Insects as Novel Ruminant Feed: Comparison
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In the last decade, there has been a growing interest in using edible insects as animal feed due to their high nutritive value and environmental advantages over the conventional livestock feeds. Insects have been used in the diets of some animals (poultry, fish, and swine) however, their evaluation in ruminants is still limited. The current in vitro study evaluated the usage of four different kinds of edible insects to partially substitute soybean meal as an example to the conventional high-quality expensive protein sources in ruminants’ diets. This study showed that the evaluated insects had high protein and fat contents. Substitution of 25% of soybean meal with the tested insects in a ruminant diet had no adverse effect on rumen fermentation profile or nutrient digestibility. Moreover, the inclusion of some species in the diet led to reduction of the methane production up to 16-18% which is an additional environmental benefit. The findings of this study are encouraging for further work in this promising area to improve the sustainability of livestock industry.  

  • alternative protein sources
  • fatty acids
  • insects
  • methane
  • rumen fermentation
  • soybean
  • sustainability

1. Introduction

Global food production systems are facing the great challenge of responding to the dramatic increase in the human population and meeting the growing demand for food [1]. According to the United Nations, the world will be home to approximately 9 billion people by 2050; therefore, the demand for meat and milk is expected to increase to levels that are 58% and 70% higher than those in 2010, respectively [2]. Although livestock, especially ruminants, are one of the main important sources of animal products, this sector is responsible for approximately 14–18% of anthropogenic greenhouse gases (GHG), such as methane (CH4) and carbon dioxide (CO2) [3]. Moreover, the livestock industry is considered a hungry resource; it occupies approximately 70% of the agricultural land and consumes 8% of the world’s water [4]. Therefore, any increase in animal products is severely challenged by land degradation and GHG emissions [5]. Additionally, feed cost is one of the major constraints for further development in the livestock production industry. The cost of feed is approximately 70% of the total budget, and the required protein amounts account for over 15% of the total feed cost [6]. Typically, soybean meals are the major protein source and are commonly used in ruminant diets due to their high contents of protein and essential amino acids [7]. However, soybean production is also associated with high environmental impacts [8], and its price has been increasing with some fluctuations [9]. Therefore, to meet the increasing demand for animal products in the near future, innovative solutions and alternative sustainable ingredients to replace the conventional protein in animal diets with a reduced impact on the environment are urgently required.
In recent years, the use of edible insects to substitute or reduce other expensive high-quality feed in animal diets seems to be one of the most promising solutions to the above-mentioned problems [10,11][10][11]. The production of insect biomass as animal feed has major environmental advantages over conventional sources, as insects are able to efficiently convert low-value organic by-product wastes from fruits and vegetables into sellable nutrient sources (high feed conversion efficiency), grow rapidly, require less land and water, and produce lower GHG emissions [12,13][12][13]. Moreover, insects are characterized by their high protein (42–63%) and fat (10–40%) contents, making them ideal candidates for animal diets [10,14][10][14]. Additionally, the use of insects as animal feed is likely to be more widely accepted, as it could provide a valuable opportunity to develop a novel product [15,16][15][16]. Research interest in this field is still in its infancy; however, in the last few years, there has been increasing interest in both the economic sector and scientific community [17,18][17][18].
Although no data are currently available on the rearing of insects on a commercial scale, the commercial farming of insects such as crickets for the feed market is developing in many countries, and it is projected that insect meal production will increase to 1.2 million tons by 2025 [11]. During the last five years, the number of articles detailing the usage of edible insects in animal diets has substantially increased [12]. Several published papers have shown that insects could be used as a feed ingredient to partially or completely replace soybean meal and fishmeal, such as in broiler chicken [19], laying hen [20], free-range chickens [21], quail [22], rabbit [23], swine [24], as well as carnivorous [25] and omnivorous fish [26] diets. However, evaluation of their utilization in ruminant diets is still limited to date which is related to the potential risk of mad cow disease (Bovine Spongiform Encephalopathy). The European Union regulations prohibit the use of processed animal protein to feed food-producing animals [27]. The European Union allows the usage of insect as a feed in aquaculture since July 2017, with a recent approval from the European parliament and Council, and the Standing Committee on Plants, Animals, Food and Feed in April 2021 for the usage of insects to feed poultry and pig [28]. The prohibition of insect usage as ruminant feed is also currently applied in most of the developed countries (USA, Canada, China, and Japan). In contrast, many countries, including the developing ones, have less clear or no specific laws for the usage of insects as ruminant feed [15]. Legal rules on the use of insects as feed vary across the world, but there is noticeable interest among researchers and feed producers all over the world for further innovation and research in that promising area. This would lead to changes in the countries’ regulations to allow the use of insects as ruminant feed in the near future. Importantly, prior to establish a new livestock industry based on insects as feed, the safety of insects and the substrate on which they are reared should be carefully considered.

To the best of our knowledge, two studies have been conducted in ruminants evaluating the use of black soldier fly larvae (Hermetia illucens), Jamaican field crickets (Gryllus assimilis), and mealworms (Tenebrio molitor) as a substitute for soybean meals on the rumen fermentation profile, digestibility, and CH4 production [29,30][29][30]. These in vitro studies reported that substitution of soybean meal with the tested insects reduced CH4 production but had a lower nutritional value in terms of lower in vitro dry matter digestibility and production of volatile fatty acids due to the higher chitin content. Therefore, there is a need to determine the optimal inclusion levels of insects in ruminant diets to achieve favourable nutritional, economic, and environmental benefits. It has been reported that there are many insect species that may be well suited for use as feed ingredients [31,32][31][32]. Therefore, the current study was conducted to evaluate the inclusion of different kinds of edible insects, e.g., Acheta domesticus, Brachytrupes portentosus, Gryllus bimaculatus, and Bombyx mori, as partial substitutes for soybean meal. We hypothesized that inclusion of lower levels of these insect species to partially replace soybean meal might not have adverse effects on the rumen fermentation profile. To the best of our knowledge, this is the first study reporting the comprehensive chemical analysis of these insects and evaluating their effects on the rumen fermentation characteristics, nutrient digestibility, and CH4 production when used as partial substitutes for soybean meal in a ruminant diet.

2. Chemical Composition

The proximate analysis showed that the four kinds of insects had a higher protein percentage (61.3%, 53.3%, 56.5%, and 52.4% for A.d, B.p, G.b, and B.m, respectively) than KG hay (10.5%) and SBM (48.3%). The results for the fat content were also higher (14.6%, 22.3%, 15.8%, and 26.7% for A.d, B.p, G.b, and B.m, respectively) compared with KG hay (2.8%) and SBM (2.3%) (Table 1 and Table 2).
Table 1. Chemical composition (% in dry matter) of the basal diet used for 24-h in vitro incubation.
%KleingrassSoybean Meal
Proximate analysis (% in dry matter) of the insects used for 24-h in vitro incubation.
% Acheta

domesticus		 Brachytrupes

portentosus		 Gryllus

bimaculatus		 Bombyx mori
Table 3). The insects contained all the essential amino acids, and the amino acid profiles of the insects were almost the same as that of SBM (Table 4).
Table 3.
Fatty acids profile (%) of soybean meal and insects.
Fatty Acid Soybean Meal Acheta

domesticus		 Brachytrupes portentosus Brachytrupes portentosusGryllus

bimaculatus		 Gryllus

Bombyx mori
bimaculatus Bombyx mori
Treatments SEM p-Value
Kleingrass Soybean Meal Acheta

domesticus		 Brachytrupes

portentosus		 Gryllus

bimaculatus		 Bombyx mori
-N (p < 0.01), except for when G.b was included, as this value was comparable to the 60% KG + 40% SBM (p = 0.98) and 100% KG (p = 0.36) diets (Table 6).
Table 6. Effect of substituting soybean with insects on pH, digestibility, and NH3-N from 24-h in vitro incubation (n = 12).
Treatments    
Parameter Kleingrass Soybean Meal

5 NH3-N: ammonia-nitrogen. SEM: Standard error of the mean. a, b, c Values with different superscripts in the same row are significant different (p < 0.05).

5. Volatile Fatty Acids Production

The 60% KG + 40% SBM diet had an improved fermentation profile in terms of the concentration of different VFA and the production of total VFA, but the A/P ratio decreased when compared with the 100% KG diet (p < 0.01). Substitution of 25% of the SBM in the basal diet with all the tested insects had no effect on either the concentration of different VFA or the total VFA production compared with the 60% KG + 40% SBM diet (p > 0.05, Table 7).
Table 7. Effect of substituting soybean with insects on VFA production from 24-h in vitro incubation (n = 12).
Treatments    
Parameter Kleingrass Soybean MealAcheta

domesticus		 Brachytrupes

portentosus		 Gryllus

bimaculatus		 AchetaBombyx mori

SEM		 p-Value
domesticus
Brachytrupes

portentosus Gryllus

bimaculatus Bombyx mori SEM p-Value
Dry matter (in fresh matter)91.6988.16
Dry matter (in fresh matter) 95.57 96.13 95.55
Essential amino acids
Gas production (mL) 30.17
pHc 40.25 a 6.59 40.29 a96.55
bc Organic matter
14:0 0.1 0.6 0.6 6.58 c40.21 a0.2 35.08 bc 36.96 ab 0.71 6.62 a
Organic matter88.8692.82
<0.001 6.61 ab 6.62 94.60 95.16 94.81 94.67
16:0 15.2 Arginine25.3 26.3 24.2 7.08 7.08 7.03 6.86
Gas production/DM 1 (mL/g) 66.30 cCrude ash11.147.18
22.0 5.67
89.92 a 88.83 a 88.33 a 77.17 bc 81.06 ab 1.59 <0.001 Crude ash 5.40 4.84 5.19 5.33
0.6
16:1 (cis-9) 0.2 Lysine 6.310.7 0.6 0.8 6.01 6.02 5.89 6.88
Gas production/d.DM 21.0 (mL/g) 171.36 b 198.99 a 194.82 a 192.43 a 177.51 b 174.58 b 2.12 <0.001 Crude protein10.54 Crude protein 61.2548.31
53.32 56.54 52.44
17:0 0.2 0.2 0.2 0.2 Histidine0.1 Ether extract2.752.33
Ether extract 14.63 22.29 15.82 26.71
Neutral detergent fibre
39.31
40.38
Acetate (mmol/L)a 18:0 4.2 8.9 11.0 7.0 6.7 Neutral detergent fibre67.4019.51
37.65 40.37 Acid detergent fibre
2.82 2.52 2.58 2.64
CO2 (%) 95.25 a 94.06 c 93.97 c3.62
93.97 c 94.58 b 94.36 bc 0.09 <0.001 Phenylalanine 5.19 3.73 3.62
78.98 c6.62 ab 0.01 CH4 (%) 4.75 c 5.94 a 6.03 a3.66 6.03 a5.07
5.42 b 5.64 ab 0.09 <0.001 18:1 (cis-9) 15.3 Tyrosine25.0 24.8 27.9 31.4 3.40 5.79 5.71 5.92
CO2 (mL) 28.72 c 37.84 Acid detergent fibre35.659.86
17.29 17.34 24.21 20.72
18:2 n-6 (cis-9,12) 52.6 36.8 34.3 Acid detergent lignin6.591.09
Table 2.
84.99
ab 85.32 <0.001
a 85.12 ab 82.47 b 84.78 ab 1.71 <0.001 IVDMD 1 (%)
6.46
38.60 b
Propionate (mmol/L)45.14 a 21.04 45.60 a b45.80 a 24.45 43.28 a a 37.85 a 37.77 ab 33.16 bc 34.84 ab 0.65 <0.001
37.1 Threonine 4.07 4.18 4.07
CH4 (mL) 1.45 c6.3 2.41 4.05 a 2.44 4.65
a 2.44 a 1.93 b 2.11 ab 0.07 <0.001 Acid detergent lignin 2.64 4.88 3.39 10.89
18:3 n-3 (cis-9,12,15) 9.8 0.8 0.9 0.9 Leucine
CH431.7 7.86 /CO2 ratio (mL/mL)7.87 0.050 d7.93 8.03 7.50 Chitin 14.65 12.46 20.82 9.83
The fatty acid profile of the insects showed that they were rich in unsaturated fatty acids (63.3%, 60.6%, 66.7%, and 70.4% for A.d, B.p, G.b, and B.m, respectively) (Table 3). The SBM was rich in linoleic acid (52.6%), oleic acid (15.3%), and palmitic acid (15.2%). The A.d was rich in linoleic acid (36.8%), palmitic acid (25.3%), and oleic acid (25%). Similarly, B.p, was rich in linoleic acid (34.3%), palmitic acid (26.3%), and oleic acid (24.8%). The G.b was rich in linoleic acid (37.1%), oleic acid (27.9%), and palmitic acid (24.2%). Finally, B.m was rich in α-linolenic acid (31.7%), oleic acid (31.4%), and palmitic acid (22%) (
0.063
ab
0.064
ab
0.064 a 0.057 c 0.060 bc 0.00 <0.001
20:0 0.3 0.3 0.3 0.4 0.3
Isoleucine 4.69 4.50 4.43 4.36 4.53
a46.22 a 1.05 <0.001
24.48 a 24.46 a 23.49 a 24.57 a 0.41 <0.001 IVOMD 2 (%) 39.27 b 47.51 a 46.08
Butyrate (mmol/L)a 49.77 a 48.15 a 8.08 45.78 a 1.54 c 9.00 ab 9.16 a 9.16 a 8.71 b 8.68 0.010
b 0.15 <0.001 IVNDFD 3 (%) 31.91 c 34.28 bc 42.99 a 45.95 a 41.09 ab 38.54 abc 1.35 0.003
IVADFD
Total VFA 14 (%) 27.50 ab 28.69 ab 34.76 ab 30.70 ab 27.26 b 35.20 a 0.96 0.016
NH3-N 5 (mg/dL) 9.33 b 11.68 b 23.89 a 18.69 a 13.03 b 19.45 CO2/DM (mL/g) 63.11 c 84.54 a 83.44 a 82.97 ab 72.93 bc 76.42 ab 1.45 <0.001 unknown 0.9 1.5 1.3 1.0 Methionine 1.40 1.76
CH41.71 /DM (mL/g)0.4
Table 4.
Amino acids profile (%) of soybean meal and insects.
Amino Acid Soybean Meal Acheta

domesticus
a
0.84
<0.001
a
183.01
a
180.76 a 167.82 b 164.64 b 1.89 <0.001
CH4/d.DM (mL/g) 8.19 c 11.87 a 11.81 a 11.67 a 9.69 b 9.94 b 0.26 <0.001

1 DM, Dry matter. 2 d.DM, Digestible dry matter. SEM: Standard error of the mean. a, b, c, d Values with different superscripts in the same row are significant different (p < 0.05).

4. pH, In Vitro Nutrient Digestibility and Ammonia-Nitrogen Production

The inclusion of different insects significantly increased (p < 0.05) the pH compared with the 60% KG + 40% SBM diet. Adding SBM to KG improved the IVDMD and IVOMD (p < 0.05), but it did not show the same effect with regards to IVNDFD and IVADFD (p > 0.05, Table 6). Substituting SBM with different kinds of insects had no effect on IVDMD, IVOMD, or IVADFD when compared with the 60% KG + 40% SBM diet (p > 0.05), while IVNDFD was improved by the inclusion of insects in the experimental diets, especially in the case of added A.d and B.p (p < 0.05, Table 6). Notably, supplementation with insects in the basal diet increased the concentration of NH3

1 IVDMD: In vitro dry matter digestibility. 2 IVOMD: In vitro organic matter digestibility. 3 IVNDFD: In vitro neutral detergent fibre digestibility. 4 IVADFD: In vitro acid detergent fibre digestibility.

(mmol/L)
108.10
b
118.44 a 118.96 a 118.74 a 114.66 a 118.02 a 2.22 <0.001
Acetate (mol/100 mol) 72.94 a 71.64 b 71.60 b 71.54 b 71.78 b 71.70 b 0.17 <0.001
Propionate (mol/100 mol) 19.53 b 20.72 a 20.66 a 20.70 a 20.59 a 20.91 a 0.13 <0.001
1.61
Butyrate (mol/100 mol) 7.54 ab 7.65 a 7.74 a 7.75 a 7.62 a 7.39 b 0.06 <0.001
3.10
A/P 2 ratio 3.75 a 3.46 b 3.48 b 3.47 b 3.50 b 3.44 b 0.03 <0.001 3.19 c 5.37 a 5.39 a 5.36 a 4.24 b 4.63 ab 0.15 <0.001 Cysteine 1.49 1.01 0.97 0.94
CO2/d.DM (mL/g) 163.17 b1.57
187.12 Valine 5.02 6.31 6.32 6.47 5.85
Tryptophan 1.40 1.12 1.06 1.08 1.71
Non-essential amino acids
Alanine 4.43 9.70 10.23 10.45 5.73
Glycine 4.37 6.09 6.14 6.14 5.73
Proline 5.21 6.21 6.29 6.33 4.75
Glutamic acid 18.45 11.88 12.07 11.79 11.95
Serine 5.08 5.17 4.92 5.01 4.77
Aspartic acid 11.73 9.08 8.90 8.75 10.48

3. Gas Production and Composition

The production of total gas, CH4, and CO2 per digestible DM (d.DM) (mL/g) in the 60% KG + 40% SBM diet was significantly higher than that in the 100% KG diet (p < 0.01). Substituting 25% of SBM in the diets with A.d and B.p did not affect gas production/d.DM (mL/g), but gas production was significantly lower when SBM was replaced with G.b and B.m (p = 0.03, Table 5). Moreover, the inclusion of G.b and B.m significantly reduced the production of CH4/d.DM (mL/g) (p < 0.05) by 18.4% and 16.3%, respectively, when compared with 60% KG + 40% SBM diet. The same effect was shown with regards to CO2/d.DM. In contrast, adding A.d and B.p did not show any differences in the amounts of CH4 and CO2 produced when compared with the 60% KG + 40% SBM diet. The ratio of CH4/CO2 (mL/mL) in the produced gas when G.b was used as a supplement was significantly lower (p = 0.004) than that in the 60% KG + 40% SBM diet (Table 5).
Table 5. Effect of substituting soybean with insects on gas production and composition from 24-h in vitro incubation (n = 12).
Parameter

1 VFA: Volatile fatty acids. 2 A/P: Acetate/Propionate. SEM: Standard error of the mean. a, b, c Values with different superscripts in the same row are significant different (p < 0.05).

 

6. Conclusion

The current study revealed that the evaluated insects were rich in fat and protein with almost the same essential amino acid profile as that found in soybean meal. Substitution of 25% of soybean meal with the four tested insects in the ruminant diet did not adversely affect the fermentation profile or nutrient digestibility. Additionally, inclusion of Gryllus bimaculatus and Bombyx mori in the diet demonstrated the potential to reduce CH4 production by up to 18.4% and 16.3%, respectively. Therefore, the investigated insects could be used as a sustainable source to replace 25% of the high-quality expensive protein source soybean meal without any negative effects. Further studies with increasing inclusion levels of these insects are required to investigate their impacts when used to completely replace soybean meal and as promising candidates for more effective mitigation of CH4 production.

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