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Journal of Applied Animal Research

ISSN: 0971-2119 (Print) 0974-1844 (Online) Journal homepage: https://www.tandfonline.com/loi/taar20

Recent advances in role of insects as alternative


protein source in poultry nutrition

Sohail Hassan Khan

To cite this article: Sohail Hassan Khan (2018) Recent advances in role of insects as alternative
protein source in poultry nutrition, Journal of Applied Animal Research, 46:1, 1144-1157, DOI:
10.1080/09712119.2018.1474743

To link to this article: https://doi.org/10.1080/09712119.2018.1474743

© 2018 The Author(s). Published by Informa


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Published online: 14 May 2018.

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JOURNAL OF APPLIED ANIMAL RESEARCH
2018, VOL. 46, NO. 1, 1144–1157
https://doi.org/10.1080/09712119.2018.1474743

Recent advances in role of insects as alternative protein source in poultry nutrition


Sohail Hassan Khan
Poultry Research Institute, Rawalpindi, Pakistan

ABSTRACT ARTICLE HISTORY


Insects are considered as a potential substitute for fishmeal (FM) and soybean meal (SBM) in feeding Received 12 January 2018
mixtures for poultry diets. The intent of this paper is to appraise the current work relating to the use of Accepted 30 April 2018
insects as alternative protein in poultry feeding and the potential of large production of insects for the
KEYWORDS
poultry feed industry. Certainly insects have a mammoth prospective as a protein source and other Insects; chemical
active substances (i.e. polyunsaturated fatty acids, antimicrobial peptides) for poultry. On the basis of composition; digestibility;
numerous studies, insects meal belonging to the orders Diptera (black soldier fly, housefly), Coleoptera performance; poultry
(mealworms), Megadrilacea (earthworm), Lepidoptera (silkworm and cirina forda) and Orthoptera
(grasshoppers, locust and crickets), may be fruitfully used as feed ingredient in poultry diets.
Information regarding their nutritional composition and biological evaluation was collected and
compared it to SBM and FM.

1. Introduction
of pesticides, loss of biodiversity and a huge CO2 footprint
The consumption of insects (also called entomophagy) is tra- (van Huis 2015). Likewise, in recent years, the increasing price
ditionally practised by more than two billion people worldwide, of soybean has become a critical aspect for the economic sus-
around 524 insect species are estimated to be consumed in tainability of the poultry meat industry, particularly in some
Africa, 349 in Asia, 679 in the America, 152 in Australia and developing countries (Gale and Arnade 2015). The FM is
only 41 in Europe (Jongema 2015). Mexico has the highest based on fish cultivated in aquaculture or marine fish species.
number of insect species that are documented as edible, fol- Due to problems with over-fishing and environmental pollution,
lowed by Thailand, Congo, India, Australia, China and Zambia marine fish can be regarded as a limited resource. This is
(Ramos-Elorduy et al. 2012; Jongema 2015). Insects constitute reflected by a drastic increase of the market price for FM
about three-fourths of the total organisms present on earth during the last ten years, which has given rise to the demand
(Pedigo 2002). According to Rumpold and Oliver (2013), the for a new and more sustainable protein source (Veldkamp
insects could be divided into orders such as Diptera (black and Bosch 2015). Alternative protein sources of comparable
soldier fly, housefly), Coleoptera (mealworms), Megadrilacea value are therefore urgently needed in order to make poultry
(earthworm), Lepidoptera (silkworm and cirina forda) and production a sustainable production form in the future. More-
Orthoptera (grasshoppers, locust and crickets). Out of the over, the International Feed Industry Federation (IFIF 2016) pre-
more than 2000 eaten species explained in scientific literature, dicts that livestock production will have doubled by 2050.
beetles are 31%; caterpillars of butterflies and moths are 18%; Therefore, to meet the future requirements for protein new
bees, wasps and ants are 14% and locusts, grasshoppers and protein sources may be explored.
crickets are 13% (van Huis et al. 2013). Generally, insects are sat- Insects are suggested as an alternative protein source in
isfactory sources of nutrients (proteins, fat, energy, vitamins and poultry feed, due to similar fat (30–40% dry matter; DM) and
minerals). In this regard, literature showed that intake of 100 g protein content (40–60% DM) to that of SBM or FM (Makkar
of caterpillars’ fulfils about 76% of the requisite quantity of pro- et al. 2014). A shift from conventional protein sources such as
teins on daily basis and accomplishes about 100% daily require- SBM and FM towards insect meals might result in a more effi-
ment of the vitamins in humans (Agbidye et al. 2009). Similarly, cient use of natural resources and lower emissions of green-
the nutritive values of three silkworm pupae are considered at house gases as well as limiting eutrophication of water
par in nutrients of one chicken egg (Mitsuhashi 2010). environments (loss of nutrients) (van Zanten et al. 2014). Due
In poultry nutrition the supply of essential amino acids to the reasons mentioned above, the potential of insect
(EAAs) to grow rapidly in a short period of time is a key protein in poultry diets has attracted much attention. Chickens
factor. For this reason SBM-based diets (as the major protein with access to outdoor areas pick up insects at all life stages and
source of the diet) are supplied together with FM that covers eat them voluntarily, which indicates that they are evolutiona-
any amino acid (AA) deficiency from vegetable proteins rily adapted to insects as a natural part of their diet (Bovera
(Agazzi et al. 2016). The production of soybean is connected et al. 2015a). Therefore, it seems reasonable to consider the
with deforestation, soil erosion, eutrophication, extensive use inclusion of insect proteins as raw material to be used in

CONTACT Sohail Hassan Khan sohailhassan64@gmail.com; sohailhassan@yahoo.com Poultry Research Institute, Murree Road, Shamsabad, Rawalpindi, Pakistan
© 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distri-
bution, and reproduction in any medium, provided the original work is properly cited.
JOURNAL OF APPLIED ANIMAL RESEARCH 1145

commercial feed manufacturing and to develop intensive magnesium (Mg; 0.39% DM), iron (Fe; 0.14% DM), manganese
farming systems for insects. The FAO strongly recommends (Mn; 246 mg/kg DM), zinc (Zn; 108 mg/kg DM) and copper
the use of insects as human food and animal feed as a tool (Cu; 6.0 mg/kg DM). Cullere et al. (2016) reported that the
for poverty alleviation (FAO 2010). most abundant EAAs were valine (val) and leucine (leu),
Another concern in Europe is the lack of protein-rich ingredi- whereas alanine (alan) and glutamic acid (glu) were rich in
ents for animal feeding, especially to organic poultry due to defatted BSF larvae meal. The AAs concentration of defatted
exclusion of synthetic amino acids (AAs) and oil cakes extracted BSF larvae meal differed from the full-fat BSF larvae meal pre-
with solvents (SBM and rapeseed meal (EC, No. 834/2007). sented by De Marco et al. (2015): regarding EAAs, lysine (lys),
Current legislation allows 5.0% non-organic substrates in methionine (meth), arginine (arg) and histidine (hist) contents
organic diets, until 31 December 2017 (EC 834/2007 No. 2092/ were lower in defatted BSF larvae meal compared with those
91; EC 836/2014 No. 834/2007). It is a general concern that a of the above-mentioned study, whereas for isoleucine (isoleu),
100% organic diet is unable to meet the requirements of leu, phenylalanine (phy), threonine (thr) and val the situation
EAAs of poultry, particular sulfur-containing AAs (Sundrum was reversed. The fatty acid (FA) composition of the BSF
and Richter 2005). Furthermore, extensive use of dietary larvae depends on the FA composition of the diet. The lipids
protein, for reaching the required amount of EAAs, is a of larvae fed on cow manure contained 21% of lauric acid,
common practise in organic poultry production (Elwinger 16% of palmitic acid, 32% of oleic acid and 0.2% of omega-3
et al. 2008). FA, while these proportions were respectively 43%, 11%, 12%
Generally available literature confirms the feasibility of total and 3% for larvae fed 50% fish offal and 50% cow manure
or partial replacement of FM with insect meal. In particular, no (Makkar et al. 2014). Total lipid content also increased from
negative effects have been reported on growth of insect meal- 21% to 30% DM. Feeding BSF larvae reared on cow manure
fed chicks, however most of papers have described similar or and 22% of fish offal within 24 h of their pupation was sufficient
even better growth rates in chicks when compared to SBM or for a substantial enrichment in polyunsaturated fatty acid
SBM + FM. In the same way the digestibility of nutrients (PUFA), especially in docosahexaenoic acid and eicosapentae-
seems to be unaffected, or at least improved, by the use of noic acid (St-Hilaire et al. 2007). Recently, Maurer et al. (2016)
insect meal in poultry diet when compared with FM: this is reported that dried full-fat BSF larvae meal contained 41.5%
especially true when insect meal has a comparable AAs CP, 26.5% EE, 4.3% ash, 0.80% Ca, 0.50% P, 0.08% Na and
profile and replaces the whole FM in the diet (Khatun et al. 0.33% chloride while dried partly-defatted BSF larvae meal con-
2003, 2005) determining some economical positive effects sisted 59.0% CP, 11.0% EE, 5.0% ash, 0.98% Ca, 0.63% P, 0.08%
(Okah and Onwujiariri 2012). Na and 0.28% chloride . In this study, the Ca content of the BSF
Until now, the main research efforts in poultry diets have larvae meal was very low (0.80 and 0.98%) compared to 5–8%
focused on the black soldier fly (BSF), housefly (HF), mealworm mentioned by Arango Gutierrez et al. (2004). This might be
(MW), silkworm pupae (SWP), earthworm (EW), grasshopper due to harvest before the pre-pupal stage.
(GH), locust, cricket and cirina forda (westwood). This review
aims to explain the nutritional value and functional properties
2.2. Effect of black soldier fly on poultry performance
of the above mentioned insect species on the performance of
poultry when these insects were used as a feed ingredient. BSF are possibly the most widely studied and the earliest refer-
enced paper for their use as protein source in poultry feed (Hale
1973). They avoid human contact and are not generally con-
2. Black soldier fly larvae (Hermetia illucens)
sidered a pest or pathogen vectoring species. Oluokun (2000)
BSF larvae are naturally found in poultry, pig and cattle manure compared BSF larvae with SBM and FM on broiler production.
but can also be grown on organic wastes such as coffee bean The nutritional profile of maggots is comparable to FM and, in
pulp, vegetables, catsup, carrion, and fish offal. It has been some aspects, better than SBM. The author suggested that
suggested that the larvae contain natural antibiotics (Newton maggot meal could replace FM to upgrade the nutritive value
et al. 2008). The BSF larvae (also called as BSF larvae meal, of SBM in the broiler diets without any adverse effect on the
BSF prepupae meal and BSF maggot meal) are used live, body weight gain (BWG), feed intake (FI) and feed conversion
chopped, or dried and ground forms. ratio (FCR). The feeding of dried BSF larvae as a substitute for
SBM resulted in a similar BWG but a lower FI as compared to
control indicating an improved FCR (Makkar et al. 2014).
2.1. Chemical composition
Recently, Maurer et al. (2016) carried out a feeding trial with
The DM content of fresh larvae is quite high (35–45%), which partly defatted meal of dried BSF larvae in small groups of
makes them easier and less costly to dehydrate than other laying hens. Experimental diets contained 12 and 24% meal
fresh byproducts (Newton et al. 2008). Proximate analysis of replacing 50 or 100% of soybean cake used in the control
BSF larvae contained 41.1–43.6% crude protein (CP), 15.0– diet, respectively. After three weeks (wks) of experiment,
34.8% ether extract (EE), 7.0% crude fibre (CF), 14.6–28.4% ash there were no significant differences between feeding groups
and 5278.49 kcal/kg gross energy (GE) on DM basis (Arango with regard to egg production, FI, egg weight and feed effi-
Gutierrez et al. 2004; St-Hilaire et al. 2007). Arango Gutierrez ciency. There was a tendency (P = 0.06) for lower albumen
et al. (2004) reported that larvae are rich in calcium (Ca; 5–8% weight in the 24% meal group; yolk and shell weights did not
DM) and phosphorus (P; 0.6–1.5% DM), however, other minerals differ. No mortality and no sign of health disorders occurred.
profile is potassium (K; 0.69% DM), sodium (Na; 0.13% DM), The DM of faeces increased with increasing proportions of
1146 S. H. KHAN

meal in the diet, with a significant difference between 24% meal were found the highest in HF pupae as compared to the
and the control groups (P = 0.03). An increase of black faecal lesser MW. With regard to protein quality, maggots are compar-
pads was observed in the 12% and 24% meal groups. Higher able to meat and bone meal as well as FM and are superior to
DM of faeces and a larger proportion of dark, firm faecal pads SBM (NRC 1994; Inaoka et al. 1999). The maggots had great
with 24% gave reason to assume that in this diet the proportion apparent digestibilities for protein (98.50%) and EAAs
of meal was too high. The causes of these differences are not (94.80%) more than the SBM. Ukanwoko and Olalekan (2015)
fully understood. In growing broiler quail, Cullere et al. (2016) assessed the effect of source and the time of harvest on proxi-
tested three diets as control, 10% defatted BSF larvae meal (sub- mate composition of maggot meal. It was noted that maggot
stituted 28.4% soybean oil and 16.1% SBM) and 15% defatted meal with raw egg attractant had the highest CP (45.84%)
BSF larvae meal (substituted 100% soybean oil and 24.8% and EE (19.30%) as compared to maggot meal without fly
SBM). It was observed that quails showed the same BWG, FI, attractant (39.58 and 19.12%, respectively). Maggot meal with
FCR and mortality rate in all dietary groups. Apparent digestibil- chopped mango attractant had the highest ash content
ity of nutrients (DM, OM, CP, EE and starch) was overall compar- (7.13%). Maggot meal with raw egg attractant had the
able among the three groups except EE, whose digestibility was highest CF (6.14%). The highest value of CP was observed
the highest (P < .001) in control (92.9%) and 15% BSF meal after 48 h of harvest (58.06%). The highest EE and CF were
(89.6%) groups. Feed choice trial showed that broiler quails observed at 120 h of harvest (24.60 and 7.60%, respectively).
did not express a preference toward control or 15% BSF meal
diets and breast meat weight and yield did not differ among
3.2. Effect on digestibility
all groups.
It may be concluded that maggot meal could replace FM or Apparent fecal digestibility of dried HF meal was evaluated in
SBM in the broiler and laying hen diets without any adverse broiler chickens in two studies. Hwangbo et al. (2009) fed 4-
effect on performance. wk-old broilers a diet with 30% dried HF larvae meal or SBM
for 7 d and Pretorius (2011) fed 3-wk-old broilers a corn meal-
based diet containing 50% dried HF larvae meal or dried HF
3. Housefly (Musca domestica)
pupae meal. The results showed that the value of apparent
Common HF larvae can grow on poultry, pig and cattle manure; fecal digestibility of CP for HF larvae in first study was higher
they have yet been reared on municipal organic waste. Maggots (98.5%) than the second study (69%). The latter study also
are HF larvae that are prepared to make maggot meal. They showed that CP fecal digestibility was greater for HF pupae
have a rapid reproductive rate, high feeding value and easy than for the larvae. Digestibility of most AAs was in both
to process and stored for sustainable use. Maggots are available studies around 90% or greater. Surprisingly, Pretorius (2011)
throughout the year (Moreki et al. 2012). reported considerably greater apparent fecal digestibility
values for individual AAs than for CP. There is a need for evalu-
ation of nutrient digestibility of (processed) insects as feed
3.1. Chemical composition
ingredients, which is a prerequisite for formulating insect-con-
The HF maggots are rich in CP (63.99%) and EE (24.31%) as taining feeds. Bosch et al. (2014) reported in vitro digestibilities
reported by Hwangbo et al. (2009). The CP and EE contents of organic matter and nitrogen in HF fly pupae were found as
are changed with the drying method and age of the 83.2 and 84.3%, respectively. Pieterse and Pretorius (2013) eval-
maggots; CP contents decreased and EE content increased uated the dried larvae and pupae meal using chemical- and
with age (Aniebo and Owen 2010). Pretorius (2011) found broiler-based biological assays. Proximate analysis showed as
that HF larvae meal (on DM basis) contained 60.38% CP, CP (60.38 and 76.23%, with total tract digestibility (TTD) of
14.08% EE, 10.68% ash and GE value of 4800.80 kcal/kg and 69% and 79%, respectively), EE (14.08 and 14.39%, with TTDs
the HF pupae contained 76.23% CP, 14.39% EE, 7.73% ash of 94% and 98%, respectively), CF (8.59% and 15.71%, with
and GE value of 4877.23 kcal/kg. He noted that the HF larvae TTDs of 62% and 58%, respectively), GE value (4800.80 kcal/kg
and pupae meal had an apparent metabolizable energy (AME) and 4877.23 kcal/kg, respectively) and apparent ME value
value of 3398.77 kcal/kg and 3618.51 kcal/kg, respectively. The (3398.77 kcal/kg and 3618.51 kcal/kg, respectively). The AAs
maggots showed higher Ca, P and metabolizable energy (ME) analysis revealed a favourable AAs composition with high lys
content (4140 kcal/kg) than SBM (2250 kcal/kg). The essential concentrations but marginally low meth concentrations. The
fatty acid (EFA), linoleic acid, was found at levels of 26.25 and ratios between Arg & lys and isoleu & leu of larvae and pupae
36.27% of the total fats for the HF larvae and pupae meal, meal were found as 0.67 & 0.9 and 10.68 & 0.64, respectively.
respectively (Pretorius 2011). He also reported that the
maggots contained higher percentage of palmitoleic acid,
3.3. Effect of house fly on poultry performance
oleic acid and linoleic acid as EFAs than the HF pupae. The
maggots had also higher AA content than the SBM and con- There is an extensive literature on the suitability of maggots or
tained a higher percentage of EAAs (29.46%) than non-EAAs pupae of HF to rear broilers chicks (Akpodiete and Inoni 2000;
(28.22%). Specifically, the maggots contained higher quantity Téguia et al. 2002; Awoniyi et al. 2003; Adeniji 2007; Adesina
of the EAAs lys, arg, phy, tryp and val. Maggots have low et al. 2011; Okah and Onwujiariri 2012), layers (Dankwa et al.
levels of meth and cys, it would be necessary to provide meth 2002; Agunbiade et al. 2007) and ducklings (Mensah et al.
alongwith feed that contains maggots (Pretorius 2011). Bosch 2007). In all cases, these studies showed that maggots, either
et al. (2014) reported that phy, lys and Meth contents of CP fresh or dried, could entirely or partially replace conventional
JOURNAL OF APPLIED ANIMAL RESEARCH 1147

protein ingredients such as FM, meat meal or groundnut cake larvae meal in the diets of laying hens. In the study, FM was
without affecting survival, daily FI, BWG, FCR, egg laying and replaced with larvae meal in a cassava based diet in two
other performance factors. Téguia et al. (2002) obtained laying hen hybrids (50 wks in lay).The results showed that FI
better results with maggot meal as compared to conventional and FCR were not affected by the experimental treatments (P
FM (Téguia et al. 2002). However, when various proportions of > .05), but the hen-day production was significantly affected
maggot and FM, or maggot and meat meals were used, the (P < .05) when 3.00% FM and 4.72% larvae meal were fed. This
best growth performance was often observed with variable effect can be due to the complimentary effect when larvae
combinations of maggot meal and conventional meal than and FM are supplemented together which creates a better
that of single protein source. This may be due to the combi- AAs profile supplied to the animal (Agunbiade et al. 2007).
nation of maggot meal with conventional feed might provide Larvae meal supplementation had no significant effect (P
a more balanced diet for the birds. Most trials indicated that > .05) on egg quality traits when compared to the control diet
partial replacement of FM by maggot meal in broiler diets is (Agunbiade et al. 2007). The findings showed that when
possible. The HF maggots and pupae can replace 7% of the larvae meal were supplemented at a level of 7.08% together
FM in broiler chicken feed (Inaoka et al. 1999). Inclusion rates with 1.50% FM and at a level of 9.44% with no FM a significant
greater than 10% in the diet decreased FI and performance, decrease (P < .05) in shell thickness and shell weight were
perhaps due to the darker colour of the meal, which may be observed. These differences are related to the lower Ca
less appealing to chickens (Atteh and Ologbenla 1993; Bamg- content associated with larvae meal supplementation and not
bose 1999). An imbalanced AAs profile may also explain the an inherent negative effect of larvae meal. Larvae meal could
negative effects observed when the inclusion levels are replace 50% of the dietary animal protein supplied by FM
greater than 10% (Makkar et al. 2014); meth supplementation without deleterious effects on egg production and shell
might enhance performance. Hwangbo et al. (2009) sup- strength. In another study, supplementation of maggots (30–
plemented broiler feed with 10–15% HF larvae and found 50 g) also improved (P < .05) clutch size (115 vs 9.5), number
improvement in growing performance and carcass quality. of eggs hatched (9.8 vs 7.1), egg weight (43.5 vs 33.6 g) and
The CP contents remained steady in the breast muscle but lys chick weight (34.2 vs 29.8 g) as compared to only scavenging
and tryp contents increased. This may be due to the best AAs in the village chicken (Dankwa et al. 2002). Based on the
profile, rich CP content (63.99% DM) and high protein digestibil- results of above studies; it seems that maggot meal could be
ity (98.5%) of the larvae. Awoniyi et al. (2003) conducted a per- replacement for FM in broilers and laying hens feeding.
formance trial with 3- to 9-wk-old broiler chickens that were fed
five isonitrogenous and isocaloric diets in which maggot meal
4. Mealworm larvae (Tenebrio molitor)
replaced 0, 25, 50, 75 and 100% of 4% FM in the diet. The
diet with 25% of FM protein replaced with maggot meal was Only a limited number of organic waste sources have been
the most efficient in terms of average weekly BWG and described in literature for rearing of yellow MW. The MW has
protein efficiency ratio. At 9 wk of age, however, live, dressed been grown on dried and cooked waste materials from fruits,
and eviscerated weights as well as relative length, breadth, vegetables, and cereals in various combinations (Ramos-
and weights of the pectoral and gastrocnemius muscles were Elorduy et al. 2002). They are omnivores but are typically fed
not significantly influenced by the diets (Awonyi et al. 2003). on wheat bran or flour supplemented with soybean flour,
Atteh and Ologbenla (1993) found that a 33% replacement of skimmed milk powder or yeast (Makkar et al. 2014).
conventional FM by maggot meal was an ideal for chicks, but
higher proportions of maggots reduced FI and BWG. Pretorius
4.1. Chemical composition
(2011) conducted a performance study with broilers using
seven dietary treatments consisting of a commercial diet Scientific literature regarding the nutritive composition of MW
(corn-soybean) and diets supplemented with 10% HF larvae larvae shows variation depending on diet, climate conditions
meal, 10% FM, 25% HF larvae meal, 25% FM, 50% HF larvae and phase of development. The minimum and maximum
meal and 50% FM. No significant differences in performance values of CP, EE, ash, CF and energy in MW larvae were reported
results were observed between a 10% HF larvae meal and a as 45–60% (Józefiak and Engberg 2015), 25–43% (van Broekho-
10% FM supplementation. Broilers fed the 10% larvae meal or ven et al. 2015; Józefiak and Engberg 2015), 3.0–4.5% (Ramos-
10% FM diets had significantly greater breast muscle portions Elorduy et al. 2002; Józefiak and Engberg 2015), 5.0–8.8%
relative to carcass weight than the chicks that received the com- (Ramos-Elorduy et al. 2002; Józefiak and Engberg 2015) and
mercial diet. The 25% HF larvae meal supplementation signifi- 244–781 cal/kg DM, respectively (Finke 2002; De Marco et al.
cantly improved broiler BW, FI and cumulative FI when 2015). The total CP content of MW adult, exuvium and excreta
compared with the 25% FM supplementation diet in the were reported as 63.34, 32.87, and 18.51%, respectively (Ravza-
growth phases. Okah and Onwujiariri (2012) also reported naadii et al. 2012). Same researchers reported that total EE
that the chickens fed the control diet gained lower BW than content was 7.59, 3.59 and 1.3% for MW adult, exuvium and
those fed the 20 and 30% of maggot meal in replacement excreta, respectively. Recently, Bovera et al. (2015b) compared
of FM. the chemical composition and AAs profile of MW larvae with
There is little published literature on the use of HF larvae SBM and reported that CP, EE and acid detergent fibre (ADF)
meal in the diets of laying hens and the only published litera- contents were higher in MW larvae (51.93, 21.57 and 7.20%,
ture of interest was the work done by Agunbiade et al. (2007), respectively) than SBM (44.51, 1.84 and 4.79%, respectively).
who investigated the effect when FM was replaced with The two protein sources had a different composition in EAAs,
1148 S. H. KHAN

and this was particularly manifest for meth + cys (the SBM was better (P < .05) as compared to control group (2.01). No sig-
showed contents 3.27 times higher than MW) but also for nificant difference was seen in the FI of different groups. The
isoleu (+1.75), arg (+1.70) and lys (+1.68). Moreover, thr dressing percentage was higher (P < .05) at 0.3% MW sup-
(+1.26), leu (+1.25), hist (+1.19) and val (+1.10) were higher in plemented group (66.10) as compared to control (63.28). It
SBM, whereas the tryp content was higher in MW larvae than was observed that organolyptic properties evaluation i.e.
in SBM. They concluded that only meth and lys content of taste, tenderness, juiciness, flavour and colour were not influ-
both protein sources were not adequate for broilers and a enced by the addition of MW in the diet of broilers. Antibody
diet supplement was necessary. All the other AAs had a suffi- titer against Newcastle disease virus for all experimental
cient concentration to satisfy broiler needs for growth also in groups showed non-significant result. This indicated that MW
MW larvae. Recently, Hussain et al. (2017) recorded a consider- supplementation had no adverse effects on heamagglutination
able amount of CP (45.83%) and EE (34.20%) and almost all antibody titer. Gross return and net profit was higher (P < .05)
EAAs especially meth (1.34%) and lys (4.51%) in MW. for 0.3% MW group (0.41US$) followed by 0.1% MW (0.40US
Ravzanaadii et al. (2012) reported that MW larvae are too low $), 0.2% MW (0.36US$) groups and lowest return (0.34 US$)
in Ca (434.59 mg/kg) and rich in K (9479.73 mg/kg) and P was control group.
(7060.70 mg/kg). The Ca content and the Ca:P ratio are not ade- Ramos-Elorduy et al. (2002) reduced the level of inclusion of
quate for poultry production (particularly for hens), but such SBM (55%CP) to 31, 26 and 20% of the diet and replaced it by 0,
problems can be solved by feeding MW with a Ca fortified 5, and 10% of dried yellow MW, respectively. Sorghum (9% CP)
diet for 1 or 2 d (Makkar et al. 2014). The micro-minerals represented 61–64% of the diet (by weight) and did not differ
profile was found as Zn (104.28 mg/kg), Fe (66.87 mg/kg) and among the three treatments. Performance results after 15 d
Cu (13.27 mg/kg). Remarkable composition of the long chain showed no significant differences among treatments. Fresh
of FAs in larvae meal were detected with the highest com- MW larvae contained 40% DM and 1.0–4.5% total ash (Józefiak
ponent oleic acid alongwith linoleic acid and palmitic acid as et al. 2016). The above stated results are main causes for limiting
values 43.17, 30.23, 16.72%, respectively (Ravzanaadii et al. their supplement (up to 10% of DM of total diet) in the broiler
2012). Finke (2015) reported that MW contained considerable diets.
quantities of most of the B vitamins (B2: 8.7; B3: 46.5; B5: 15.6; Ramos-Elorduy et al. (2002) reported that MW may be added
B6: 6.90; folic acid: 1.55 & biotin: 0.43 mg/kg) and choline in SBM based diets without any negative effects on BWG, FI and
(1410 mg/kg), although lower levels of both vitamins B1 FCR. Likewise, Schiavone et al. (2014) noticed better BWG at
(1.1 mg/kg) and B12 (0.0013 mg/kg) were found in MW. maximum level of 25% MW. Bovera et al. (2015a) replaced com-
pletely SBM with MW larvae in broiler’s diet. The use of MW as
the main protein source in the broiler diet had no significant
4.2. Effect on digestibility
effect on most growth performance, carcass traits and chemical
Bosch et al. (2014) reported that in vitro organic matter and & physical properties of meat. However, the FCR in the entire
nitrogen digestibilities of yellow MW were found as 91.5 and experimental period (30–62 d) was improved (P < .05) in the
91.3%, respectively. De Marco et al. (2015) compared two MW group compared with the SBM group. The full digestive
insect larval meals (MW and BSF) regarding the apparent digest- system in broilers fed SBM had a lower (P < .05) absolute and
ibility coefficients of the total tract (CTTAD) of nutrients and the relative weight than that of broilers fed MW larvae. Similarly,
AME and AMEn and amino acid apparent ileal digestibility coef- the weight and the percentage of the spleen in the SBM
ficients (AIDC) for broilers. There was non-significant difference group were lower (P < .05) than those in the MW larvae
between two insect meals for the CTTAD of the all nutrients group. The length of the entire intestine in the group fed
except EE value in MW showed more digestible (0.99) than larvae meal was greater (P < .05) than the other group and
that of BSF meal (0.88). Similarly, no statistical difference was the same happened when intestinal length was expressed as
noted between two insect meals for AME and AMEn (AME = percentage of broiler BW (P < .05). Among the different intesti-
4026.94 and 4151.14 kcal/kg DM for MW and BSF, respectively; nal tracts, the ileum and ceca of broilers fed larvae meal had a
AMEn = 3826.31 and 3964.84 kcal/kg DM for MW and BSF, greater (P < .05) length than that of broilers fed SBM. In another
respectively). The average AIDC of the AAs was found higher study, Bovera et al. (2015b) reported that MW larvae did not
in MW (0.86) as compared to BSF (0.68). Above study provided affect FI and BGR of broilers from 30–62 d of age when com-
updated information and never before evaluated nutritional pared to an isoproteic and isoenergetic SBM diet. However,
values of MW and BSF meal, which could be two potential the FCR was more favourable in the MW larvae group (3.62)
future ingredients for use in the formulation of broiler diets. than SBM group (4.13) from 46 d of age and in the entire
The acquired knowledge of AME and AMEn will be useful for period of the trial and the European efficiency factor was also
nutritionists and feed companies to obtain better formulate higher in broilers fed on the larvae diet (156.2) than SBM diet
novel poultry feeds. (132.6). The protein efficiency ratio was higher in the SBM
(1.92) than in the insect meal group (1.37). The albumin/globu-
lin ratio was decreased when broilers fed on insect meal diet.
4.3. Effect of mealworm on poultry performance
Such low albumin/globulin ratios indicated better disease
Hussain et al. (2017) reported that BWG was improved with resistance and immune response of birds, probably due to
increasing level of MW (1322.0, 1346.3 and 1423.3 g for 0.1, the prebiotic effects of chitin (a polysaccharide constituting
0.2 and 0.3% MW, respectively). Mean FCR for supplemented insects and crustaceans exoskeleton). The increase of aspartate
groups (1.88, 1.84 & 1.75 for 0.1, 0.2 and 0.3% MW, respectively) aminotransferase in broilers of the insect meal group falls in the
JOURNAL OF APPLIED ANIMAL RESEARCH 1149

normal range for broilers and is not accompanied by an et al. (2015) found chemical composition of fresh EW and
increase in gamma glutamyl transferase, lactic dehydrogenase dried EWM contained CP (6.89 & 41.42%, respectively), CF
or lactic dehydrogenase, thus suggesting no alteration occurred (0.55 & 1.77%, respectively), EE (2.25 & 9.20%, respectively),
in liver and muscle cells. ash (1.32 & 9.20%, respectively), NFE (4.14 & 25%, respectively)
The results showed that MW larvae can be a suitable alterna- and ME (10.64 MJ/kg for EWM). The contents of lys and meth in
tive protein source for broilers and also when used as principal fresh EW was 0.51% and 0.14% (DM basis), respectively, that was
protein contributor to the diet. 7.40% and 2.10% per protein unit. The lys and meth contents in
EWM were 3.33% and 0.96% (DM), respectively, that is 8.03%
and 2.32% per protein unit. Bahadori et al. (2015) observed
5. Earthworm
CP (65.68%), EE (7.02%) and ME (3258 kcal/kg) in EWM. The
The EW belongs to the phylum Annelida (ringworm). They are Ca and P contents were 0.45 and 1.22%. The lys and meth con-
generally classified into three ecological categories regarding tents in EWM were 4.44% and 1.2%, respectively. In another
their feeding strategy: endogeic (soil feeders), anecic (burrowers) study, EWM (DM basis) contained 52% CP, 7.8% CF, 18% EE
and epigeic (litter feeders). Species from the first two categories and 12.65% ash (Mohanta et al. 2016).
feed on a blend of organic matter and soil while epigeic EW feed
exclusively on organic matter (Dominguez et al. 2010). 5.2. Effect of earthworm on poultry performance
The EW are a natural feed source for poultry kept under free-
5.1. Chemical composition range systems and, live or dried, are highly palatable to poultry
Babiker (2012) recorded rich source of ash contents in EW (Tiroesele and Moreki 2012). Loh et al. (2009) replaced partially
(43.50%), whereas CP, CF, EE, NFE and ME were found as SBM and FM with EWM in broiler diets (0, 5, 10, 15 and 20%).
38.87, 1.15, 3.71, 9.81% and 7.99 MJ/kg, respectively on DM The BWG and FCR of the 10% (2089 g and 1.99, respectively)
basis. Mineral profile was noted as Ca (0.93%), P (0.50%), K and 15% (2087 g and 1.94, respectively) EWM groups were
(0.58%), Mg (0.36%), Cu (109.86 mg/kg), Fe (5.69 mg/kg), Mn better (P < 0.05) than that of the control group (1928 g and
(268.73 mg/kg) and Zn (151.17 mg/kg). The EW had the con- 2.08) but no effect on FI. The digestibility of CP for EWM was
siderable amount of lys contents (2.56%). Sogbesan and 63%. In Japanese quail diets, Prayogi (2011), who replaced FM
Ugwumba (2008) reported that the proximate and mineral com- with EWM as 0, 5, 10 and 15%. Feed consumption was reduced
position (on DM basis) of EW contained 63.0% CP, 5.9% EE, 1.9% (P < .05) in birds fed EWM diets (9.53, 9.83 and 9.14 g/d for 5,
CF, 8.9% ash, 11.8% NFE, 0.43% Na, 0.53% Ca, 0.62% K, 0.94% P 10 and 15% EWM) than that of birds fed control diet (11.53 g/
and 3525.36 kcal/kg ME. In addition, the same authors found d). However, the BWG of the birds fed 10% EWM (3.67 g) was
that the EAAs composition (g/16 gN) for the EW they analyzed better (P < .05) than those of the birds fed 5% (3.59 g/d) and
as arg (2.83%), hist (1.47%), isoleu (2.04%), leu (4.11%), lys 15% (3.0 g/d) EWM diets. Son and Jo (2013) reported that
(6.35%), meth (5.30%), phy (6.26%), thr (4.43%) and val (4.43%). adding 0.4% EWM to the broiler diets improved the FI and BW
Istiqomah et al. (2009) reported that proximate analysis of and also increased the digestibility of the nutrients. Bahadori
earthworm meal on DM basis (EWM; Powdering method of et al. (2015) evaluated the effect of five dietary treatments on
EW was done by using 3% formic acid addition) was found as broiler performance such as control, diet containing 1% vermihu-
63.06% CP, 18.5% EE, 0.19% CF, 12.41% NFE and 5.81% ash. mus without EWM, diet containing 1% EWM and 1% vermihu-
They also compared the EAAs profile of EW and EWM. The mus, diet containing 2% EWM and 1% vermihumus and diet
results showed that EAAs of EW was dominated by hist containing 3% EWM and 1% vermihumus. The results showed
(0.63% of DM basis), whereas the EWM was dominated by that FI and FCR decreased (P < .05) in whole period with increas-
isoleu (1.98% of DM basis). The non-EAAs of EW and EWM ing the amount of EWM. The effect of experimental treatments
were dominated by glu acid (1.52% and 3.60% of DM basis, was not significant on BWG and some carcass component.
respectively). The value of EAA index obtained from EWM was Overall, the results showed that 2% and 3% of EWM along with
higher (58.67%) than those from EW (21.23%). So, EWM had 1% vermihumus improved the FCR of broiler chickens.
higher AA balance than EW. Reinecke et al. (1991) evaluated
protein quality of three species of EW (Eisenia fetida, Eudrilus
6. Grasshoppers
eugeniae and Perionyx excavatus) and CP contents on DM
basis were found 66.13, 58.38 and 61.63%, respectively com- The GH can be harvested from their habitats such croplands,
pared to FM (61%). This finding shows that the protein grasslands, wetlands and paddocks (Khusro et al. 2012). Har-
content of EW differs among species and also probably due vesting GH from these habitats could reduce the use of hazar-
to stage of growth. Furthermore, Paoletti et al. (2003) found dous chemical to control pest. Thus these harmful insects
that EW contained large amounts of CP (64.5–72.9%), TFAs may be utilized in a useful way as economic and self-sustaining
(6.6–10.5 mg/g), Ca (1020–7070 mg/kg) and Fe (1050– protein supplement in poultry diet especially in the developing
2990 mg/kg) alongwith notable amounts of other important countries.
elements. Tiroesele and Moreki (2012) reported that proximate
analysis of EW on DM basis was recorded as CP (63%), CF (1.9%),
6.1. Chemical composition
EE (5.9%), ash (8.9%), NFE (11.8%) and ME (3525.36 kcal/kg).
They also observed major mineral profile (mg/kg) as Ca The nutrient composition of grasshopper meal (GHM) was
(5300), P (9400), Na (4300) and K (6200). Recently, Ljiljana assessed by many scientists (Ojewola et al. 2003; Ojewola and
1150 S. H. KHAN

Udom 2005; Adeyemo et al. 2008; Alegbeleye et al. 2012). Data It is also important to know whether GH can compete with
from these and other studies, summarized in Heuzé and Tran the other conventional protein sources like FM, SBM etc.
(2013), were highly variable. The CP content was varying from Above description indicated that Acridids have been identified
29 to 77.1% due to various species, developmental stages and as one potential feed component for poultry feed since they
different processing methods. Ojewola and Udom (2005) have higher CP content than other protein sources such as
reported that GH had 28.13% CP, 2.38% CF, 9.97% ash, 4.18% SBM (48%) and FM (50–55%). Hasanuzzaman et al. (2010) and
EE and 1618 kcal/g GE on DM basis. Also, Ojewola et al. (2005) Adeniyi et al. (2011) reported EE content of fish and meat
found that CP (35.67%), CF (1.06%), EE (15.86%), ash (6.02%) varied from 4 to 9% which is also similar to that of GH
and GE (1917 kcal/kg) on DM basis. On the other hand, (Ganguly et al. 2013). According to Koumi et al. (2011), the
Hassan et al. (2009) reported that CP, CF, EE, ash and NFE con- carbohydrate content of fish and SBM could be around 23
tents of GH were noted as 53.58%, 9.21%, 26.52%, 4.31% and and 27%, respectively, which are very close to the value of
6.40%, respectively on DM basis. Furthermore, Melo et al. the carbohydrate content of almost 30% noted in the GH
(2011) found that GH contained 71.5% CP, 5.75% EE, 2.50% (Ganguly et al. 2013). Among vitamins, this insect has a
ash, 3.89% CF and 16.36% NFE on a DM basis. Sun et al. higher proportion of thiamin (vitamin B1) than wheat germ,
(2012) reported that the fresh GH biomass contained between peas, bread, beans, rice, soybean, milk and egg; whereas for
29 and 35% DM, which contained 62–67% of CP, 1.29– riboflavin (vitamin B2) it is richer than cheese, bread, beef
2.52 mg/kg of vitamin E, 7–9% of CF and 3923–4018 kcal/kg liver, milk, eggs, yogurt, spinach, trout and chicken and niacin
of ME. Wang et al. (2007) reported that the adult GH mainly con- (vitamin B3) is in greater amount than bread, peas, beans,
tained: CP 65.42%; fat 8.3% and chitin 8.73% on DM basis. The corn, wheat, milk, bacon and eggs, and in general is poor in
content of AAs compared well with FM; the meth, cys and lys terms of vitamin C (Ramos-Elorduy and Pino 2001). However,
contents in the GHM were 1.70, 0.69 and 3.79% on DM mineral contents in GH were quite lower as compared with
basis. The coefficient of total tract true AA digestibility of meat, fish, soybean or corn (Adeniyi et al. 2011; Koumi et al.
meth, cys and lys in the GH were 0.97, 0.84 and 0.95 deter- 2011).
mined in cecectomized roosters, respectively. The TMEn of It may be concluded that chemical composition of GH can be
the GHM was 2710. 33 kcal/kg determined in the cececto- comparable with other protein sources used in poultry diets.
mized roosters. The FA analysis showed PUFAs of the GHM
to be present in high quantities and the total content of
6.2. Effect of grasshopper on poultry performance
oleic, linoleic and linolenic acids was 0.8449 of total FAs.
Ghosh et al. (2016) found that all EAAs such as lys (4.29%), Liu and Lian (2003) replaced 20% and 40% FM with GHM in
thr (3.75%), cys (3.5%), isoleu (2.85%), and leu (2.53%) were broiler diets without any effect on BWG and FI. However,
showed in good amount in short-horn GH while arg, tyr, Ojewola et al. (2003) reported depressed BWG and FE except
hist, meth, tryp and val are detected in low amount. Among protein content of carcass when added GHM at the levels of
the estimated AAs, glu acid and glutamine were found in 2.5–7.5% in broiler diets (1–49d). Ojewola et al. (2005)
quite high content (30% of the DM of the insect) followed suggested that 2.5% GHM in the broilers diet was appropriate
by serine (6% of DM). Five FAs such as palmitic acid, stearic and cheaper alternate against imported FM (100% replace-
acid, oleic acid, linoleic acid and linolenic acid were the ment) whilst the generally diet contained somewhat less
major in GH and comprised about 89.6% of TFAs (Ghosh protein (22.2% vs. 22.8%).
et al. 2016). Among these FAs, content of linoleic acid (on When maize-GHM-SBM diets were formulated on an equal
DM basis) was found to be the highest (0.555%) followed by CP and TMEn basis, upto 15.0% GHM could replace control
palmitic acid (0.503%), stearic acid (0.487%), oleic acid diet without any adverse affects on broiler BWG, FI, gain:feed
(0.470%) and linolenic acid (0.294%). Same workers reported ratio from 8 to 20 days post-hatching (Wang et al. 2007). In
that among mineral profile (mg/100 g), Mg content was two studies, Hassan et al. (2009) and Muftau and Olorede
found to be the highest (84.84) followed by Zn (17.34), Fe (2009) evaluated the effect of replacing FM with GHM (0, 50
(16.19) and Cu (4.36). Similarly, among vitamins (mg/100 g), and 100%) on the carcass characteristics and the economics
vitamin-B3 was found to be highest (29.59) followed by of broiler chicken production. The BWG of birds increased sig-
vitamin C (26.73), vitamin B2 (2.55) and vitamin A (0.12). Cur- nificantly as the level of GHM increased. The FI of GHM was sig-
rently, Ssepuuya et al. (2017) observed that GH (Ruspolia Niti- nificantly lower than the control diet. The carcass
dula) contained 36–40% CP, 41–43% EE, 2.5–3.2% measurements showed significant difference (P < .05) in the
carbohydrate, 2.6–3.9% ash, 11.0–14.5% CF and 900– treatment means, with the exception of the breast, pancreas,
2300 μg/100 g total carotenoids on a DM basis. The food proventriculus, heart, spleen, liver, lungs, crop and chest.
habits of GH influence their chemical composition (Finke Whole GHM diet showed the highest return (16.61 US$), fol-
and Oonincx 2014). Insects from the Acrididae, Pyrgomorphi- lowed by 50% GHM diet (12.23 US$) and 100% FM diet (6.69
dae and Romaleidae families are mostly graminivores. On US$). They suggested that GHM can completely replace 100%
the other hand, insects from the Tettigoniidae family feed of FM in broiler’s diet, without affecting their biological per-
on small insects and the sappy part of plants (Capinera formance and economic return. Japanese quails (Cotornix japo-
2008). Studies have indicated that other factors such as sex, nica Japonica) were fed with various diets in which GHM
stage of life and environmental factors (temperature, day gradually replaced FM. For a range of growth parameters, the
length, humidity, light intensity, etc.) can influence the chemi- best results were obtained with the diet in which 50% of FM
cal composition of insects (Finke and Oonincx 2014). was replaced with GHM. Fecundity (i.e. the number of eggs
JOURNAL OF APPLIED ANIMAL RESEARCH 1151

laid per female) was significantly higher compared with the locust meal fail to excel or simulate the super-concentrate
control treatment (Haldar 2012). Sanusi et al. (2013) replaced meal in terms of Ca, P and lys. In this study, the AA profile
FM (by 25, 50, 75 and 100%) with GHM in broiler starter and fin- lacked information on sulphur-containing AAs. Adeyemo et al.
isher diets. The results showed that at the starter phase, daily FI (2008) reported that proximate analysis (DM basis) of desert
(57.42–60.30 g), daily BWG (17.9–20.2 g) and FCR (2.9–3.4) locust meal was found as 52.3% CP, 12%EE, 19%CF and 10%
among diets were statistically similar. Similarly, the correspond- ash. Variation in results of different studies could be attributed
ing values of daily FI (135.5–146.1 g), daily BWG (34.5–45.8 g) to differences in locust species, stage of their development and
and FCR (3.2–4.5) at finisher phase were also statistically the season of the year during which the samples were collected.
similar among the diets. The results suggested that GHM can
completely replace FM in broiler diets without adverse effect
on the performance characteristics. 7.2. Effect of locust on poultry performance
In two studies, Sun et al. (2012, 2013) assessed the impact of Limited number of studies was conducted on poultry perform-
a diet containing GH on the characteristics of lipid oxidation of ance. In the earlier study (Fronda 1935), replacement of FM with
carcass meat, physicochemical and sensory characteristics in a locust meal in broilers diets was not improved the performance
free-range, grassland-based broiler production system. A total except better palatability. However, the current studies showed
of 80 (28d-old) male broilers were introduced into a rangeland partial substitution of FM with locust meal is usually suitable.
where there was a dense population of GH (PB). Control birds Adeyemo et al. (2008) replaced 50% FM with desert locust
(CB) were reared under intensive conditions and given a meal (i.e. 1.7% in the diet) in broilers starter diets and found
maize-soybean diet. The results showed that the activities of better BWG (2097.43 g), FI (4658.28 g) and FCR (2.22) as com-
glutathione peroxidase (GSH-Px) and superoxide dismutase pared to higher levels of locust meals (3.4% and 6.8%) and
(SOD) in the muscle of chicken breasts or legs from PB broilers control diets. Gibreil and Idris (1997) used locust sprayed with
were higher (GSH-Px: 0.123 & 0.102 U/g; SOD: 70.13 & 65.24 U/g insecticides and non-sprayed in broiler diets and replaced
for breast and legs, respectively) than those from the CB (GSH- equivalent amount of protein provided by 5% super-concen-
Px: 0.095 & 0.083 U/g; SOD: 58.53 & 50.96 U/g for breast and trate of control diet. Three experimental diets were fed to
legs, respectively), but no significant differences were found groups of commercial broiler chicks from 0 to 2 or 7 wks of
for the activities of catalase between the PB broilers and the age. The results indicated that locust meal sprayed with insecti-
controls. Furthermore, treatment PB produced birds with signifi- cide tended to depress FI (2.9 kg/bird) as compared to non-
cantly lower live BW, breast, wing, thigh and drum weights, and sprayed locust meal (3.04 kg/bird) and control (3.35 kg/bird)
higher dressing percentage and breast percentage of carcass, groups. Moreover, live BW and FCR were depressed by both
compared with CB. Treatment PB produced breast meat with types of locust meals than control group. Locust meal was
significantly higher redness values, shear force and protein deficient in lys and therefore cannot be used as sole protein
content, and lower pH values, cooking loss, moisture and fat supplement in sorghum based broiler diet and it can be used
content compared with CB. Sensory panel results for breast as a base for production of commercial protein supplements.
and thigh meats showed no treatment effect on colour and jui-
ciness, but significantly higher scores for chewiness, flavour,
aroma and overall appreciation, and lower scores for tenderness 8. Crickets (Gryllus testaceus walker)
from treatment PB compared with CB. They concluded that
meat in free-range broilers feeding on GH has more antioxida- Common names are crickets, cricket meal, house cricket, field
tive potential and longer storage life and rearing chickens on cricket or Mormon cricket and it inhabits paddy fields and
rangeland may provide an alternative way to produce poultry fallow lands. It can survive and grow well on a variety of
meat which is considered superior by modern consumers. organic materials (Makkar et al. 2014) including forage diets,
agricultural (rice bran, cassava tops or leaves) and food industry
(spent grain and residues from mungbean sprout production)
7. Locust (Schistocerca gregaria) by-products and plants considered as weeds are potential
The common names are locust meal, locusts, desert locust, cheap and sustainable feed sources. Crickets are considered
migratory locust, brown locust, red locust. Locusts and other easy to rear at farm (FAO 2013) and that is probably one impor-
Orthoptera used for poultry feeding are fed live (free-range tant reason why there are very large numbers of cricket farmers
chickens) or dried and ground (broilers). Sometimes they are (around 20,000) raise crickets in Thailand (FAO 2013).
boiled before drying (Khusro et al. 2012).
8.1. Chemical composition
7.1. Chemical composition
Crickets were reported to have a high CP level ranging from 55
Gibreil and Idris (1997) reported that locust meal contained to 73% and sufficient EAAs, except for meth and lys, which can
higher CP (89 vs 45%) and ME (2714 vs 2000 kcal/kg) but be supplied directly in the feed (Finke 2002; Barroso et al. 2014).
lower EE (3.9 vs 4.8%), Ca (0.26 vs 10.6%) and P (0.44 vs Wang et al. (2005) reported that the CP and EE of field cricket
3.30%) contents than super-concentrate meal used in broiler (DM basis) was 58.3% and 10.3%, respectively which is compar-
diets. The AA profile of locust meal (%DM) contained arg able with those of conventional protein feed supplements i.e.
(2.76), gly (3.5), hist (0.98), leu (3.39), isoleu (2.21), lys (1.97), SBM (46.8 and 1.84%, respectively), meat meal (48.5 and
phy (1.51), thr (1.81), tyr (3.11) and val (3.26). Data showed 8.47%, respectively) and FM (60.2 and 4.11%, respectively).
1152 S. H. KHAN

The percentage of lys, meth and cys were 4.79, 1.93 and 1.01%, significant increase in growth. In later experiment, Finke et al.
respectively in field cricket while they were 4.51, 1.59 and (1985) fed purified diets to broiler chicks to identify the limiting
0.49%, respectively in FM, indicated that the EAAs of this AAs in Mormon crickets and found that meth and arg were
insect were adequate for poultry (Wang et al. 2005). However, probably colimiting. However, when Mormon crickets were
in studies on the Mormon cricket, CP contents were noted as incorporated into practical diets replacing SBM as the major
58% (DM basis) and AAs analysis indicated that meth, arg and source of protein in an 8-wk feeding trial, the corn-cricket diet
tryp, in that order, were found as limiting amino acids (DeFoliart compared favourably with a corn-SBM diet, with non-significant
et al. 1982). The true amino acid digestibility (TAAD) coefficients differences in chick BWG or feed:gain ratio. In taste tests, no off-
for EAAs of field cricket ranged from 82% for cys to 99% for flavour was detected in the meat of broilers that had been fed
asparagines (Wang et al. 2005). The average of TAAD coeffi- Mormon crickets. In another similar experiments, Nakagaki et al.
cients of field cricket (92.9%) was higher than that of FM (1987) conducted two broiler feeding trials to determine the
(91.3%). The TMEn of the field cricket was found as 2960 kcal/ protein quality of dried house cricket meal. In the first trial, semi-
kg measured in conventional birds (Wang et al. 2005). purified diets were used to identify limiting amino acids. There
Adeyeye and Awokunmi (2010) found CP for males (32.4%) were no significant differences in BWG of chicks fed diets with
and females (25.8%) of field cricket, while carbohydrate was amino acid additions, but feed:gain ratios showed that arg,
48.9 and 54.8% for females and males, respectively. The meth and tryp were limiting. In the second trial, dried house
energy content of cricket meal ranged from 3582.69 kcal cricket meal was included into practical diets replacing SBM
(male) to 3821.53 kcal (female) which compared favourably as the major source of protein. There were no significant differ-
with the cereal value of 3104.99–3821.53 kcal/kg. Also, the Fe ences in BWG between chicks fed corn-soybean meal diet and
content is 31–100 mg/kg. Field cricket is a good source of Na those fed corn-cricket diets. However, feed:gain ratios improved
(1037–2226 mg/kg), K (746–1122 mg/kg), P (10880–10936 mg/ significantly when diets were supplemented with meth and arg.
kg) and Zn (515–1032 mg/kg). Abdul Razak et al. (2012) com- Wang et al. (2005) reported that cricket meal replaced partial
pared the nutritive values of house cricket meal with given protein supplement on an equal of CP percentage and TMEn
values of SBM and FM as reported by Mcdonald et al. (1995). basis, broilers BWG, FI and gain:feed ratio from 8 to 20d post-
The CP content of house cricket meal was 60.4% and this hatching were not significantly affected among diets 5%
value was higher than that of either SBM (44%) or FM (351 g, 586 g & 0.618 g/kg, respectively), 10% (357 g, 575 g &
(59.95%). Total amount of tryp, tyr and val in the house 0.621 g/kg, respectively) and 15% (351 g, 576 g & 0.609 g/kg,
cricket meal were 2.8%, 2.4% and 3.2%, respectively. These respectively) cricket meals. Abdul Razak et al. (2012) evaluated
values were higher than those in SBM (0.6, 1.4 and 2.4%, the protein quality of house cricket meal using protein effi-
respectively) and FM (0.7, 1.8 and 3.0%, respectively). The per- ciency ratio (PER) and net protein ratio (NPR) methods. Treat-
centages of lys, meth and cys in cricket meal were 2.4, 0.5 ment diets consisted of basal diet (N-free), basal + cricket
and 0.8%, respectively. These values were similar to those in meal, basal + SBM and basal + FM. Broiler chicks fed cricket
SBM (2.9, 0.6 and 0.7%) but lower than FM (4.5, 1.7 and 0.8%). meal diet recorded higher (P < .05) BWG (88.5 g) than chicks
Total ME value (kcal/kg) for cricket meal (3114.24) was close fed SBM (81.7 g) but slightly lower than that of FM (92.1 g).
to that of corn (3202.67) but was much higher than that of Similar trend was observed in gain/feed ratio among treat-
SBM (2165.39) and lower than FM (3585.09). Similarly, Bosch ments. The PER values for cricket meal, SBM and FM were
et al. (2014) reported that house crickets contained the most 3.42, 3.11 and 3.71, respectively. NPR values for cricket meal,
CP (70.6%) followed by lesser MW (64.8%) and the roaches SBM and FM were 3.66, 3.29 and 3.96, respectively. The PER
(66.3%) and house crickets were relatively high in Arg (5.7%) and NPR values of house cricket meal were higher (P < .05)
but low in Hist (3.4%). Finke (2015) reported that vitamins E than that of SBM but slightly lower than that of FM. The
and K contents in crickets were 53.7 IU/kg and 78.4 mg/kg, results suggested that the house cricket meal has a consider-
respectively. This insect contained substantial quantities of able amount of protein and energy which could to be included
most of the B-vitamins (B1: 2; B2: 16.6; B3: 29.5; B5: 20.3; B6: in poultry diets.
2.13; folic acid: 1.07; biotin: 0.21 and B12: 0.193 mg/kg) and
choline (1.02 mg/kg). Crickets contained sufficient vitamins B1
9. Silkworm
and B12 to meet the requirements of both rats and poultry.
This insect also contained sufficient quantities of inositol Other common names are silkworm pupae (SWP), silkworm
(345 mg/kg). It revealed that the cricket contained not only meal, spent silkworm pupae, defatted silkworm pupae meal,
high quantity of protein but also considerable amounts of deoiled silkworm pupae meal, non-defatted silkworm pupae
digestible AA, carbohydrate, energy, vitamins and minerals for meal, nondeoiled silkworm pupae meal, Eri silkworm pupae
poultry. meal, Muga silkworm pupae meal. A number of species of silk-
worm are known as Bombyx mori Linnaeus; Antheraea assamen-
sis; Antheraea mylitta; Antheraea paphia; Samia cynthia ricini
8.2. Effect of cricket on poultry performance
(Makkar et al. 2014). The SWP are available after the removal
In feeding trials, corn-and-cricket-based diets showed signifi- of silk cocoons through spinning or reeling as discarded
cantly better growth of broiler chicks than conventional corn- waste in large quantities (Khatun et al. 2005). Similarly, silkworm
soybean-based diet supplemented with meth at 3 wks of age caterpillar is not a worm but the caterpillar of moth butterfly
(DeFoliart et al. 1982). It was observed that supplementing (Bombyx Mori) whose cocoon is used to make silk (Ijaiya and
the corn-cricket diet with additional AAs resulted in non- Eko 2009). The world’s 90% production results from the
JOURNAL OF APPLIED ANIMAL RESEARCH 1153

cocoons of the domesticated mulberry silkmoth Bombyx mori. (95.71–98.25 g), BWG (46.10– 98.51 g), FCR (1.98–2.08) or
Silkworm caterpillar hatches from a tiny black egg laid by the protein efficiency ratio (2.41–2.54) between dietary treatments.
adult moth. It nourishes on mulberry and shear butter leaves Silkworm caterpillar meal proved less expensive (cost/kg of
constantly and grows to full size of 7.5–10 cm within 4–6 wks gain = 0.16 US$) at 100% replacement than conventional FM
((Ijaiya and Eko 2009). (cost/kg of gain = 0.19US $), making it well suited in economic
terms as a substitute. Khatun et al. (2003) formulated broiler’s
diet containing control diet (6% FM + 0 SWP) and three treat-
9.1. Chemical composition
ment diets (4% FM + 2% SWP; 2% FM + 4% SWP and 0% FM +
The SWP is a waste product of silk industry that could be used as 6% SWP). They reported that the BW (1274.24, 1425, 1440.15
a top class unconventional protein and energy source for and 1474.99 g/bird, respectively at 42d of age), FCR (2.25,
poultry diets after proper processing at a reasonable cost. 1.95, 1.93 and 1.88, respectively), dressing percentage (58.75,
Mishra et al. (2003) reported that the proximate compositions 68.15, 69.37 and 73.0, respectively) and profitability (0.15,
for SWP on fresh basis were found in the range of moisture 0.19, 0.21 and 0.22 US$/kg broiler, respectively) increased line-
(65–70%), CP (12–16%), EE (11–20%), carbohydrate (1.2–1.8%), arly on increasing level of SWP. In another study, the BWG of
and ash (0.8–1.4%). The energy contents of the SWP were in Rhode Island Red (RIR) layer chicks was found high (26.7 g/
the range of 706–988 kJ. Zhou and Han (2006) reported that day) when fed diet containing 50% FM + 50% SWP (Dutta
the dried SWP powder contained 71.9% CP, 20.1% EE and et al. 2012). Khatun et al. (2005) fed iso-nitrogenous and iso-
4.0% ash on a DM basis. In another study, the percentages of caloric diets containing control diet (6% protein concentrate
CP and EE contents (DM basis) were 55.6 and 32.2, respectively + 0% SWP) and two treatment diets (0% protein concentrate
(Tomotake et al. 2010). The mineral analysis indicated high K + 6% SWP and 0% protein concentrate + 8% SWP) to RIR layer
content with a low Na/K ratio and low heavy metal content. chicks. They reported that the BW (1406, 1500 and 1450 g/
Longvah et al. (2011) reported that proximate composition of bird, respectively at 45 wks of age), FCR (2.25, 1.95, 1.93 and
Eri silkworm pre pupae and pupae as a good source of CP 1.88, respectively) and feed cost/bird (1.10, 0.87 and 0.87 US$,
(16 g %), EE (8 g %) and minerals on fresh basis. The high CP respectively), egg production (79.25, 81.50 and 79.33%, respect-
content in the defatted Eri silkworm meal (75%) with 44% ively from 28 to 45 wks on hen day basis) and feed efficiency
total EAAs makes it an ideal candidate for preparing protein (2.26, 2.10 and 2.24, respectively). The above results revealed
concentrate isolates with enhanced protein quality that can that growth, egg production and profitability were significantly
be used in poultry diets. Zhou and Han (2006) reported that higher in birds fed 6% SWP diets as compared to birds fed other
the SWP protein contained 18 known AAs, including all of the diets. Recently, Ullah et al. (2017a) evaluated broiler’s diets con-
EAAs and sulphur-containing AAs. Compared with the AA taining control diet (100% SBM + 0 SWP) and four treatment
profile recommended by FAO/WHO, the pupal protein was of diets (75% SBM + 25% SWP; 50% SBM + 50% SWP; 25% SBM +
high quality due to its high content of EAAs. Longvah et al. 75% SWP and 0% SBM + 100% SWP). Live BW and FI were
(2011) reported that the AA scores of Eri pre pupae and higher (P < .05) in birds fed diet containing 25% SBM + 75%
pupae protein were 99 and 100 respectively, with leucine as SWP group (2143.3 g and 4572.4 g, respectively) than other
the limiting AA in both cases. Net protein utilization of pre groups. However, FCR and dressing percentage were similar
pupae and pupae was 41 as compared to 62 in casein. (P > .05) among the all groups. Cost per kg of feed steadily
Protein digestibility corrected AA score was 86. Kotake-Nara declined (P < .05) with increasing dietary level of SWP inclusion
et al. (2002) reported that the total lipid content of the SWP levels (0.41, 0.40, 0.39 and 0.38 US$, respectively), indicating
was 4.8 and 9.0% for the male and female (wet basis), respect- higher economic benefit. However, the gross return per bird
ively. Total α-tocopherol contents as antioxidant in total lipids and profit per kg meat were higher for diet containing 25%
were found as 125.2 and 224.1 µg/g lipid for the male and SBM + 75% SWP group (2.95 and 0.65 US$, respectively). In
female, respectively. The SWP contained carotenoids (lutein another study, same scientists (Ullah et al. 2017b) conducted
and neoxanthin) that may also act as antioxidant in total a feeding trial in laying hens (52 wks old) for 42 days and
lipids. The SWP contained n-3 FAs, especially α-linolenic acid replaced SBM with SWP meal in the same ratio as mentioned
(36.3%), as a major component (Tomotake et al. 2010). Kwon in the above study. The results showed that BW, daily FI, hen
et al. (2012) also reported that FA composition of SWP oil day production, average egg weight and FCR did not differ sig-
revealed a high ratio of EFAs (α-linolenic acid + linoleic acid; nificantly (P > 0.05) among the dietary groups. Apparent total
49.0%) and non-essential FAs (19.9% oleic acid, 2.5% palmitoleic tract digestibility of nutrients was not different in the control
acid, 19.7% palmitic acid, 8.6% stearic acid and 0.3% eicosapen- group compared to treatment groups. Blood profile and egg
taenoic acid). quality parameters also showed no significant (P > .05) differ-
ences among dietary groups. Based on above two studies, it
could be concluded that SWM can be effectively used as an
9.2. Effect of silkworm on poultry performance
alternative protein source to SBM without any adverse effects
Banday et al. (2009) reported that the broilers fed with pro- on broiler as well as layer performance. The literature implied
cessed SWP at both 25 and 50% levels showed an increase (P that improved performance of broilers with the replacement
< .05) in BWG and improved FCR as compared to raw SWP. of FM or SBM with SWP could be related to their higher
Ijaiya and Eko (2009) replaced FM (by 25, 50, 75 and 100%) content of EAAs (particularly tryp), minerals, energy, nutrient
with silkworm caterpillar meal in broiler finisher diet. There digestibility and an increased rate of protein accumulation
were no significant differences in performance in terms of FI (Khatun et al. 2003; Ullah et al. 2017a). Moreover, Fagoonee
1154 S. H. KHAN

(1983) argued that the SWP contained growth prompting westwood larvae meal (WWLM) on laying performance and
factors such as ecdysteroid activity (a hormone involved in egg characteristics of hens and concluded that it can replace
protein synthesis and tissue formation), although this has not up to 75% FM in the diet of laying hens without affecting FI,
been established since. BWG, egg production, feed efficiency and egg quality character-
The results showed that SWP can replace FM or SBM as inex- istics. Hen day production of birds fed 0% WWLM (77.86%), 25%
pensive alternative protein source for broilers diet. WWLM (78.32%), 50% WWLM (77.82%) and 75% WWLM
(77.37%) were similar but higher (P < 0.05) than that of those
fed 100% larvae meal (73.39%). The data showed that at
10. Cirina forda (westwood) 100% replacement, daily egg production, egg weight and effi-
Westwood is an edible insect, which belongs to the class ciency of feed utilization were significantly reduced. Thus the
insecta, order Lepidoptera and family Sarturnidae. larvae powder represents a potential alternative for the highly
nutritious and rather expensive FM.

10.1. Chemical composition


11. Conclusions
Dried larvae of Cirina forda contained 46.5–79.6% CP, 10.89% EE
Due to high nutritional value and ubiquitous presence, insects
and major mineral elements (Meyer-Rochow 1978; Malaisse and
are a potential sustainable feed resource in poultry nutrition.
Parent 1980). Osasona and Olaofe (2010) reported that the
Generally results of studies confirm the feasibility of total or
mean values of CP, EE, ash and carbohydrate (on DM) in
partial replacement of FM with insect meal. In particular, no
larvae of Cirina forda (westwood) were found as 20.0, 12.5, 8.7
negative effects have been reported on growth of insect
and 54.3%, respectively. The mineral composition (mg/100 g
meal-fed poultry, however most of papers have described
DM) showed K (47.6), P (45.9), Na (44.4), Mg (43.8), Zn (24.2),
similar or even better growth rates in chicks when compared
Ca (12.9) and Fe (1.3). However, Badanaro et al. (2014) reported
to SBM or SBM plus FM. In the same way the digestibility of
that the proximate compositions for fresh raw caterpillar of
nutrients seems to be unaffected, or at least improved, by the
Cirina forda were found as CP (51.43%), CF (8.42%) and ash
use of insect meal in poultry diet when compared with FM:
(18.43%). The macro mineral profile (mg/100 g) was 233.09,
this is especially true when insect meal has a comparable AAs
67.38, 35.03, 28.53 and 24.47 for P, K, Na, Ca and Mg, respect-
profile and replaces the whole FM in the diet determining
ively. The micro mineral profile was found as 6.93, 1.75, 1.07
some economical positive effects. The costs of conventional
and 0.45 mg/100 g for Fe, Mn, Zn and Cu, respectively. The
feed materials such as SBM and FM are very high demand
caterpillar of Cirina forda had 554.96, 201.01 and 244.03 mg/
and moreover, future availability may be limited. The inclusion
100 g of phospholipid, cholesterol and triglyceride, respectively
of insect meals in poultry diets may lower the cost of feeds, thus
(Ande 2003). It is also rich in EFAs such as linolenic acid
contributing to the more profitability of smallholder poultry
(33.84%), linoleic acid (7.81%) and oleic acid (12.93%; Ande
production. Further research efforts are necessary to deeply
2003). Currently, Anvo et al. (2016) reported that Cirina butyros-
investigate the impact of different insect meal on intestinal
permi caterpillars (on DM) contained high CP (62.74%) and mod-
morphology. In addition, the effects of insect feed on meat
erated lipid (14.34%) contents. The low percentages of ash and
quality traits and sensory properties should be carefully investi-
chitin (around 5.0%) were observed for this caterpillar. Minerals
gated for both consumers acceptance as well as for marketing
were mainly represented by K (1160 mg/100 g), and Fe
purposes. Further research on long-term feeding effects includ-
(12.97 mg/100 g). About 47.64% of the total AAs in caterpillars
ing laying hens before and during peak of lay and on resulting
were EAAs (lys: 6.13%; meth: 1.58%; val: 5.22%; hist: 2.80%;
egg quality is necessary to approve insects as a practicable
arg: 4.86%; leu: 4.08%; isoleu: 3.11%; phy: 3.45; thr: 2.31%).
source of feed protein.
Most abundant FAs were found as linolenic acid (35.82%) and
stearic acid (35.40%).
Disclosure statement
No potential conflict of interest was reported by the author.
10.2. Effect of Cirina forda on poultry performance
Oyegoke et al. (2006, 2013) conducted two trials for determin-
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