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Background: The present work is aimed at evaluating the effect of different inclusion levels of a partially defatted black soldier fly (Hermetia illucens, L.; HI) larva meal for ducks. A total of 192 female 3-day-old Muscovy ducklings (Cairina moschata domestica, Canedins R71 L White, Grimaud Freres Selection, France) were divided into 4 groups, assigned 4 different dietary treatments (6 replicates/treatment and 8 birds/replicate) and reared from 3 to 50 days of age. HI larva meal was included at increasing levels (0, 3%, 6% and 9%, HI0, HI3, HI6 and HI9, respectively) in isonitrogenous and isoenergetic diets formulated for 3 feeding phases: starter (3-17 days of age), grower (18-38 days of age) and finisher (39-50 days of age). The growth performance and apparent total tract digestibility were evaluated during the trial using titanium dioxide as an inert marker (0.3% of inclusion). At 51 days of age, two birds per pen were slaughtered and histomorphological investigations were performed. Results: The live weight and average daily gain showed a quadratic response to increasing HI meal in the grower period (minimum corresponding to the HI6 group). No effects of dietary inclusion levels were observed for the daily feed intake or feed conversion ratio. The apparent dry matter and organic matter digestibility were not affected by the dietary treatment. A linear decrease was observed for the crude protein apparent digestibility in the starter period (minimum for the HI9 groups). The ether extract apparent digestibility increased linearly during the grower and finisher periods (minimum for the HI0 group). The morphometric indices were not influenced by the dietary treatments. Conclusions: The inclusion of up to 9% of HI partially defatted larva meal in the diet of ducks did not cause any effect on growth performance, as well as the apparent digestibility. Moreover, dietary HI inclusion preserved the physiological intestinal development.
R E S E A R C H Open Access
Nutritional effects of the dietary inclusion
of partially defatted Hermetia illucens larva
meal in Muscovy duck
Marta Gariglio
1
, Sihem Dabbou
1
, Ilaria Biasato
2
, Maria Teresa Capucchio
1
, Elena Colombino
1
,
Fuensanta Hernández
3
, Josefa Madrid
3
, Silvia Martínez
3
, Francesco Gai
4
, Christian Caimi
2
, Sara Bellezza Oddon
2
,
Marco Meneguz
2
, Angela Trocino
5
, Riccardo Vincenzi
6
, Laura Gasco
2,4*
and Achille Schiavone
1,4,7
Abstract
Background: The present work is aimed at evaluating the effect of different inclusion levels of a partially defatted
black soldier fly (Hermetia illucens, L.; HI) larva meal for ducks. A total of 192 female 3-day-old Muscovy ducklings
(Cairina moschata domestica, Canedins R71 L White, Grimaud Freres Selection, France) were divided into 4 groups,
assigned 4 different dietary treatments (6 replicates/treatment and 8 birds/replicate) and reared from 3 to 50 days
of age. HI larva meal was included at increasing levels (0, 3%, 6% and 9%, HI0, HI3, HI6 and HI9, respectively) in
isonitrogenous and isoenergetic diets formulated for 3 feeding phases: starter (317 days of age), grower (1838 days of
age) and finisher (3950 days of age). The growth performance and apparent total tract digestibility were evaluated
during the trial using titanium dioxide as an inert marker (0.3% of inclusion). At 51days of age, two birds per pen were
slaughtered and histomorphological investigations were performed.
Results: The live weight and average daily gain showed a quadratic response to increasing HI meal in the grower
period (minimum corresponding to the HI6 group). No effects of dietary inclusion levels were observed for the daily
feed intake or feed conversion ratio. The apparent dry matter and organic matter digestibility were not affected by the
dietary treatment. A linear decrease was observed for the crude protein apparent digestibility in the starter period
(minimum for the HI9 groups). The ether extract apparent digestibility increased linearly during the grower and
finisher periods (minimum for the HI0 group). The morphometric indices were not influenced by the dietary
treatments.
Conclusions: The inclusion of up to 9% of HI partially defatted larva meal in the diet of ducks did not cause any
effect on growth performance, as well as the apparent digestibility. Moreover, dietary HI inclusion preserved the
physiological intestinal development.
Keywords: Black soldier fly, Digestibility, Ducks, Histopathology, Insect, Performance
Introduction
With an increase of 1.8% per year estimated until 2050,
poultry production is one of the fastest growing sectors [1].
The production of duck meat has undergone a great ex-
pansion in recent years, passing from 2.23 million tonnes
in 1996 to over 4.5 million tonnes in 2016 [2]. Duck
production plays an important role in Italy, with 3.27 thou-
sand tonnes being produced in 2017 [3]. Duck farming has
agreatpotential,sinceducksareamongthefastestpro-
ducers of animal proteins and may contribute to the future
nutritional needs of the growing world population [4].
The reduced availability of natural resources and the
environmental impact of vegetable production require
the research of alternative forms of protein for animal
production. Considering the feeding habits of birds, in-
cluding poultry (chicken, duck, turkey and geese), in-
sects can represent a valuable alternative to the common
© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
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(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
* Correspondence: laura.gasco@unito.it
2
Department of Agricultural, Forest and Food Sciences, University of Turin,
largo Paolo Braccini 2, Turin, Grugliasco 10095, Italy
4
Institute of Science of Food Production, National Research Council, largo
Paolo Braccini 2, Turin, Grugliasco 10095, Italy
Full list of author information is available at the end of the article
Gariglio et al. Journal of Animal Science and Biotechnology (2019) 10:37
https://doi.org/10.1186/s40104-019-0344-7
protein sources, thanks to their nutritional characteris-
tics [5]. The use of insects in feeds leads to advantages
from both an environmental and nutritional point of
view. Compared to conventional vegetable protein
sources, insects rearing requires very little soil and water,
and their low emission of greenhouse gases and ammo-
nia implies an overall low environmental impact. A
study conducted by an EU initiative PROteINSECT esti-
mated that 1 ha of land can produce up to 150 tons of
insect protein per year. Instead, 1 ha of land can produce
less than 1 ton of soybean protein [6]. Moreover, insects
can be reared on organic waste (such as fruit and vege-
table) and can converting them into nutrients of high
biological value, thanks to their high feed conversion ef-
ficiency [7,8]. Researchers have recently been evaluating
the use of insects in animal feeding, and they have
highlighted that insects could be used as a partial or
total substitute for the currently used protein sources.
The most promising species are Hermetia illucens (HI)
[912], Musca domestica [13,14] and Tenebrio molitor
(TM) [1518]. Thanks to the favourable nutrient com-
position of HI, in terms of protein content (3763%),
amino acid profile, fat content (739%) and other
macro- and micronutrients, it could be considered a
valuable alternative to common protein sources, such as
soybean meal (SBM) [19]. The effects of the inclusion of
HI larva meal and oil on growth performance have been
investigated in many studies [1012,2022], with con-
flicting results being obtained. Only a few works are
available regarding the digestibility of HI meal in poultry
[9,10,2224] and these show extremely variable results
in terms of dry matter (DM), crude protein (CP) and
ether extract (EE). In these studies, nutrient digestibility
was frequently influenced, according to the authorsin-
terpretation, by the chitin content of the diets, which
can negatively affect digestibility. Despite the limited
availability of studies, the evaluation of the gut histomor-
phometry represents a relevant research topic, since it
could affect the growth performance and the digestibility
of a diet [25], depending on the protein source and level
of the diet [26,27]. A recent study by Cutrignelli et al.
[22] has found that the inclusion of HI larva meal in lay-
ing hen diets significantly affects the gut histomorpho-
metry, resulting in a lower villi-to-crypt ratio than SBM
group. The above-mentioned studies have shown a wide
variability and more research is required to obtain a bet-
ter understanding of the effect of the inclusion of HI in
poultry diets.
To date, no research has investigated the possibility of
including insect meal in duck diet. Therefore, the aim of
the study was to evaluate the growth performance, di-
gestibility and intestinal morphology of female broiler
ducks (Cairina moschata domestica) fed diets including
HI meal.
Materials and methods
Birds and husbandry
The present trial was performed at the poultry facility of
the University of Turin (Italy). The experimental proto-
col (Prot. No. 380576, 4
th
December 2017) was approved
by the Bioethical Committee of the University of Turin
(Italy). The poultry house was 7 m wide × 50 m long × 7
m high, and was equipped with a waterproof floor and
walls, completely covered by tiles and had an automatic
ventilation system. A total of 192, 3-day-old, females
Muscovy ducks (Canedins R71 L White, Grimaud Freres
Selection, France) were housed in 24 pens and randomly
allotted 4 dietary treatments, each group consisting of 6
pens as replicates with 8 birds per pen (average live weight
(LW): 71.32 ± 2.95 g). Each pen was 1.20 m wide × 2.20 m
long and was covered with rice hulls as litter. During the
first 3 weeks, the animals were heated by infrared lamps.
The lighting schedule was 23 h light : 1 h darkness until
day 3 of the trial, and thereafter the dark period was grad-
ually increased to 6 h and maintained constant until
slaughtering. The environmental parameters were moni-
tored daily during the whole period of the trial.
Diets
Four dietary treatments were obtained in which increas-
ing levels of a partially defatted HI larva meal (Hermetia
Deutschland GmbH & Co KG, Baruth/Mark, Germany)
were included. In order to assess the effect of HI meal
inclusion in the diets, HI meal was included as a substi-
tute to gluten meal, a commonly used raw material in
commercial duck feeding, which nutritional value is
comparable to HI meal.
The control group (HI0) was fed a diet without insect
meal (9% inclusion of corn gluten meal); 3%, 6% and 9%
of the gluten meal was substituted with HI larva meals
in the HI3, HI6, and HI9 diets, respectively (Table 1).
The diets were isonitrogenous and isoenergetic and
were formulated using the apparent metabolisable en-
ergy (AMEn) values for a partially defatted HI, which
had been calculated by Schiavone et al. [23] and accord-
ing to INRA for the other ingredients [28] both for
broiler chickens. The essential amino acids requirements
were calculated with matrix value for digestible amino
acids according to Schiavone et al. [23] for HI meal and
Pingel et al. [29] for the other ingredients, for chickens and
ducks, respectively. Feed and water were provided ad libi-
tum throughout the trial. A 3-phase feeding program was
applied: a starter diet (days 3 to 17), a grower diet (days 18
to 38) and a finisher diet (days 39 to 51).
Chemical analysis of the HI meal and experimental diets
The experimental diets were ground to pass through a
0.5-mm sieve and stored in airtight plastic containers.
Gariglio et al. Journal of Animal Science and Biotechnology (2019) 10:37 Page 2 of 10
HI larva meal and the experimental diets were analysed
for DM (AOAC, method number #934.01), ash (AOAC,
method number #942.05), CP (AOAC, method number
#984.13), neutral detergent fiber (NDF; AOAC, method
number #2002.04) and acid detergent fiber (ADF; AOAC
method number #973.18) [30]. The EE (AOAC, method
number #2003.05) was determined according to Inter-
national AOAC [31].
Table 1 Ingredients (g/kg as fed) and nutrient composition (%) of the experimental diets
a
Ingredients Starter period (days 3 to 17) Grower period (days 18 to 38) Finisher period (days 39 to 50)
HI0 HI3 HI6 HI9 HI0 HI3 HI6 HI9 HI0 HI3 HI6 HI9
Corn meal 600.0 600.0 600.0 600.0 638.0 638.0 638.0 638.0 670.0 670.0 670.0 670.0
Soybean meal 212.0 212.0 212.0 212.0 160.0 160.0 160.0 160.0 100.0 100.0 100.0 100.0
HI larva meal 0.0 30.0 60.0 90.0 0.0 30.0 60.0 90.0 0.0 30.0 60.0 90.0
Bran 42.5 42.5 42.5 42.5 36.3 36.3 36.3 36.3 66.2 66.2 66.2 66.2
Corn gluten meal 90.0 60.0 30.0 0.0 90.0 60.0 30.0 0.0 90.0 60.0 30.0 0.0
Soybean oil 16.5 16.5 16.5 16.5 28.5 28.5 28.5 28.5 34.5 34.5 34.5 34.5
Dicalcium phosphate 10.0 10.0 10.0 10.0 13.0 13.0 13.0 13.0 4.0 4.0 4.0 4.0
Calcium carbonate 8.0 8.0 8.0 8.0 14.0 14.0 14.0 14.0 17.4 17.4 17.4 17.4
Sodium chloride 2.5 2.5 2.5 2.5 2.5 2.5 2.5 2.5 2.5 2.5 2.5 2.5
Sodium bicarbonate 2.0 2.0 2.0 2.0 2.0 2.0 2.0 2.0 2.0 2.0 2.0 2.0
DL-methionine 2.5 2.5 2.6 2.8 1.7 1.8 1.9 2.2 0.3 0.4 0.5 0.8
L-lysine 3.9 3.9 3.8 3.6 3.9 3.8 3.7 3.4 3.0 2.9 2.8 2.5
Mineral-vitamin premix
b
5.0 5.0 5.0 5.0 5.0 5.0 5.0 5.0 5.0 5.0 5.0 5.0
Choline chloride 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1
Optifos 250 bro 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0
Avizyme 1500× 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0
Titanium dioxide 3.0 3.0 3.0 3.0 3.0 3.0 3.0 3.0 3.0 3.0 3.0 3.0
Total 1,000 1,000 1,000 1,000 1,000 1,000 1,000 1,000 1,000 1,000 1,000 1,000
AMEn
c
, kcal/kg 2,897 2,892 2,888 2,884 2,994 2,990 2,986 2,981 3,052 3,048 3,044 3,040
Nutrient composition
d
DM, % 89.3 89.8 90.1 89.7 88.8 89.2 89.1 89.1 88.7 89.0 89.3 88.9
CP, % DM 25.1 24.7 25.2 24.8 23.0 22.5 22.5 22.4 20.2 20.2 20.1 20.1
EE, % DM 4.7 4.8 4.9 5.1 6.2 6.2 6.4 6.6 7.3 7.4 7.6 7.7
NDF, % DM 12.7 12.3 12.7 12.4 12.9 13.1 12.6 12.7 12.7 13.1 12.7 12.9
ADF, % DM 3.4 3.5 3.7 3.3 3.5 3.5 3.7 3.5 3.4 3.5 3.5 3.4
Ash, % DM 5.6 6.0 5.6 5.8 7.8 7.5 7.5 8.0 6.5 6.4 6.9 6.7
Fatty acid composition, % of total FAME
SFA 19.0 20.7 23.9 26.9 17.7 20.2 22.5 25.5 17.3 19.4 22.2 23.7
MUFA 27.6 26.1 25.5 24.6 25.8 24.9 24.2 23.5 24.9 24.8 23.8 23.8
PUFA 52.8 52.6 49.9 47.9 55.9 54.4 52.7 50.5 57.2 55.3 53.5 51.8
PUFA/SFA 2.78 2.54 2.08 1.78 3.15 2.69 2.34 1.98 3.31 2.85 2.40 2.18
n-3 3.3 3.4 3.4 3.3 4.1 4.2 4.1 4.1 4.5 4.5 5.3 5.0
n-6 49.1 48.9 46.1 44.3 51.6 49.9 48.2 46.1 52.3 50.4 47.9 46.4
n-6/n-3 14.88 14.38 13.56 13.42 12.58 11.88 11.76 11.24 11.62 11.20 9.04 9.28
HI Hermetia illucens,AMEn apparent metabolisable energy, DM dry matter, CP crude protein, EE ether extract, NDF neutral detergent fiber, ADF acid detergent
fiber, FAME fatty acid methyl esters, SFA saturated fatty acids, MUFA monounsaturated fatty acids, PUFA polyunsaturated fatty acids
a
Four dietary treatments: HI0 = control; HI3 = 3% inclusion level of Hermetia illucens; HI6 = 6% inclusion level of Hermetia illucens; HI9 = 9% inclusion level of Hermetia illucens
b
Mineral-vitamin premix: vitamin A (retinyl acetate), 12,500 IU; vitamin D
3
(cholecalciferol), 3,500 IU; vitamin E (DL-a-tocopheryl acetate), 40 mg; vitamin K
(menadione sodium bisulfite), 2.0 mg biotin, 0.20mg; thiamine, 2.0 mg; riboflavin, 6.0 mg; pantothenate, 15.21 mg; niacin, 40.0 mg; choline, 750.0 mg pyridoxine,
4.0 mg; folic acid, 0.75mg; vitamin B
12
, 0.03 mg; Mn, 70mg; Zn, 62.15 mg; Fe, 50.0 mg; Cu, 7.0 mg; I, 0.25mg; Se, 0.25 mg
c
Calculated according to Schiavone et al. [23] for HI meal and INRA [28] for the other ingredients
d
The chemical analyses were carried out on three replicates of each feed sample
Gariglio et al. Journal of Animal Science and Biotechnology (2019) 10:37 Page 3 of 10
The chitin content of HI meal was determined accord-
ing to Finke et al. [32] using ADF adjusted for its nitrogen
content.
In order to perform the amino acids determination in
HI meal, samples were prepared using a 22-h hydrolysis
step in 6 mol/L HCl at 112 °C under a nitrogen atmos-
phere. Performic acid oxidation occurred prior to acid
hydrolysis for methionine and cystine. The amino acids
in hydrolysate was determined by means of HPLC after
postcolumn derivatization, according to the procedure
described by Madrid et al. [33]. Tryptophan was not de-
termined. The lipid extraction and fatty acids profiling
of the experimental diets [3436] were carried out at the
laboratory of the Department of Animal Medicine, Pro-
duction and Health, University of Padua, Legnaro, Italy
according to the method of Christie [37]. All the analysis
were performed in triplicate (Table 1).
The chemical composition of the HI meal was the fol-
lowing: DM, 92.41 g/kg; CP, 56.71% DM; EE, 10.70% DM;
ash, 16.38% DM; chitin, 6.43% DM; DL-methionine, 0.63%
DM and L-lysine, 1.89% DM.
Growth performance
Birds were individually labeled with a wing mark and
weighed at their arrival. Mortality and clinical signs of ill-
ness were monitored daily throughout the trial. The live
weight (LW) of the animals was recorded at an individual
level at the beginning and at the end of each feeding phase
(3, 17, 38 and 50 days of age), and the feeds were removed
2 h before the birds were weighed. The average daily gain
(ADG) and average daily feed intake (DFI) were recorded
at a pen level at the end of each growth period.
The feed conversion ratio (FCR) was calculated for
each growth period and for the overall experimental
period. All the measurements were made using elec-
tronic scales (Sartorius-Signum®, Bovenden, Germany).
Digestibility trial
The digestibility trial was performed at the end of each
feeding phase using titanium dioxide (TiO
2
, 0.3 g/kg) as
an indigestible marker in each experimental diet (Table 1),
in order to evaluate the apparent total tract digestibility
coefficients (ATTDC). The Kaczmarek et al. [38]method
was used to collect the excreta, with slight modifications,
as reported by Dabbou et al. [39]. Briefly, all the birds were
removed from each pen and housed in wire-mesh cages
(n= 6 replicates) for approximately 1 h/d for four con-
secutive days to collect fresh excreta samples.
After collection, the excreta samples, from which the
feathers and litter had been removed, were immediately
frozen at 20 °C. At the end of each collection period, the
excreta were pooled, lyophilized, grounded and stored at
4 °C. All the analyses were carried out on two replicates
for each sample. The ATTDC was evaluated for DM, CP,
EE and OM. The uric acid (UA) content in the excreta
samples was determined spectrophotometrically (UNI-
CAN UVVis Spectrometry, Helios Gamma, the United
Kingdom) according to the Marquardt method [40]. The
nitrogen contained in uric acid is the 33.33%. The CP
amount in the excreta (CP corrected) was calculated using
the excreta CP, corrected for UA as follows:
CP corrected ¼total nitrogen UAnitrogenðÞ6:25:
The TiO
2
content was measured on a UV spectropho-
tometer (UNICAN UVvis Spectrometry, Helios
Gamma, the United Kingdom) following the Myers et al.
[41] method .
The ATTDC of the dietary nutrients was calculated
using the following method [42]:
ATTDC Xdiet ¼Total X ingestedtotal X excretedðÞ
total X ingested

Digestibility ¼%Xdiet =%TiOdiet
ðÞ%Xexcreta=%TiOexcreta
ðÞ
%Xdiet =%TiOdiet
ðÞ

where Xrepresents DM, CP, EE or OM.
Slaughtering procedures
At 50 days of age, the final LW of the birds was recorded
individually and 12 ducks per diet (two birds per pen)
were chosen on the basis of the LW pen average and
identified by means of a shank ring. Then the feed was
removed and, after 12 h of fasting (at 51 days of age), the
selected animals were transferred to a commercial abat-
toir and slaughtered by electrical stunning and bleeding,
according to the standard EU regulations. The plucked
and eviscerated carcasses were obtained, the head, neck
and feet were removed.
Histomorphological investigations
Gut segments (approximately 5 cm in length, 12 animals
per each group) of the duodenum, jejunum and ileum
were sampled during slaughtering and flushed with 0.9%
saline to remove all the contents. The collected intestine
segments were the loop of the duodenum, the tract be-
fore Meckels diverticulum (jejunum) and the tract be-
fore the ileocolic junction (ileum). The gut samples were
fixed in a 10% buffered formalin solution, routinely em-
bedded in paraffin wax blocks, sectioned at a 5-μm
thickness, mounted on glass slides and stained with
Haematoxylin & Eosin (HE) for morphometric analysis.
The evaluated morphometric indices were as follows: vil-
lus height (Vh, from the tip of the villus to the crypt),
crypt depth (Cd, from the base of the villus to the sub-
mucosa) and the villus height-to-crypt depth (Vh/Cd)
ratio [27]. Morphometric analyses were performed on 10
Gariglio et al. Journal of Animal Science and Biotechnology (2019) 10:37 Page 4 of 10
well-oriented and intact villi and 10 crypts chosen from
the duodenum, jejunum and ileum [26].
Statistical analysis
The statistical analyses were performed using the SPSS
software package (version 21 for Windows, SPSS Inc.,
Chicago, IL, USA). The mortality rate was analysed by
means of a Chi-square test, using the HI0 group as the
reference. Shapiro-Wilks test established normality or
non-normality of distribution. The assumption of equal
variances was assessed by means of Levenes homogen-
eity of variance test. The experimental unit was the pen
for growth performance and digestibility, while the duck
was used for the intestinal morphology. The collected
data were tested by means of one-way ANOVA. Polyno-
mial contrasts were used to test the linear and quadratic
responses to increases in the HI inclusion level in the
diet. Intestinal morphometric indices were analysed by
fitting a general linear mixed model (GLMM). GLMM
allowed the morphometric indices (Vh, Cd and Vh/Cd,
separately) to depend on three fixed factors (diet, intes-
tinal segment and interaction between diet and intestinal
segment). Animal was included as a random effect to ac-
count for repeated measurements in the same duck. The
interactions between the levels of the fixed factors were
evaluated by means of pairwise comparisons.
Differences among treatments were considered statisti-
cally significant when the Pvalues 0.05.
Results
Growth performance
The cumulative mortality rates of the HI0 (4.16%), HI3
(2.08%), HI6 (2.08%) and HI9 (2.08%) groups were not
influenced by the dietary treatments (P> 0.05). The
growth performances of the broiler ducks are summa-
rized in Table 2. Overall LW was not influenced by the
dietary treatments (P> 0.05), except at 38 days of age,
when a quadratic response was observed in LW for in-
creasing HI meal levels with a minimum being observed
for the HI6 group (P< 0.05).
ADG was not affected by the dietary treatments (P>0.05),
with the exception of the HI6 group in the second period
(1838 days of age), where the ADG showed a quadratic
response (P< 0.05). DFI and FCR were not affected by the
dietary treatment nor in the different feeding phases or
over the whole experimental trial (P>0.05).
Digestibility trial
The apparent digestibility coefficients are reported in
Table 3. DM digestibility was not affected by the dietary
treatment throughout the trial, as well as the OM
(P> 0.05). In the starter period (317 days of age) the CP
digestibility decreased linearly with a minimum
corresponding to the HI9 groups (P<0.05)(4.11%
compared to HI0, respectively), whereas the EE digestibil-
ity decreased linearly with the inclusion of HI in the diets
(P<0.05).
Table 2 Effect of the dietary HI larva meal inclusion on the growth performance of female ducks (n=6)
Items Age Dietary treatments
a
SEM P-value
HI0 HI3 HI6 HI9 Linear Quadratic
LW, g 3 d 70.70 70.41 72.65 71.51 0.60 0.405 0.733
17 d 575.44 567.31 572.56 575.74 4.76 0.893 0.582
38 d 1906.79 1861.96 1797.10 1900.12 14.18 0.426 0.005
50 d 2540.57 2511.14 2456.14 2554.84 20.13 0.946 0.123
ADG, g/d 317 d 36.05 35.49 35.71 36.02 0.32 0.974 0.529
1838 d 63.40 61.65 58.31 63.07 0.69 0.417 0.011
3950 d 52.81 54.10 54.92 54.56 1.14 0.582 0.738
350 d 52.55 51.93 50.71 52.84 0.43 0.926 0.125
DFI, g/d 317 d 53.69 53.45 52.16 51.85 0.59 0.226 0.979
1838 d 142.03 139.06 136.99 139.92 1.28 0.481 0.273
3950 d 167.48 170.82 160.32 171.80 2.83 0.924 0.485
350 d 120.58 121.32 117.58 121.48 1.20 0.927 0.530
FCR, g/g 317 d 1.49 1.51 1.46 1.44 0.01 0.099 0.489
1838 d 2.24 2.26 2.35 2.22 0.03 0.913 0.159
3950 d 3.17 3.17 2.93 3.18 0.051 0.639 0.220
350 d 2.29 2.34 2.32 2.30 0.019 0.925 0.406
HI Hermetia illucens,SEM standard error of the mean, LW live weight, ADG average daily gain, DFI daily feed intake, FCR feed conversion ratio
a
Four dietary treatments: HI0 = control; HI3 = 3% inclusio n level of Hermetia illucens; HI6 = 6% inclusion level of Hermetia illucens; HI9 = 9% inclusion level of
Hermetia illucens
Gariglio et al. Journal of Animal Science and Biotechnology (2019) 10:37 Page 5 of 10
In the periods from 18 to 38 days of age and from 39
to 50 days of age, the EE digestibility showed a linear in-
crease, with a maximum corresponding to the HI9 group
(P< 0.001) (+ 1.94% and + 3.05% compared to HI0 in the
grower and finisher periods, respectively). However, CP
digestibility was not affected by the dietary treatments in
the grower and finisher periods (P> 0.05).
Histomorphological investigations
The effects of the diet, gut segment and interaction be-
tween the diet and gut segment on the gut morphomet-
ric indices of the ducks are summarized in Table 4.The
intestinal segment significantly affected Vh, Cd and Vh/Cd
(P< 0.001). On the other hand, no influence of diet or inter-
action between the diet and intestinal segment (P> 0.05)
were observed on the morphometric indices. The
duodenum showed higher Vh and Cd values (P<0.05and
P< 0.01, respectively) than the ileum, and the morphomet-
ric indices were also greater (P<0.05 and P< 0.01, re-
spectively) in the jejunum than in the ileum. The
duodenum also showed a greater Vh/Cd (P< 0.05) than
the other gut segments.
Discussion
Growth performance
Currently, no literature is available regarding the use of in-
sect meals in duck feeding. For this reason, all the com-
parisons with literature data referred to other poultry
species fed with HI meals and other insect meals.
The final LW of the birds was in line with the weight
reported by Pingel et al. [29]. The results showed that
HI meal could be a valuable alternative to corn gluten
meal, and HI meal can be included in duck diets by as
much as 9% without any negative effects on the final
LW, ADG, DFI and FCR of the animals. Despite the
lower LW and ADG of HI6 birds in the grower period
(1838 days of age), DFI and FCR were not influenced
by the dietary treatment, and the final LW of the HI6
group was in line with the weight of the other treat-
ments. Similarly, Cullere et al. [10] did not observe any
differences in the final LW of broiler quails (Coturnix
coturnix japonica) fed two different diets at 10% and
15% of inclusion levels of HI meal (in substitution of
SBM protein and oil). Our results also agree with what
Bovera et al. [24] previously reported for laying hens fed
25% and 50% HI in substitution of SBM (73 g/kg and
146 g/kg of inclusion, respectively), thus showing that
LW and DFI were not influenced by the dietary treat-
ments. The inclusion of up to 10% of HI larva meal in
the diet of broiler chickens influenced their final LW
and also improved the DFI of chicks in the starter period
[12]. As far as other insect species with potential interest
as feeds are concerned, Adenjii [13] did not observe any
dietary effects on the performance of broiler chickens
when groundnut cake was substituted with housefly
maggot (M. domestica) meal. Biasato et al. [16],
Ramos-Elorduy et al. [43] and Bovera et al. [44] also re-
ported that the inclusion of TM meal in broiler chicken
diets (from 5% to 15% of inclusion) did not affect the
final LW and DFI of the birds. On the other hand, the
replacement of SBM with 25% and 50% of HI meal (100
and 190 g/kg of inclusion, respectively) and 25% TM
meal (120 g/kg of inclusion) in Barbary partridge (Alec-
toris barbara) resulted in a higher LW than the control
[45]. Finally, the results reported by Khan et al. [46], per-
taining to broiler chicks fed with silkworm (Bombyx
mori), housefly maggot and TM in substitution of SBM
Table 3 Effect of the dietary inclusion of HI larva meal on the nutrients apparent digestibility of Muscovy ducks (n=6)
Age Apparent
digestibility
Dietary treatments
a
SEM P-value
HI0 HI3 HI6 HI9 Linear Quadratic
317 d DM 0.960 0.960 0.960 0.953 0.002 0.174 0.315
CP 0.852 0.872 0.828 0.817 0.007 0.010 0.195
EE 0.945 0.967 0.963 0.962 0.002 0.003 0.085
OM 0.963 0.963 0.966 0.962 0.001 0.853 0.453
1838 d DM 0.953 0.956 0.962 0.960 0.002 0.086 0.511
CP 0.800 0.802 0.802 0.828 0.005 0.085 0.269
EE 0.958 0.966 0.968 0.977 0.002 < 0.001 0.891
OM 0.958 0.964 0.967 0.963 0.001 0.215 0.168
3950 d DM 0.943 0.948 0.952 0.953 0.002 0.099 0.703
CP 0.733 0.682 0.715 0.718 0.012 0.913 0.259
EE 0.953 0.958 0.965 0.983 0.003 < 0.001 0.092
OM 0.950 0.953 0.958 0.958 0.002 0.072 0.642
HI Hermetia illucens,SEM standard error of the mean, DM dry matter, CP crude protein, EE ether extract
a
Four dietary treatments: HI0= control; HI3 = 3% inclusion level of Hermetia illucens; HI6 = 6% inclusion level of Hermetia illucens; HI9 = 9% inclusion leve l of Hermetia illucens
Gariglio et al. Journal of Animal Science and Biotechnology (2019) 10:37 Page 6 of 10
(7.8%, 8.0% and 8.1% of inclusion, respectively), pointed
out a higher LW in insect-fed chicks than in the control.
In this trial, the FCR was not affected by the dietary
treatments, according to the results of Elwert et al. [47]
and Cullere et al. [10] pertaining to broiler chickens and
broiler quails, respectively, fed with increasing levels of
defatted HI meal. On the contrary, an improved FCR
was observed in Barbary partridge fed diets with 25%
and 50% of substitution of SBM with HI and TM meal
[45]. An improved FCR was also reported by Khan et al.
[46] (silkworm, housefly maggot, TM) and Bovera et al.
[44] (TM), who found that the FCR of broiler chickens
was lower in chicks fed insect meal than the control diet
with SBM.
TheuseofHIlarvamealasasubstitutetocorngluten
meal results to be suitable in Muscovy ducks feeding.
During the whole experimental period, the growth perfor-
mances observed in the present study were not influenced
by dietary inclusion levels of HI meal, as already observed
by other researches in quails and laying hens [10,24]. Fur-
thermore, the absence of gut histomorphological alterations
can also explain the growth performance results, as well as
the slightly affected nutrient digestibility.
Digestibility trial
The herein obtained results show that the inclusion of HI
larva meal in Muscovy duck diets partially affected the ap-
parent digestibility coefficients of the nutrients. Consist-
ently with our results, Cullere et al. [10]didnotreport
any differences in DM and OM total tract apparent digest-
ibility in broiler quails as a result of the HI inclusion level
in the diet. On the contrary, in laying hens fed 17% HI
meal in the diet, the apparent ileal digestibility of DM was
lower in the group fed HI meal than in the control [22].
Results reported by Bovera et al. [24] showed that the in-
clusion of HI meal by up to 7.3% in laying hen diets did
not affect the apparent DM ileal digestibility, compared to
the control with vegetable protein meal, whereas the in-
clusion of 14.6% reduced the apparent DM ileal digestibil-
ity. In another study, the use of TM in broiler chicken
diets worsened the apparent ileal DM digestibility com-
pared to the control with SBM [44].
In our trial, the CP and EE apparent digestibility in the
starter period (317 days of age) showed an opposite linear
trend, with a reduction in CP digestibility (up to 3.5% in
HI9, compared to the control) and an improvement in EE
digestibility (+ 2.0 in HI9, compared to the control) follow-
ing the increasing inclusion levels of HI meal in the diet.
The lower CP digestibility for the HI6 and HI9 groups in
the starter period could be related to the higher chitin con-
tent of the diet, because of the higher inclusion level of HI
meal [48]. In fact, Cutrignelli et al. [22] and Bovera et al.
[24] also observed a reduction in the apparent ileal CP di-
gestibility of laying hens compared to the control diet with
SBM, and explained this result as a consequence of the
presence of chitin in the diet. Indeed, De Marco et al. [9]
assumed that the chitin, the structural component of the
exoskeleton of insects, can negatively affect the nutrient di-
gestibility, resulting as an indigestible fiber for domestic
poultry. However, no differences in CP total tract apparent
digestibility were reported by Cullere et al. [10] for broiler
quails, after a substitution of protein/fat sources with HI
larva meal of up to 15% of inclusion. However, in our trial,
the apparent CP digestibility was similar during the grower
(1838 days of age) and finisher (3950 days of age) pe-
riods, thus suggesting an adaptation to the chitin levels in
the diet. The studies conducted by Tabata et al. [49,50]
showed that the birds have acid chitinase genes in their
genome. In particular, in poultry (such as ducks), the acid
chitinase is expressed mainly at the level of the glandular
stomach. The level of acid chitinase mRNA in stomach tis-
sue is regulated by feeding behaviour, which was higher in
omnivorous species than in herbivorous and carnivorous
species [50]. Moreover, it could be speculated that the chi-
tin level in the diet could influence the acid chitinase ex-
pression with an overall improvement in feed digestibility.
In our trial, the EE apparent digestibility was higher in
HI groups than the control group. However, despite this
positive result, the EE apparent digestibility was only 2.2%
and 1.9% higher than the control in the starter and grower
periods respectively (317 and 1838 days of age) and
3.0% higher than the control in the finisher period (3950
days of age). This result partially agrees with the results of
Cullere et al. [10], who found that the EE total tract
Table 4 Intestinal morphometric indices in the ducks in relation to diet and intestinal segment (n= 12, end of the trial)
Index Diet (D)
d
Intestinal segment (IS)
e
SEM P-value
HI0 HI3 HI6 HI9 DU JE IL D IS D IS D × IS
Vh, mm 1.55 1.51 1.52 1.63 2.12
a
1.41
b
1.14
c
0.06 0.06 0.442 < 0.001 0.508
Cd, mm 0.16 0.14 0.15 0.15 0.18
a
0.15
b
0.13
c
0.01 0.01 0.346 < 0.001 0.782
Vh/Cd 9.80 11.06 10.67 10.83 12.62
a
9.67
b
9.48
b
0.60 0.45 0.469 < 0.001 0.966
Vh villus height, Cd crypt depth, Vh/Cd villus height-to-crypt depth ratio
The means with different superscript letters (
a, b, c
) within the same row per fixed effect (i.e. diet, intestinal segment) differ significantly (P< 0.05)
d
Four dietary treatments: HI0 = control; H I3= 3% inclu sion level of Hermetia illucens; HI6 = 6% inclusion level of Hermetia illucens; HI9 = 9% inclusion level of Hermetia illucens
e
Three intestinal segments: DU duodenum, JE jejunum, IL ileum
Gariglio et al. Journal of Animal Science and Biotechnology (2019) 10:37 Page 7 of 10
apparent digestibility in broiler quails fed with a 15% in-
clusion level of HI was higher than a 10% group, but simi-
lar to the control diet. On the other hand, Cutrignelli et al.
[22] and Bovera et al. [24] found that the apparent ileal EE
digestibility in laying hens was similar for HI meal- and
SBM-fed birds. The linear increase in EE digestibility is
not supported by the fatty acids profile, in particular by
the polyunsaturated fatty acids (PUFA) content, that is
usually related to an EE digestibility improvement [51]. In-
deed, in the present study the dietary PUFA content, as
well as the ratio polyunsaturated fatty acids/saturated fatty
acids (PUFA/SFA ratio), decreased following the HI larva
meal inclusion (Table 1). The highest EE digestibility at
the maximum inclusion level (HI9 group) could be related
to the overall amount of EE in the diets (+7.84%, + 6.06%
and + 5.19% higher in HI9 group than HI0 group in
starter, grower and finisher periods, respectively) [52].
As a whole, the absent or moderate effects on nutrient
ATTDC had no impact on the ducksgrowth perfor-
mances, without affecting final LW, ADG, DFI and FCR.
Histomorphological investigations
Dietary HI meal inclusion did not affect the gut morph-
ology of the ducks of our study. Since the rapid growth
of chickens has been reported to strictly depend on the
morphological and functional integrity of the digestive
tract [25], it is reasonable to hypothesize that insect meal
utilization does not negatively influence gut develop-
ment and, as a consequence, animal performance. The
greater mucosal development observed in the duodenum
than in the other gut segments is also in agreement with
the previous studies available on broilers [11,1417,53,
54], thus suggesting that insect meal utilization leads to
the preservation of the physiological intestinal morph-
ology. Indeed, the duodenum is the intestinal tract that
undergoes the fastest cell renewal, and is also the first
gut segment to receive the physical, chemical and hor-
monal stimuli caused by the presence of the diet in the
lumen [54]. The obtained results about the preservation
of gut histomorphology in all dietary groups contributes
to validate what has been previously discussed in terms
of nutrient digestibility and growth performances.
Conclusions
To the best of the authorsknowledge, this is the first
study that has evaluated the possibility of including in-
sect meal in duck nutrition, and to have demonstrated
how HI larva meal can be a valuable protein sources for
ducks. Increasing inclusion levels of a partially defatted
HI meal in Muscovy duck diets did not affect the growth
performances of the birds, which showed similar LW,
ADG, DFI and FCR to the control group fed with corn
gluten meal, and only had weak effects on the apparent
total tract digestibility during the first stages of growth.
Moreover, these increasing levels did not affect the intes-
tinal morphology or cause histopathological alterations.
From this preliminary investigation, it appears that HI
larva meal can be included in duck feeding at levels of
up to 9% of the diet, with no negative effects on growth,
digestibility or animal health. Furthermore, the obtained
results help to expand the information available about
the use of insects in poultry nutrition.
Abbreviations
ADF: Acid detergent fibre; ADG: Average daily gain; AMEn: Apparent
metabolisable energy; ATTDC: Apparent total tract digestibility coefficients;
Cd: Crypt depth; CP: Crude protein; DFI: Average daily feed intake; DM: Dry
matter; DU: Duodenum; EE: Ether extract; FAME: Fatty acid methyl esters;
FCR: Feed conversion ratio; GLMM: General linear mixed model;
HE: Haematoxylin & Eosin; HI: Hermetia illucens; IL: Ileum; JE: Jejunum;
LW: Live weight; MUFA: Monounsaturated fatty acids; NDF: Neutral detergent
fiber; OM: Organic matter; PAS: Periodic acid-Schiff; PUFA: Polyunsaturated
fatty acids; SB: Sudan Black; SBM: Soybean meal; SEM: Standard error of the
mean; SFA: Saturated fatty acids; TM: Tenebrio molitor; Vh: Villus height; Vh/
Cd: Villus height-to-crypt depth ratio
Acknowledgements
The authors would like to thank Mr. Heinrich Katz, the owner of Hermetia
Baruth GmbH, Baruth/Mark (Germany), for providing the black soldier fly
meal and A.I.A. Agricola Italiana Alimentare S.p.A (Fossano, CN, Italy) for
providing the feed ingredients. The authors are also grateful to Mr. Dario
Sola and Mr. Mario Colombano for the bird care and technical support.
Funding
Research supported by the University of Torino (Italy) funding: SCHA_RILO_16_02.
Availability of data and materials
The datasets analysed in the current study are available from the corresponding
author on request.
Authorscontributions
MG, SD, FG, LG and AS conceived and designed the experiment. MG, SD, LG,
FG, CC, SBO, VR and AS prepared the diets, performed the trial and collected
the experimental data. MG, SD, FH, JM and SM performed the digestibility
determinations. IB, MTC and EC performed the morphometric investigations.
AT established the fatty acids profile. MG, SD, IB and MM performed the
statistical analysis. LG, FG, AS, MG, SD, AT analyzed and interpreted the data.
LG, MG, SD, IB, AS, FG and AT wrote the first draft of the manuscript. All the
authors critically reviewed the intellectual content of the manuscript and
gave their approval for the final version to be published.
Ethics approval and consent to participate
The experimental protocol was approved by the Bioethical Committee of the
University of Turin (Italy) (protocol number: 380576, 04/12/2017).
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Author details
1
Department of Veterinary Sciences, University of Turin, largo Paolo Braccini
2, Turin, Grugliasco 10095, Italy.
2
Department of Agricultural, Forest and Food
Sciences, University of Turin, largo Paolo Braccini 2, Turin, Grugliasco 10095,
Italy.
3
Department of Animal Production, University of Murcia, Campus de
Espinardo, 30071 Murcia, Spain.
4
Institute of Science of Food Production,
National Research Council, largo Paolo Braccini 2, Turin, Grugliasco 10095,
Italy.
5
Department of Comparative Biomedicine and Food Science, University
of Padua, viale dellUniversità 16, Padua, Legnaro 35020, Italy.
6
A.I.A. Agricola
Italiana Alimentare S.p.A, via Val Pantena 18G, 37142 Verona, Italy.
7
Institute
of Interdisciplinary Research on Sustainability, University of Turin, via
Accademia Albertina 13, 10100 Turin, Italy.
Gariglio et al. Journal of Animal Science and Biotechnology (2019) 10:37 Page 8 of 10
Received: 19 December 2018 Accepted: 15 March 2019
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Gariglio et al. Journal of Animal Science and Biotechnology (2019) 10:37 Page 10 of 10
... Likewise, the protein digestibility coefficient in rats fed diets supplemented with dried Tenebrio Molitor larvae was 75.1% (Goulet et al., 1978). Additionally, Gariglio et al. (2019) showed that the EE apparent digestibility was better in defatted black soldier fly larva meal groups of ducks than in the control group, which agrees with the current findings. Furthermore, Ahmed et al. (2021) found that using edible insects at 25% of SBM enhanced nutrient degradability significantly. ...
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The current study aims to determine the effect of partial substitution of soybean meal (SBM) with Vespa Oriental meal (VOM) [(0%, VOM 0), 25% (VOM 25), and 50% (VOM 50)] in the diets of thirty 12-week-old V-line male rabbits with an average body weight of 1.060±0.01kg on growth performance, digestion, and some blood biochemical changes. The experiment lasted for 90 days. The results revealed that the crude protein (CP) contents of VOM and SBM used in the present study were 76.84 and 43.76 %, respectively, Furthermore, the digestibility of CP (74.65 % & 76.07 %,) and nitrogen-free extract (NFE) (68.390 & 70.123 %,) was considerably higher in rabbits fed VOM 25 and VOM 50, respectively than in rabbits fed VOM 0 (72.033 % & 65.44 %). The daily body gain in rabbits fed the VOM 50 diet was 9.18 %, higher than in rabbits on the VOM 0 diet. Also, the VOM 25 and VOM 50 diet-fed rabbits had considerably larger carcass weight, liver, kidney, and cecum length than the control group. Total volatile fatty acids were significantly higher in the caecal contents of VOM 25 and VOM 50 rabbits, despite lower caecal Ammonia-N concentration compared to the control diet. Hematological parameters live and renal functions of rabbits fed the VOM 50 diet were considerably improved compared to those fed the control diet. The VOM 25 and VOM 50 groups exhibited better TDN and DCP values (P < 0.05) than the control group in terms of nutritional value. It is concluded that Vespa Orientalis wasp meal can be used as an effective alternative high-quality protein source to soybean meal, up to 50%, with no adverse impacts on rabbits' performance.
... The black soldier fly larva (BSFL; Hermetia illucens) is one of the insect species widely used globally as feed because of its rich nutritional profile. Studies have shown that black soldier fly larvae meal (BSFLM) can replace 25 to 100% of fish or soybean meals in broiler chicken, quails and barberry partridge feed and ensure optimal health status, satisfactory growth performance and overall meat quality (Cullere et al., 2016Dabbou et al., 2018;Gariglio et al., 2019;Makkar et al., 2014;Secci et al., 2018). However, the amino acid profile of the BSFL is highly variable (Liland et al., 2017;Makkar et al., 2014). ...
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We evaluated the effect of dietary inclusion of different ratios of Desmodium intortum (DI) and black soldier fly larvae meal (BSFLM) on sensory traits and physicochemical qualities of broiler chicks meat. Three formulations: T1:75%BSFL:25%DI; T2:50%BSFL:50DI, and T3:25BSFL:75% DI as a protein source were tested. A conventional feed was used as the control diet. On day 42, the chickens were slaughtered, and thigh muscles were used for sensory and physicochemical evaluations. T1 was preferred for its flavour and tenderness, T2 for its juiciness and T3 for its colour, flavour, taste and overall acceptability scores. In terms of physical properties, all three types of meat had significantly lower moisture content and a higher water holding capacity than the control. T3 had the lowest moisture content, cooking loss and pH, whereas the meat from control diet had the highest cooking loss and pH. No significant differences were found in terms of meat lightness; however, meat from control diet showed the highest redness value, and T3 had the highest yellowness value. Dietary inclusion of DI-BSFL affected the fatty acid and cholesterol profiles of the meats. A holistic Principal Component Analysis indicated that the tested meats were distinct in their sensory and physicochemical properties. These variations in physicochemical properties may account for the difference in organoleptic perception, especially for T3. Further research should focus on feed modulation in relation to consumers’ preference and potential health benefits.
... Moreover, BSF, being neither a non-vector nor a pest, is easy to culture in simple structures. In addition, it is known to reduce the presence of harmful bacteria from the food substrates (Erickson et al., 2004;Liu et al., 2008) and has a prebiotic effect on the fish (Gariglio et al., 2019). Successful dietary inclusion of BSF larvae in fish diets has shown improved fish yields and reduced production cost, thus promoting profitability and resource utilization. ...
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Aquaculture plays a major role in curbing malnutrition and food insecurity. Nonetheless, aquaculture sustainability is threatened by expensive fish feeds due to the overreliance on fish meal (FM) as the main source of protein. Fish meal is not only expensive but also scarce due to declining capture fisheries and competition from other animal feed producers. This has prompted research on potential FM replacers, amongst them the black soldier fly (BSF) larvae (Hermetia illucens). The BSF larvae can effectively convert organic wastes into a potential valuable feed source, and its high nutritional content (crude protein of up to 64% dry matter) is vital for fish feed formulation. Nevertheless, there are no documented studies on the complete replacement of FM in the diets of fish using BSF larvae. Therefore, the current study reviewed 107 research publications related to BSF larvae vis-a-visfish feeds production to build capacity for existing theories, identify gaps, and suggest new and further research directions, based on the previous studies available in the area of larvae production and utilization in aquaculture nutrition. The study results are expected to help farmers make an informed decision on how to reduce the cost of fish production, increase yields, thus promoting food security, livelihoods, and ecological balance.
... Poultry production is one of the most important industries, and due to its accelerated growth, it contributes to the economic development of several countries (Windhorst 2006). This industry is dominated by chicken farming, but duck farming is also economically valuable, contributing to food security (Gariglio et al. 2019). It has grown in recent years (1998 to 2018), going from 2.6 to 4.5 million tons of meat per year (FAOSTAT 2020). ...
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Proper health management is essential for productivity in duck farming. However, there is limited information on the effect of management conditions on rates of metabolic problems and parasitic infections in anatids. We evaluated the rates of metabolic syndromes and gastrointestinal parasite involvement in Muscovy ducks up to 12 weeks of age, under 3 management conditions: backyard, organized, and organized with probiotics. Individuals under organized management developed 2 metabolic problems: ascites, which was rare (3.5%), fatal, and affected both males and females, and angel wing syndrome, which was more frequent (10.6%), has low impact on general health, and only affected males. The treatments do not have a significant effect on the development of ascites, but only individuals in controlled conditions presented this syndrome, and due to its low prevalence, further studies with a larger sample size are required. The risk of angel wing syndrome increased significantly with probiotic supplementation. Regarding to parasitic infection, the improvement of sanitary management and the use of probiotics supplementation reduced the occurrence of coccidiosis. Similarly organized management with probiotic supplementation showed a protective effect on helminthiasis by reducing the frequency of Heterakis gallinarum and greatly reducing the helminth egg load. Coccidiosis and helminthiasis infections were not significantly correlated with the final weight of the ducks. Therefore, organized management and the use of probiotics seems to reduce the impact of parasitic infection, although it increases the risk of developing metabolic syndrome.
... In particular, T. molitor and H. illucens have been demonstrated to be a valid alternative to common fishmeal for salmon, seabass and trout, when included until 50% in feed formula (Belghit et al., 2019;Dumas, Raggi, Barkhouse, Lewis, & Weltzien, 2018;Gasco et al., 2016;Magalhães et al., 2017;Renna et al., 2017). Furthermore, these insect species have been demonstrated suitable also for broiler chickens, quails, ducks (Woods et al., 2019;Gariglio et al., 2019), pigs, and rabbits (Adeniji, 2008;Martins et al., 2018). Insects can be employed for feed purposes whole, or as processed products in ground and paste forms, or other less recognizable forms (e.g., extracts of protein, fat) (Sun-Waterhouse et al., 2016). ...
Chapter
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Chapter
Insects have application in poultry feed because of their capacity to sustainably repurpose wastes into nutrient-dense feeds, combined with the demand for poultry meat and eggs in the diets of the growing human population. Additionally, poultry naturally consumes insects, thus insects may enhance poultry welfare. Several insects are commercially reared including the house cricket (Acheta domesticus L.), yellow mealworm (Tenebrio molitor L.), and black soldier fly larvae (Hermetia illucens L.). Insect nutrient concentrations are affected by species, stage of development, feedstock on which they are raised, and processing method. Insects are a concentrated source of energy and protein with an excellent balance of essential amino acids, of which methionine levels are higher than standard corn and soybean meal sources commonly utilized in poultry diets. Because they are readily eaten and well utilized by poultry, insects are an effective source of nutrition in poultry feed for a burgeoning world population.
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This study investigated the effect of replacing soybean meal (SBM) with black soldier fly larvae meal (BSFLM) on the growth performance, feed utilization, carcass body composition, and amino ac-ids profile of Nile tilapia (Oreochromis niloticus). Three isonitrogenous (30% crude protein) diets containing BSFLM in varying proportions of 0% (BSFLM0), 50% (BSFLM50), and 100% (BSFLM100), were formulated to replace SBM. A commercial diet (COMM0) sourced from the local market was used as a positive control. Male sex-reversed O. niloticus juveniles of a mean weight 20.88 ±0.16 g were stocked in 12 cages each at a density of 12.5 fish m-3. Fish were hand-fed at 5% (28 days), 3% (54 days), and 2.5% (84 days) of the body weight twice a day (1000 hrs and 1600 hrs). Significant differences (P < 0.05) were found in the final body weight, body weight gain (BWG), specific growth rate (SGR), feed conversion ratio (FCR), survival rate, and condition factor (K). The best growth performance and feed utilization was recorded in fish fed on BSFLM100. The different diets had significant effects on the body composition and amino acid pro-files of the experimental fish (P<0.05). Fish fed on BSFLM100 exhibited highest values for phenylal-anine, threonine, Isoleucine, lysine, proline, and glutamic acid amino acids. The partial enterprise budget analysis indicated that replacing SBM with BSFLM at 50% and 100% reduced the cost of production compared to the control diet (BSFLM0) and commercial diet (COMM0). The study demonstrated that BSFLM is a cost-effective alternative to SBM in the diets of Oreochromis nilot-icus hence can replace soybean meal up to 100% without negative effect on growth and carcass body composition
Chapter
Globally, the utilization of alternative protein sources in livestock feed has been extensively deliberated and established to be the best novel approach. Extensive research indicated that insects provide good opportunities as a sustainable, high quality, and low-cost component of animal feed. The use of insects in animal diet sounds to be the prospective opportunity leading to sustainability of animal feeds and meet the intensifying worldwide plea for livestock products. The value of these protein sources has, however, increased due to limited production, competition between humans and animals. The use of insects for feeding farmed animals represents a promising alternative because of the nutritional properties of insects and the possible environmental benefits, given the sustainability of this type of farming. Yet little has been documented about the nutrient composition of various insect meals, the impact of insect meal in the animal feed industry, safety, and attitude and willingness of farmers to accept insect-based animal feed and food. Therefore, this chapter seeks to document the potential utilization of insect meal as livestock feed.
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The opportunity to use insects as protein sources for poultry has many environmental advantages. Moreover, the administration of insects to poultry can provide animal welfare and health benefits, allowing the expression of their natural behaviour, reducing aggression, and supplying nutrients. However, there is limited research on consumer’s acceptance of farmed animals fed with insects. Our study aims to understand consumers’ attitude towards, intention to purchase, and willingness to pay (WTP) for meat obtained from a farmed duck fed on: (1) an insect-based meal; and (2) live insect diet. We conduct an online survey of 565 Italian meat consumers, including an information treatment regarding the sustainability and nutrition benefits of using insects as feed. Our results demonstrate that providing more information about the positive effects of using insects in feed production may motivate those more interested in environmental issues to purchase insect-fed duck meat products. Compared to the control group, the purchase intention of consumers in the treatment group is also affected by their attitude towards animal welfare. Their WTP for such products is directly affected by their previous entomophagy experience. Attitude and intention to purchase an insect-fed duck are the main predictors of consumers’ WTP for a duck fed with both insect-meal and live insects. This study provides insights for policymakers and the private sector. We suggest that increasing consumers’ awareness by communicating the positive environmental impact of the use of insect as feed can potentially differentiate meat products for consumers and influence their purchase preferences.
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Background The present work aimed at evaluating the effect of the dietary replacement of soybean oil (S) by two types of insect fats extracted from black soldier fly larvae (H, Hermetia illucens L.) and yellow mealworm larvae (T, Tenebrio molitor L.) on growth performance, nutrient digestibility, blood parameters, intestinal morphology and health of growing rabbits. Methods At weaning, 200 crossbred rabbits (36 days old) were allotted to five dietary treatments (40 rabbits/group): a control diet (C) containing 1.5% of soybean oil and four experimental diets where soybean oil was partially (50%) or totally (100%) substituted by H (H50 and H100) or T (T50 and T100) fats. Total tract digestibility was evaluated on 12 rabbits per treatment. The growth trial lasted 41 d and, at slaughtering (78 days old), blood samples were collected from 15 rabbits per treatment, morphometric analyses were performed on duodenum, jejunum and ileum mucosa, and samples of liver, spleen and kidney were submitted to histological evaluation. Results No difference was observed between the control and the experimental groups fed insect fats in terms of performance, morbidity, mortality and blood variables. The addition of H and T fats did not influence apparent digestibility coefficients of dry matter, protein, ether extract, fibre fractions and gross energy. Gut morphometric indices and organ histopathology were not affected by dietary inclusion of H and T fats. Conclusions H and T fats are suitable sources of lipid in rabbit diets to replace soybean oil without any detrimental effect on growth performance, apparent digestibility, gut mucosa traits and health. Electronic supplementary material The online version of this article (10.1186/s40104-018-0309-2) contains supplementary material, which is available to authorized users.
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The feed utilisation of young chicks is characterised by a suboptimal fat digestibility, which can be improved by means of dietary emulsifiers. The objective of this study was to evaluate the effect of dietary Globin on the energy efficiency and digestibility of starter feeds and on the production performance of broilers throughout the whole rearing cycle. A total of 224-day-old ROSS 708 chickens (14 birds/pen, 8 replicates/treatment) were fed ad libitum with either a basal diet (C) or a basal diet with the addition of 0.05% Globin during the starter (d1–10), growing (d10–25) and finisher (d25–35) periods. Nutrient digestibility (aD), protein metabolisability (aMCP), energy efficiency (EE) and net energy for production (NEp) were assessed during the starter period. The average daily feed intake (ADFI), average daily gain (ADG), feed conversion ratio (FCR) and protein efficiency ratio (PER) were measured of each growth period. Globin significantly decreased FCR (p = .020) and increased aDfat (p = .021), EE (p = .028) and NEp (p = .011) during the starter period. aMCP (p = .049) and PER (p = .039) were higher in the Globin group than in the Control group. The increased availability of energy from dietary fat, as a result of Globin supplementation, possibly shifted the use of the absorbed amino acids towards an anabolic metabolism, and this could explain the increased aMCP and PER but similar aDCP. The overall performance was similar between groups, although Globin tended to increase PER (p = .064) overall. • Highlights • Globin dietary supplementation was studied in broiler chickens. • Globin improved digestibility and nutrient efficiency utilization in the first period. • The overall performance was similar between groups.
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Background Gut health in poultry depends on the balance between the host, intestinal microbiota, intestinal microscopic features and diet. The effects of insect meal (a promising alternative protein source for poultry feed) on chicken gut morphology have recently been reported, but no data about intestinal microbiota and mucin composition modulation are available. The present study evaluated the effects of dietary Tenebrio molitor (TM) meal inclusion on gut health of free-range chickens by intestinal microbiota, morphology and mucin composition characterization. Results One hundred forty female medium-growing hybrids were divided into 2 dietary treatments (control feed [C] and 7.5% TM inclusion, with 5 replicate pens/treatment and 14 birds/pen) and slaughtered at 97 days of age (2 birds/pen for a total of 10 chickens/diet). The gut microbiota assessment on cecal content samples by 16S rRNA amplicon based sequencing showed higher alpha (Shannon, P < 0.05) and beta (Adonis and ANOSIM, P < 0.001) diversity in birds fed TM diet than C. In comparison with C group, TM birds displayed significant increase and decrease, respectively, of the relative abundances of Firmicutes and Bacteroidetes phyla, with higher Firmicutes:Bacteroidetes ratios (False Discovery Rate [FDR] < 0.05). The relative abundance of Clostridium, Oscillospira, Ruminococcus, Coprococcus and Sutterella genera was higher in TM chickens than C (FDR < 0.05). On the contrary, TM birds displayed significant decrease of the relative abundance of Bacteroides genus compared to the C group (FDR < 0.05). Gut morphology evaluation by morphometric analysis on small intestine revealed similar villus height, crypt depth and villus height to crypt depth ratio between C and TM birds. Characterization of gut mucin composition by periodic-acid Schiff, Alcian Blue pH 2.5 and high iron diamine staining on small and large intestine showed unaffected mucin staining intensity in TM chickens when compared to C group. Conclusions Dietary TM meal inclusion may positively modulate the gut microbiota of the free-range chickens without influencing the intestinal morphology and mucin composition. Since the rapid growth of chickens directly depends on morphological and functional integrity of the digestive tract, the gut health assessment by a post mortem multidisciplinary approach appears to be fundamental. Electronic supplementary material The online version of this article (10.1186/s12917-018-1690-y) contains supplementary material, which is available to authorized users.
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Background The present study has evaluated the effects of different inclusion levels of a partially defatted black soldier fly (Hermetia illucens L.; HI) larva meal on the growth performance, blood parameters and gut morphology of broiler chickens. A total of 256 male broiler chickens (Ross 308) were reared from d 1 to d 35 and assigned to 4 dietary treatments (8 replicates/treatment and 8 birds/replicate). HI larva meal was included at increasing levels (0, 5%, 10% and 15%; HI0, HI5, HI10 and HI15, respectively) in isonitrogenous and isoenergetic diets formulated for 3 feeding phases: starter (1–10 d), growing (10–24 d) and finisher (24–35 d). Two birds per pen were slaughtered at d 35 and morphometric investigations and histopathological alterations were performed. Results The live weight (LW) showed linear and quadratic responses to increasing HI larva meal (maximum for HI10 group). Average daily gain (ADG) showed a linear and quadratic responses to HI meal (maximum for HI10 group) during starter and growing periods. A linear decrease was observed for ADG during the finisher period. The daily feed intake (DFI) showed a linear and quadratic effect during the starter period (maximum for HI10 group). Linear and quadratic responses were observed for the feed conversion ratio (FCR) in the growing period and for the whole period of the experiment. The FCR showed a linear response in the finisher period (maximum for HI15). No significant effects were observed for the blood and serum parameters, except for the phosphorus concentration, which showed linear and quadratic responses as well as glutathione peroxidase (GPx) activity, the latter of which showed a linear response. The HI15 birds showed a lower villus height, a higher crypt depth and a lower villus height-to-crypt depth ratio than the other groups. Conclusions Increasing levels of dietary HI meal inclusion in male broiler chickens may improve the LW and DFI during the starter period, but may also negatively affect the FCR and gut morphology, thus suggesting that low levels may be more suitable. However, no significant effects on the haematochemical parameters or histological findings were observed in relation to HI meal utilization.
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Work was undertaken to investigate the potential use of housefly (Musca domestica) larvae reared on broiler manure as a source of nutrition for poultry production in the United Kingdom. Nutritional analysis showed that larvae have a high (>45% dry wt.) protein content and a favorable amino acid profile that is rich in key amino acids, such as lysine and methionine. A broiler digestibility trial was carried out to determine the apparent ileal digestibility coefficients (AIDC) and true ileal digestibility coefficients (TIDC) of amino acids (AA) from insect larval meal (ILM) from M. domestica and fishmeal (FM) in broiler chickens. This was calculated using multiple linear regression technique based upon 3 inclusions of each protein source in a semisynthetic diet. One-hundred-forty-four day-old male (Ross 308) broilers were fed from hatch on a commercial starter diet for 20 days. Experimental diets were fed from d 21 to 28, and feed intakes were measured daily. On d 28, the trial was terminated, ileal digesta were collected for the determination of AIDC and TIDC of AA, and inflammatory responses (gizzard erosion and eye discharge) were measured. No significant differences were observed in digestibilities between protein sources for any AA. Furthermore, ILM feeding did not induce gizzard erosion or eye discharge at any inclusion. These results provide strong evidence to suggest that ILM of the common housefly can provide a successful alternative protein source to FM in broiler diets.
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Chitin, a polymer of N-acetyl-D-glucosamine (GlcNAc), functions as a major structural component in chitin-containing organism including crustaceans, insects and fungi. Recently, we reported that acidic chitinase (Chia) is highly expressed in mouse, chicken and pig stomach tissues and that it can digest chitin in the respective gastrointestinal tracts (GIT). In this study, we focus on major livestock and domestic animals and show that the levels of Chia mRNA in their stomach tissues are governed by the feeding behavior. Chia mRNA levels were significantly lower in the bovine (herbivores) and dog (carnivores) stomach than those in mouse, pig and chicken (omnivores). Consistent with the mRNA levels, Chia protein was very low in bovine stomach. In addition, the chitinolytic activity of E. coli-expressed bovine and dog Chia enzymes were moderately but significantly lower compared with those of the omnivorous Chia enzymes. Recombinant bovine and dog Chia enzymes can degrade chitin substrates under the artificial GIT conditions. Furthermore, genomes of some herbivorous animals such as rabbit and guinea pig do not contain functional Chia genes. These results indicate that feeding behavior affects Chia expression levels as well as chitinolytic activity of the enzyme, and determines chitin digestibility in the particular animals.
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The objective of the present study was to evaluate the effects of partial or total replacement of finisher diet soybean oil with black soldier fly ( Hermethia illucens L.; HI) larva fat on the growth performance, carcass traits, blood parameters, intestinal morphology and histological features of broiler chickens. At 21 days of age, a total of 120 male broiler chickens (Ross 308) were randomly allocated to three experimental groups (five replicates and eight birds/pen). To a basal control diet (C; 68.7 g/kg as fed of soybean oil), either 50% or 100% of the soybean oil was replaced with HI larva fat (HI50 and HI100 group, respectively). Growth performance was evaluated throughout the trial. At day 48, 15 birds (three birds/pen) per group were slaughtered at a commercial abattoir. Carcass yield and proportions of carcass elements were recorded. Blood samples were taken from each slaughtered chicken for haematochemical index determination. Morphometric analyses were performed on the duodenum, jejunum and ileum. Samples of liver, spleen, thymus, bursa of fabricius, kidney and heart were submitted to histological investigations. Growth performance, carcass traits, haematochemical parameters and gut morphometric indexes were not influenced by the dietary inclusion of HI larva fat. Histopathological alterations developed in the spleen, thymus, bursa of fabricius and liver and were identified in all of the experimental groups, but HI larva fat inclusion did not significantly affect ( P >0.05) the severity of the histopathological findings. The present study suggests that 50% or 100% replacement of soybean oil with HI larva fat in broiler chickens diets has no adverse effects on growth performance or blood parameters and had no beneficial effect on gut health.
Article
Given probable the increment in the nutritional needs of both humans and animals, animal production will have increased dramatically by 2050. Insect meals could be an alternative protein source for livestock, and they would also be able to reduce the environmental problems related to intensive animal production system. The aim of this study was to evaluate productive performance, blood analysis, nutrient digestibility, and changes in the internal organs of laying hens fed Hermetia illucens larvae meal (HI) at two different levels in substitution (25 or 50%) of soybean meal (SBM). A total of 162 Hy-line Brown hens (sixteen weeks old) were equally divided into three experimental groups and fed isoprotein and isoenergetic diets. Egg weight, feed intake, and feed conversion rate were not affected by the soybean meal substitution at both inclusion levels of insect meal. Egg mass was positively affected by the insect meal diets, as was the lay percentage, although only at the lowest inclusion level. Dry matter, organic matter, and crude protein digestibility coefficients were lower for the HI50 diet, probably due to the negative effect of chitin. A reduction in serum cholesterol and triglycerides was observed in both insect-meal fed groups, while serum globulin level increased only at the highest level of insect meal inclusion, and, consequently, the albumin to globulin ratio decreased. Overall, a protein replacement of 25% with an insect meal from Hermetia illucens larvae in the diet of laying hens seems to be more suitable and closer to the optimal level.
Article
This research investigated the ileum morphometry and enzymatic activity, the caecal volatile fatty acid production and the apparent nutrient digestibility in laying hens fed a Hermetia illucens larvae meal (HILM) as a complete replacement of diet soybean meal (SBM). The hens fed HILM exhibited a lower live weight (P<0.05) and a higher incidence of the full digestive tract (P<0.05) than the SBM group. In the duodenum, the maltase exhibited a higher (P<0.05) activity in the HILM group while the intestinal alkaline phosphatase (IAP) had a higher (P<0.05) activity in the SBM group. In the ileum, the maltase and saccarase had a higher activity in the HILM hens (P≤0.01) while the IAP and ɤ glutamil transferase had a higher activity in the SBM group (P<0.05 and P<0.01, respectively). The HILM group showed a higher (P<0.05) villi height in the duodenum, while the opposite happened in the jejunum and the ileum. Only in the ileum the crypt depth resulted higher (P<0.05) in the HIML group than in the SBM. The higher production of acetate (P<0.05) and butyrate (P<0.01) affected the total production of volatile fatty acids of the HILM group. The coefficient of apparent digestibility of dry and organic matter as well as of crude protein was higher (P<0.05) in SBM group. The total replacement of SBM with HILM in laying hens diet from 24 to 45weeks of age resulted in a higher caecal production of butyric acid while the enzymatic activities of brush border membrane were partially reduced.