Enterobacteriaceae spp) , MWO decreased interleukin-6 and tumour necrosis factor–alpha.
[53] [22]
[54]
[55]
[47]
In blood, 5% of BSFF increased total cholesterol, HDL and LDL while no effect on ALT, AST, TG, glucose, total protein and albumin were reported for BSFF groups Laying hens [168]
Partially defatted BSFM
7.3 & 14.6 (SBM: 26.5)
Muscovy ducks [50]
Partially defatted BSFM
3, 6 & 9 (CGM: 9)
No differences in TG and cholesterol in turkey meat (breast and leg). The highest level of BSFM inclusion reported a decrease in ileal villi height, and a reduced duodenal maltase and intestinal alkaline phosphatase activity. This group also showed the highest acetate and butyrate levels No effects on the intestinal morphometric indices (villus height, crypt depth & villus height-to-crypt depth. No influence on histological features of spleen, liver, thymus and Bursa of Fabricius
[56]
[42, 57]
and on haematological parameters. TG and cholesterol levels showed a linear decrease with the increase of BSFM inclusion. Jumbo quails [42]
Defatted BSFM
Rabbit [41] Piglets [61] Finishing pigs [46]
BSFF and MWO Partially defatted BSFM Full fat BSFP
2.5, 5, 7.5 & 10 (Soy oil cake: 19.3; Full fat soya: 7.4) 0.75 & 1.5 (SBO: 0.75 & 1.5) 5 & 10 (SBM) 4&8 (SBM: 16.98)
No linear nor quadratic effects for all the blood parameters, except for the Albumin/Globin ratio.
[44]
No negative effects on gut morphology, blood parameters
[48]
No negative effect blood profile, gut morphology or histological features.
[16]
Dietary inclusion of BSFMl may enhance mucosal immune homeostasis of pigs via altering bacterial composition and their metabolites
[58]
Abbreviations. ALP: Alkaline phosphatase; ALT: Alanine aminotransferase; AST: aspartate aminotransferase; BSFF: black soldier fly fat; BSFM: black soldier fly meal; BSFP: black soldier fly prepupae meal: CAT: Catalase; CGM: corn gluten meal; CTRL: control diet; FBW: final body weight; FM: fishmeal; HDL: high-density lipoprotein; IBW: initial body weight; LDL: low-density lipoprotein; MDA: Malondialdehyde; SBM: soybean meal; SBO: soybean oil; SOD: Superoxide dismutase; TG: triglycerides; MWM: yellow mealworm meal; MWO: yellow mealworm oil.
Conflict of interest statement Nothing declared.
Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author contributions All authors equally contributed to the conceptualization, writing, review and editing of this paper. XX Acknowledgements Authors thanks the SUSINCHAIN (SUStainable INsect CHAIN - GA n. 861976 - H2020_IA) project.
References Papers of particular interest, published within the period of review, have been highlighted as: * of special interest
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