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Use of Tenebrio molitor larvae meal as protein source in broiler diet: Effect on
growth performance, nutrient digestibility, and carcass and meat trait

Article  in  Journal of Animal Science · February 2016

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 Published December 30, 2015

Use of Tenebrio molitor larvae meal as protein source in broiler diet:

Effect on growth performance, nutrient digestibility, and carcass and meat traits
F. Bovera,*1 R. Loponte,* S. Marono,* G. Piccolo,* G. Parisi,† V. Iaconisi,† L. Gasco,‡ and A. Nizza*
*Department of Veterinary Medicine and Animal Science, University of Napoli Federico II, via F. Delpino 1, 80137,
Napoli, Italy; †Department of Agri-Food Production and Environmental Sciences, University of Florence, Florence,
via delle Cascine 5, 50144 Firenze, Italy; and ‡Department of Agricultural, Forest, and Food Sciences, University of
Torino, largo Braccini 2, 10095 Grugliasco, Italy

ABSTRACT: The aim of this research was to study
the effect of insect meal from Tenebrio molitor larvae
(Tenebrio molitor larvae meal [TML]) as complete
replacement of soybean meal (SBM) on growth per-
formance, nutrient digestibility, and carcass and meat
traits of broilers. A total of eighty 30-d-old male Shaver
brown broilers were homogenously divided into 2
groups (each consisting of 8 replicates of 5 birds). Up
to 62 d of age, the groups were fed 2 isoproteic and
isoenergetic diets differing for the ingredient used as
the main protein source: the control group was fed a
corn–SBM–based diet, whereas in the TML group,
the SBM was completely replaced by TML. Broiler
growth performance was measured during the trial. At
62 d of age, 2 broilers per replicate (16 per group) were
slaughtered and apparent ileal digestibility coefficients
and carcass and meat traits were determined. The use
of TML as the main protein source in the broiler diet
had no significant effect on most growth performance
and carcass traits and chemical and physical proper-
ties of meat, the latter being important for marketing
purposes. The feed conversion ratio in the entire exper-
imental period (from 30 to 62 d) was improved in
the TML group compared with the SBM group (P <
Key words: apparent ileal digestibility coefficients, broiler,
carcass and meat traits, chitin, growth performance, Tenebrio molitor larvae meal
0.05). The apparent ileal digestibility coefficients of
DM, OM, and CP in broilers fed the SBM diet were
greater (P < 0.01) than the other group. The full diges-
tive system in broilers fed SBM had a lower (P <
0.05) absolute and relative weight than that of broilers
fed TML. Also, the weight and the percentage of the
spleen in the SBM group were lower (P < 0.05) than
those in the TML group. The length of the entire intes-
tine in the group fed TML was greater (P < 0.05) than
the other group and the same happened when intestinal
length was expressed as percentage of broiler BW (P <
0.05). Among the different intestinal tracts, the ileum
and ceca of broilers fed TML had a greater (P < 0.05)
length than that of broilers fed SBM. Also, ceca weight
(as an absolute value or percentage on live weight) in
broilers fed TML was greater (P < 0.05) than that of
broilers fed SBM. Breast pH and cooking losses in
broilers fed TML were greater (P < 0.05) than those
of broilers fed SBM. Chemical characteristic of meat
obtained from right breast of slaughtered broilers were
unaffected by dietary treatments. Tenebrio molitor lar-
vae meal can be a suitable alternative protein source
for growing broilers and also when used as principal
protein contributor to the diet.

© 2016 American Society of Animal Science. All rights reserved. J. Anim. Sci. 2016.94
doi:10.2527/jas2015-9201

INTRODUCTION change, energy use, and water dependence (Makkar

et al., 2014) and the productions of fishmeal and soy-
Feed and food production are the major contribu- bean meal (SBM) are mainly linked to these impacts
tors to land occupation, soil acidification, climate (Sánchez-Muros et al., 2014). The Food and Agriculture
Organization of the United Nations estimates that in
1Corresponding
2050, the world population will exceed 9 billion and
author: bovera@unina.it
underlines the importance of alternatives to conven-
Received April 14, 2015.
tional animal feeds (FAO, 2011). Insects could be a
Accepted November 28, 2015.
◊
◊ Bovera et al.

part of the solution (Makkar et al., 2014): among them, Table 1. Ingredients and chemical–nutritional charac-
mealworms (Tenebrio molitor L.) are an interesting pro- teristics of the diets used in the trial
tein source in feeding fish, poultry, and pig (Veldkamp et Soybean meal Tenebrio molitor
al., 2012). Tenebrio molitor is a pest of flour, grain, and Item diet larvae meal diet
food stored (Ramos-Elorduy et al., 2002) and its larval Ingredient, %
Corn grain 47.20 61.29
and pupal stages are rich in protein (46 to 60%) and easy
Soybean meal with hulls 44.75 –
to breed (Ghaly and Alkoaik, 2009). The protein quality
Insect meal – 29.65
is similar to SBM, but the methionine content is limiting
Vegetable oil 2.20 1.80
if used in poultry feeds (Ramos-Elorduy et al., 2002). Monocalcim phosphate 1.43 2.54
Tenebrio molitor also contains chitin, a polysaccharide Celite 2.00 2.00
of the arthropod’s exoskeleton (Henry et al., 2015) indi- Calcium carbonate 0.74 0.94
gestible by monogastric animals (Sánchez-Muros et al., MinVit1 0.64 0.64
2014). Chitin reduces the protein digestibility of broilers NaCl 0.42 0.42
(Khempaka et al., 2011) but may have a positive effect dl-Met 0.27 0.37
on the poultry health: van Huis (2013) observed that by Sodium bicarbonate 0.25 0.25
feeding black soldier fly larvae, mealworms, or field Fe 0.07 0.07
l-Lys HCl 0.03 0.03
crickets to chickens, the use of antibiotics may be re-
Total 100.00 100.00
duced because diets containing around 3% of chitin in-
Analyzed composition2
creased populations of intestinal Lactobacillus spp. and
DM, % 86.62 (0.04) 88.14 (0.05)
decreased intestinal Escherichia coli and Salmonella
CP, % AF3 20.36 (0.24) 20.19 (0.16)
spp. Ballitoc and Sun (2013) showed that T. molitor up Ether extract, % AF 4.75 (0.03) 5.23 (0.04)
to 10% in a broiler diet did not affect palatability and Crude fiber, % AF 4.11 (0.11) 3.93 (0.12)
birds’ performance. However, few studies are available Ash, % AF 6.77 (0.04) 6.67 (0.07)
on the effect of insect meal inclusion in poultry diets. Calculated composition
The aim of this research was to study the effect of T. mo- Lys, % AF 1.24 1.18
litor larvae meal as a complete replacement of SBM in Met + Cys, % AF 0.89 0.96
a broiler diet from 30 to 62 d of age on growth perfor- Tyr, % AF 0.24 0.27
mance, nutrient digestibility, carcass traits, and chemical Thr, % AF 0.81 0.90
and physical traits of meat. Arg, % AF 1.49 1.32
ME, kcal/kg 2,812 2,849

MATERIAL AND METHODS
Animals, Diets, and Sampling
All the animals were humanely treated according
to the principles stated by the EC Directive 86/609/
EEC (Council Directive, 2008) regarding the protec-
tion of animals used for experimental and other scien-
tific purposes. The study was performed on a private
poultry farm of the province of Caserta (Italy) and
the experimental procedures received prior the ap-
proval from the Ethical Committee of the Department
of Veterinary Medicine and Animal Production of the
University Federico II (Napoli, Italy).
A total of eighty 30-d-old male Shaver brown broil-
ers (1.76 ± 0.19 kg average BW) were homogenously
divided into 2 groups (40 birds per group, each consist-
ing of 8 replicates of 5 birds). The broilers were housed
in a semiopened building and each replicate was placed
in a floor pen (1.0 by 1.0 m2/pen) furnished with rice
hulls as litter. Up to 62 d of age, the groups were fed
2 isoproteic and isoenergetic diets, whose ingredients
and chemical–nutritional characteristics are reported in
Table 1. The control group was fed a corn–SBM–based
1MinVit mixture provides per kilogram of the diet: 24 mg vitamin A
(retinyl acetate), 20 mg vitamin E (dl-α-tocopheryl acetate), 2.3 mg men-
adione, 0.05 mg vitamin D3 (cholecalciferol), 5.5 mg riboflavin, 12  mg
calcium pantothenate, 50 mg nicotinic acid, 600 mg choline chloride,
10 μg vitamin B12, 3 mg vitamin B6, 3 mg thiamine, 1 mg folic acid, and
0.50 mg d biotin. Trace mineral (per kilogram of diet): 80 mg Mn, 60 mg
Zn, 35 mg Fe, 8 mg Cu, and 0.60 mg Se (Nutrir srl, Eboli, Salerno, Italy).
2Data are expressed as average values (SE).
3AF = as-fed basis.
diet, whereas in the other group, the SBM was com-
pletely replaced by Tenebrio molitor larvae meal (TML;
Gaobeidian Shannon Biology Co., Ltd., Shannong, P.R.
China). The diets were formulated to meet poultry re-
quirements according to the NRC (1994). Celite (cata-
log number 61790-53-2; Sigma-Aldrich, St. Louis, Mo)
was added at 20 g/kg to the diets as a source of AIA,
which was used as an indigestible marker in the calcula-
tion of digestibility coefficients of the nutrients. Mash
diets and water were provided ad libitum. The light
regimen was 16 h of light per day.
Mortality rate was recorded daily and the average
maximum and minimum temperature and humidity in-
side the building were recorded weekly. Birds’ weight and
feed consumption were recorded at the beginning and at
 Insect meal effect on broiler performance
the end of the trial to calculate BW gain and feed conver-
sion ratio (FCR) in the period from 30 to 62 d of age.
At 62 d of age, 2 broilers per replicate (16 per
group) were randomly chosen, weighed, and slaugh-
tered in a specialized slaughterhouse. After bleeding
and removal of feathers, whole digestive tract, head,
neck, and legs, carcasses were weighed (dressed car-
casses) to evaluate the dressing percentage. The internal
viscera (liver, spleen, kidney, lungs, and heart) were re-
moved and weighed, and their weights were expressed
as a percentage of live weight. The yield of the eviscer-
ated carcass on broiler live weight was calculated. The
length of the different small (duodenum, jejunum, and
ileum) and large (sum of ceca length, colon, and rec-
tum) intestine tracts were measured. The full intestinal
length was calculated and expressed as percentage of
broiler live weight. From each carcass, the right breast
and leg were separated and weighed. In addition, the
left breast meat was also collected.
The apparent ileal digestibility coefficients of DM,
OM, and CP were measured using the AIA as an inter-
nal marker according to Vogtmann et al. (1975). After
its length was measured, the ileum was separated from
20 mm after Meckel’s diverticulum to 40 mm proxi-
mal to the ileocecal junction to avoid contamination of
other intestinal contents and digesta were pooled per
replicate (1 pool from 2 broilers per replicate; 8 pools
per group), immediately frozen, and subsequently
freeze-dried. Dried ileal digesta were ground to pass
a 1-mm sieve and stored at –20°C until chemical
analysis. The apparent ileal digestibility of nutrients
was calculated as follows: 100 – 100 × [(% AIA in the
diet/% AIA in the ileal content) × (% nutrient in the
ileal content/% nutrient in the diet)].
Physical Criteria
The left breast of each carcass was separated,
stored at –80°C, and sent to the Department of Agri-
Food Production and Environmental Sciences of the
University of Florence (Italy) to measure physical
characteristics of breast meat and skin.
At the laboratories, the pectoralis muscle of each
specimen was sectioned by a transversal cut, and the
caudal part was weighed, vacuum packed in a plastic
bag, and boiled for about 14 min, until the core tem-
perature arrived at 79°C. The bags containing the sam-
ples were removed from the water and cooled to room
temperature; then, the samples were removed from the
plastic bags, dried by means of disposable paper, and
weighed again to obtain the value for cooking loss de-
termination, according to the formula 100 × [cooked
sample weight (g)/raw sample weight (g)].
◊
The measurement of pH was performed at 2 differ-
ent sites of raw pectoralis muscle of each specimen with
a Mettler Toledo (Novate Milanese, Milano, Italy) mod-
el SevenGo SG2 pH meter. The values obtained were
considered 2 replicates and subsequently their mean
was utilised. Water-holding capacity was determined by
low-speed centrifugation at 1,500 rpm × 5 min (210 x
g for 5 min at a temperature of 4°C) in raw samples of
breast (in triplicate). Texture analyses were performed
using a Zwick Roell 109 texturometer (Zwick GmbH &
Co. KG, Ulm, Germany) with Text Expert II software,
equipped with a 200-N load cell. The Warner-Bratzler
shear test (shear force) was performed using a straight
blade (width of 7 cm), perpendicular to the muscle fiber
direction, at a crosshead speed of 30 mm/min to 50%
of total deformation. Maximum shear force, defined as
maximum resistance of the sample to shearing (Veland
and Torrissen, 1999) was determined.
All measurements were made at room temperature
on the raw pectoralis muscle and after cooking by boiling
at 2 different sites for each condition (raw or cooked) and
each specimen. The obtained values were considered 2
replicates and subsequently their mean value was utilised.
A Spectro-color116 colorimeter (Bell Technology
Ltd., Auckland, New Zealand), using Spectral qc 3.6
software, was used for color measurement accord-
ing to the CIELab system (CIE, 1976). In this system,
lightness (L*) is expressed on a 0 to 100 scale from
black to white, the redness index (a*) ranges from red
(+60) to green (–60), and the yellowness index (b*)
ranges from yellow (+60) to blue (–60). Chroma and
hue angle were calculated (CIE, 1976) as follows:
chroma = (a*2 + b*2)1/2 and hue = (tan–1 b*/a*).
Chroma and hue describe, respectively, color satura-
tion and taint. Color was measured on the external
side of the skin (at level of pectoralis muscle) and on
the external and internal sides of the pectoralis muscle,
raw and after cooking by boiling, at 2 different sites
for each condition (raw or cooked) and each specimen.
The values obtained were considered 2 replicates and
subsequently their mean value was utilised.
Chemical Criteria
Chemical analyses of the TML, SBM, and di-
ets were performed in triplicate using the AOAC
International (2004) procedures: DM (method 934.01),
ether extract (method 920.39), ash (method 942.05), CP
(method 954.01), and crude fiber (method 945.18). In
addition, for the TML, the ADF (method 973.18; AOAC,
2004) and the residual nitrogen in ADF (ADFN; meth-
od 954.01; AOAC, 2004) were determined and used to
estimate the amount of chitin (Bernard and Allen, 1997;
Finke, 2007) as follows: chitin (%) = ash free ADF (%)
◊ Bovera et al.

Table 2. Chemical characteristics and AA profile of Table 3. In vivo performance of broilers fed soybean
the 2 protein sources used in the trial (source: Bovera meal (SBM) or Tenebrio molitor larvae meal (TML) in
et al., 2015) the period 30 to 62 d of age (8 experimental units per
Tenebrio molitor Soybean
group, each consisting of 5 birds)
Item meal meal Item SBM TML RMSE1 P-value
Analyzed composition1 Live weight at 30 d, kg 1.76 1.76 0.04 0.9102
DM, % 93.90 (0.02) 90.92 (0.02) Live weight at 62 d, kg 3.37 3.47 0.11 0.3343
Ash, % AF2 4.69 (0.03) 6.13 (0.04) BWG2 30 to 62 d, g/d 50.49 53.40 3.31 0.3386
CP, % AF 51.93 (0.24) 44.51 (0.12) FI3 30 to 62 d, g/d 207.8 192.4 9.18 0.1096
Ether extract, % AF 21.57 (0.18) 1.84 (0.02) FCR4 30 to 62 d, g/d 4.13a 3.62b 0.18 0.0312
ADF, % AF 7.20 (0.15) 4.79 (0.09)
a,bMeans within a row with different superscripts differ (P < 0.05).
Calculated composition
1RMSE = root mean square error.
Arg, g/100 g protein 3.61 6.17
2BWG = BW gain.
His, g/100 g protein 2.11 2.51
3FI = feed intake.
Ile, g/100 g protein 2.63 4.60
4FCR = feed conversion ratio.
Leu, g/100 g protein 4.52 4.64
Lys, g/100 g protein 1.68 2.83
Met + Cys, g/100 g protein 1.62 3.18
Thr, g/100 g protein 2.71 3.43
Val, g/100 g protein 3.72 4.09
separated using Tukey’s test (SAS Inst. Inc.) at P < 0.05.
Trp, g/100 g protein 1.75 1.45
The replicate was considered the experimental unit.
1Data are expressed as average values (SE).
2AF = as-fed basis. RESULTS

– ADFN × 6.25 (%). The full AA composition of TML

and SBM used for diet AA calculation was supplied by
the manufacturer and was reported in a previous study
in which the same insect meal was used (Bovera et al.,
2015). However, the content of the most important es-
sential AA as a percent of CP was as follows: 1.62%
Met + Cys, 1.68% Lys, 1.75% Tyr, 2.71% Thr, and
3.61% Arg. Table 2 summarizes the chemical charac-
teristics and AA profile of the 2 protein sources (TML
and SBM) used in the trial. National Research Council
(1994) equations were used to calculate the amount of
AA and ME of the diets.
The raw meat from the right breast dissection was
homogenized, freeze-dried, and analyzed using these
Association of Official Analytical Chemists (1984)
procedures: moisture (method 950.46), fat (method
930.27), and ash (method 950.153). Protein content
was calculated by difference (Bovera et al., 2012).
Statistical Analysis
Growth Performance and Ileal Digestibility
No deaths were observed during the trial in either
group. The average maximum and minimum tempera-
ture inside the building were 21 ± 2.2 and 14 ± 1.9°C, re-
spectively, during the entire experimental period, and the
average humidity was 65.3 ± 8.7%. The TML showed
the following chemical composition (on an as-fed basis):
93.9% DM, 4.69% ash, 51.9% CP, 21.6% ether extract,
and 7.2% ADF.
Table 3 shows the growth performance of broil-
ers fed SBM or TML. No differences were observed
between the SBM and TML groups for almost all the
criteria presented in the table, but FCR in the entire ex-
perimental period (from 30 to 62 d) was greater (P <
0.05) in the TML group compared with the SBM group.
Table 4 reports the apparent ileal digestibility co-
efficients of DM, OM, and CP of broilers fed the SBM
or TML diets. All the values were greater (P < 0.01) in
broilers fed SBM than the other group.

Data were analyzed by 1-way ANOVA using the Carcass Traits

GLM procedure of SAS (SAS Inst. Inc., Cary, NC), ac-
cording to the model
Yij = m + CPi + eij,
in which Y is the single observation, m is the general
mean, CP is the effect of protein source (i = SBM or
TML), and e is the error. Differences among means were
Table 5 shows the carcass traits of slaughtered
broilers. The full digestive system in broilers fed SBM
had a lower (P < 0.05) absolute and relative weight
than that of broilers fed TML. Also, the weight and
the percentage of spleen in the SBM group were lower
(P < 0.05) than those of the TML group, whereas no
differences were observed between the groups for the
other carcass traits reported in the table.
 Insect meal effect on broiler performance ◊

Table 4. Dry matter, OM, and CP ileal digestibility of Table 5. Live weight and carcass traits of broilers
broilers fed soybean meal (SBM) or Tenebrio moli- selected for euthanasia fed soybean meal (SBM) or
tor larvae meal (TML) at 62 d of age (8 experimental Tenebrio molitor larvae meal (TML) at 62 d of age
units per group, each consisting of 2 birds) (8 experimental units per group, each consisting of 2
Item SBM TML RMSE1 P-value
birds)
DM, % 88.22A 86.42B 0.95 0.008 Item SBM TML RMSE1 P-value
OM, % 88.69A 86.89B 1.01 0.011 Weight, g
CP, % 87.35A 80.20B 0.70 <0.0001 Live weight 3,376 3,469 341 0.470
A,BMeans within a row with different superscripts differ (P < 0.01). Digestive system 357.3b 424.1a 67.5 0.015
1RMSE = root mean square error. Head 88.3 84.9 13.2 0.497
Dressed carcass 2,428 2,515 276 0.194
Carcass without internal viscera 2,313 2,361 241 0.601
Liver 59.7 58.1 6.8 0.521
Kidney 16.8 18.1 3.4 0.326
Table 6 shows the length of the different traits and Hearth 16.9 18.5 2.2 0.071
of the full intestine as well as the weight and relative Lungs 24.6 26.7 4.0 0.271
incidence of ceca, right breast, and thigh. The entire Spleen 4.40b 5.57a 1.20 0.041
length of intestine was greater (P < 0.05) in the group Percentage on live weight, %
fed TML in comparison with the other group and the Digestive system 10.4b 12.7a 2.5 0.021
same happened when intestinal length was expressed Head 2.61 2.45 0.58 0.473
as percentage of broiler BW (P < 0.05). Among the dif- Carcass yield 71.2 73.2 8.4 0.379
ferent intestinal tracts, the ileum and ceca of broilers Eviscerated carcass yield 68.5 68.9 8.1 0.901
fed TML had a greater (P < 0.05) length than those of Liver 1.77 1.67 0.18 0.146
Kidney 0.50 0.52 0.15 0.395
broilers fed SBM. Also, ceca weight (as absolute value
Hearth 0.50 0.55 0.24 0.239
or percentage on live weight) in broilers fed TML was
Lungs 0.73 0.77 0.16 0.961
greater (P < 0.05) than that of broilers fed SBM.
Spleen 0.12B 0.16A 0.05 0.008
a,bMeans
within a row with different superscripts differ (P < 0.05).
Physical and Chemical Characteristics of Breast Meat A,BMeanswithin a row with different superscripts differ (P < 0.01).
1RMSE = root mean square error.
Table 7 reports the physical characteristics of skin
and meat obtained from the left breast of slaughtered
broilers. Only muscle pH and cooking losses were af-
fected by dietary treatment and both were greater (P <
0.05) in broilers fed TML than in broilers fed SBM. and length obtained in the present study can be attrib-
Chemical characteristics of meat obtained from right uted to the level of chitin supplied by TML. Based on
breast of slaughtered broilers (Table 8) were unaffect- the analysis results, the amount of chitin in the insect
ed by dietary treatments. meal used in this study was 4.62%, as fed, correspond-
ing to 64.2% of ash free ADF, in line with the finding
DISCUSSION of Finke (2007), who indicated that the ADF fraction in
insects contained an amount of protein from 9.3 to 32.7%
In the present trial, an important effect of TML inclu- and the amount of chitin ranged from 2.7 to 49.8 g/kg.
sion in broiler diet was on the characteristics of both the Chitin can modulate the intestinal development through
small and the large intestine. The results showed that the 2 mechanisms: the first is the reduction of nutrient digest-
ileum and ceca were the intestinal tracts mainly affected ibility and the second is a prebiotic activity. Chitin is a
by dietary treatments in terms of length and weight and, linear polymer of b-(1-4) N-acetyl-d-glucosamine units
as a consequence, also the entire intestinal length and and, because it is indigestible, can affect the digestibility
gastrointestinal tract (GIT) weight were affected. of protein in poultry and thus reduce the general diges-
Based on the current knowledge, very few studies tion of diet DM. This is clearly shown by the results of
are available in the literature on the effect of insect meals the present research as apparent ileal digestibility coeffi-
on GIT development of broilers. Ballitoc and Sun (2013) cients of DM and OM in broilers fed the TML diet were
found that the small intestine weight was increased when 2% lower than in broilers fed the SBM diet and that of
broilers were fed ground yellow mealworms at up to a CP as 8.2% lower. Also, Schiavone et al. (2014) found a
10% inclusion level in comparison with the control, but decrease in protein digestibility when broilers were fed
no differences were observed among the other intestinal TML at a 25% inclusion level in the diet. In broilers, the
tracts. The effect of TML diet on intestinal tracts weight length and weight of the small intestine increase when di-
◊ Bovera et al.

Table 6. Characteristics of digestive tract, breast, and Table 7. Physical properties of breast muscle and skin
thigh of broilers fed soybean meal (SBM) or Tenebrio of broilers fed soybean meal (SBM) or Tenebrio moli-
molitor larvae meal (TML) at 62 d of age (8 experi- tor larvae meal (TML) at 62 d of age (8 experimental
mental units per group, each consisting of 2 birds) units per group, each consisting of 2 birds)
Item SBM TML RMSE1 P-value Item SBM TML RMSE1 P-value
Length, cm Left breast weight, g 221.1 214.5 36.2 0.627
Duodenum 38.7 43.0 7.6 0.120 Left breast skin weight, g 21.2 22.9 4.8 0.348
Jejunum 87.6 89.2 18.7 0.818 pH 5.95B 6.12A 0.14 0.004
Ileum 89.9b 99.2a 12.5 0.022 Water-holding capacity, % 95.5 95.9 1.4 0.462
Colon 12.5 13.8 10.9 0.756 Shear force, N 143.0 140.3 7.5 0.337
Rectum 3.16 4.08 1.49 0.096 Cooking loss, % 21.4b 23.6a 2.7 0.032
Ceca 43.1B 48.7A 4.5 0.002 Skin color
Full intestine 274.9b 298.0a 27.0 0.025 Lightness 60.7 62.8 6.1 0.382
Weight, g Redness 4.66 3.77 0.36 0.332
Ceca 19.4B 24.1A 3.2 0.001 Yellowness 13.2 14.2 0.5 0.445
Right breast 238.7 235.7 42.9 0.852 Chroma 14.2 14.9 0.7 0.605
Right thigh 362.3 375.0 55.2 0.543 Hue 71.1 76.4 4.3 0.126
Percentage on live weight, % External breast color
Full intestinal length 8.14a 8.60b 1.10 0.048 Lightness 44.2 44.0 7.2 0.926
Cecal weight 0.57b 0.70a 0.19 0.011 Redness 1.18 1.07 0.05 0.249
Right breast weight 10.3 9.94 1.43 0.467 Yellowness 0.78 0.69 0.02 0.386
Right thigh weight 15.6 15.9 1.91 0.703 Chroma 1.92 1.91 0.25 0.977
a,bMeans
within a row with different superscripts differ (P < 0.05). Hue 150.3 168.1 22.1 0.612
A,BMeanswithin a row with different superscripts differ (P < 0.01). Internal breast color
1RMSE = root mean square error. Lightness 41.9 40.5 3.2 0.673
Redness 3.12 2.98 0.41 0.263
Yellowness 6.31 5.86 0.36 0.636
Chroma 6.76 6.99 0.22 0.865
ets have lower digestibilities (Smits and Annison, 1996). Hue 79.9 70.0 5.1 0.069
It is well documented that feeding a poorly digestible Cooked breast
diet to broilers results in an increase of intestinal length Shear force, N 69.3 73.2 4.3 0.597
and also in an increase in intestinal relative volume and Lightness 68.9 68.3 5.3 0.918
weight (van der Klis and Jansman, 2002). This is in line Redness 3.25 4.63 0.29 0.497
with the results of the present study as the full GIT was Yellowness 10.9 10.8 0.4 0.897
heavier in broilers fed TML, suggesting a higher relative Chroma 11.6 13.9 0.6 0.051
Hue 71.4 93.9 4.3 0.063
volume of the GIT. The increase of volume and length of
GIT when low digestible diets are fed is a compensatory a,bMeans
within a row with different superscripts differ (P < 0.05).
A,BMeans
mechanism as the organism tries to increase the amount within a row with different superscripts differ (P < 0.01).
1RMSE = root mean square error.
of feed intake as well as the surface available for nutrient
absorption (Borin et al., 2006).
Very interestingly, the decrease of nutrient digest- the insect meal protein had a low content of essen-
ibility observed in the TML group had no effects on tial AA (Met, Cys, Lys, and Trp) and that the cuticle
growth performance, and broilers of the 2 groups proteins presented an AA composition different from
reached a not-different live weight at slaughter. In ad- that of the whole insect (Finke, 2007). Based on these
dition, broilers fed TML showed an improved FCR considerations, the hypothesis is that the amount of
compared with the control, in agreement with the essential AA available for digestion was sufficient to
findings of Ballitoc and Sun (2013), who observed a sustain broiler growth, also in the case of the TML diet.
decreasing trend in FCR when TML was added from In addition, several authors (Hill et al., 2005; Dahiya
0 to 10% in a broiler diet. In this regard, it is impor- et al., 2006; Pieper et al., 2008) observed that when
tant to note, first, that protein had the most significant diets with low digestibility were fed, the indigestible
reduction in digestibility in the TML diet when com- portion of the feed remains in the intestinal tract and
pared with the other tested chemical characteristics can affect the growth performance of broilers by act-
and, second, that the increase of indigestible protein in ing as a substrate for intestinal bacteria. In this regard,
the TML diet can be ascribed to the proteins linked to Widyaratne and Drew (2011) found no differences in
chitin and therefore present in the insect exoskeleton daily weight gain, feed intake, and FCR of growing
(Belluco et al., 2013). It also has to be considered that
 Insect meal effect on broiler performance
Table 8. Chemical traits of breast meat of broilers fed
soybean meal (SBM) or Tenebrio molitor larvae meal
(TML) at 62 d of age (8 experimental units per group,
each consisting of 2 birds)
Item SBM TML RMSE1 P-value
Moisture, % 72.8 73.1 0.7 0.314
Ash, % 1.55 1.29 0.44 0.126
Protein, % 24.2 24.1 1.1 0.697
Lipid, % 1.38 1.51 0.24 0.143
1RMSE = root mean square error.
broilers fed diets with the same protein level but dif-
fering in CP ileal digestibility coefficients.
However, the effect of chitin on increasing intestinal
length and weight also can be ascribed to its ability to act
as prebiotic (Bovera et al., 2015). Khempaka et al. (2011)
reported that the inclusion of shrimp head meal (another
chitin source) at 15 and 20% as well as the addition of
1.9% of purified chitin in a broiler diet significantly in-
creased the production of butyric volatile fatty acid in
ceca. Butyric acid is considered the prime enterocyte
energy source (Bovera et al., 2010) and it is also neces-
sary for the suitable development of the gut-associated
lymphoid tissue (Mroz, 2005). It is documented that bu-
tyrate is the major intestinal energy source even when
other fuel sources (glucose or glutamine) are available
and could stimulate the growth of colorectal and ileal
mucosal cells (Topping and Clifton, 2001; Montagne et
al., 2003). This is important for maintaining the function
of the GIT, not just of the ceco-colon (Montagne et al.,
2003). When a higher amount of butyric acid is available,
the increase of nutrients for enterocytes enhances blood
flow through the intestine and then tissue oxygenation
and nutrient transport and absorption (Mahdavi and
Torki, 2009). The mechanism of action may involve lo-
cal neural networks as well as chemoreceptors together
with direct effects on smooth muscle cells (Mroz, 2005).
These signals may induce the production of growth fac-
tors able to stimulate the growth of the different intestine
tracts (Mahdavi and Torki, 2009).
Most of carcass traits presented in Tables 5 and
6 showed a high variability (root mean square er-
ror greater than 10%) and this can affect the lack of
statistical significance observed in the present trial.
It is probable that the strain used in the trial (Shaver
brown), being primarily selected for egg production,
had a wide variability for body composition traits that
and a most consistent number of replications needs to
reach definitive conclusion about these criteria.
The highest weight and incidence of the spleen in
broilers fed TML as a protein source can be attributed
to an increase in the activity of the immune system.
Several authors (Awadalla, 1998; Kusnadi and Djulardi,
◊
2011) reported that broilers under different stress condi-
tions (high temperatures, vaccinations, etc.) had a lower
spleen weight in comparison with the respective control
groups. This is due to the increase of plasma corticos-
terone that depresses growth of lymphoid organs such
as spleen or bursa Fabricii (Siegel, 1995). It could lead
to disturbances of immune system production (Kusnadi
and Djulardi, 2011). Also, this result can be attributed
to the intake of chitin that seems to exhibit a bacterio-
static effect on Gram-negative bacteria, E. coli, Vibrio
cholerae, Shigella dysenteriae, and Bacteroides fragilis
(Vidanarachchi et al., 2010), and also showed antifungal
and antimicrobial proprieties (Khoushab and Yamabhai,
2010). In this regard, van Huis (2013) observed that
feeding insects to chickens may decrease the use of
antibiotics in the poultry industry, and this should be
very important because of their well-known adverse ef-
fects on human health (drug-resistant bacteria strains).
Bovera et al. (2015) observed that the albumin:globulin
ratio was decreased when broilers were fed an insect
meal diet and Griminger and Scanes (1986) stated that
a low albumin:globulin ratio indicates better disease re-
sistance and immune response of birds.
The absence of differences in most physical meat
and skin properties (in particular, color and tenderness)
is very important as, in particular, color can influence
consumer acceptance of meat. Consumers will often
reject products in which the color varies from the ex-
pected normal appearance, and consequently, this pa-
rameter is often used to determine the economic value
of food (Qiao et al., 2001). The results on raw (internal
and external) and cooked meat, as well as on skin, indi-
cated that meat from broilers fed insect meal could be
accepted without problem by the consumers. However,
the pH values and cooking losses, higher for the breast
of poultry fed insects, could indicate a decreased qual-
ity of meat obtained by feeding insects. It is important
to observe that, for both groups, breast pH falls in the
range of “normal” meat, as for values lower than 5.7 and
higher than 6.2, breast broiler can be classified as PSE
(pale, soft, and exudative) or DFD (dark, firm, and dry),
respectively (Fletcher et al., 2000). Therefore, breast
meat of broilers involved in the present trial can be con-
sidered “normal” and the higher values recorded in the
TML group can be ascribed to a lower amount of gly-
cogen in the muscle. The values of cooking losses are
in line with other findings in literature for broiler breast
meat (Hashim et al., 2013), and even if they were higher
in the TML group, water-holding capacity was not af-
fected by dietary treatment.
◊ Bovera et al.

Conclusions Council Directive, 2008. http://ec.europa.eu/food/fs/aw/aw_legis-

lation/scientific/86-609-eec_en.pdf.
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