Aquaculture 422423 (2014) 193201

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Aquaculture
journal homepage: www.elsevier.com/locate/aqua-online

The potential of various insect species for use as food for sh

Fernando G. Barroso a,, Carolina de Haro a, Mara-Jos Snchez-Muros a, Elena Venegas b,
Anabel Martnez-Snchez c, Celeste Prez-Ban c
a
b
c

Department of Applied Biology, University of Almera, Almera, Spain

Food Technology Division, University of Almera, Almera, Spain
Instituto Universitario CIBIO, University of Alicante, Alicante, Spain

a r t i c l e

i n f o

Article history:
Received 18 June 2013
Received in revised form 11 December 2013
Accepted 12 December 2013
Available online 22 December 2013
Keywords:
Fish nutrition
Alternative feed
Insects meal
Fish meal
Amino acids
Fatty acid

a b s t r a c t
Due to the expansion of aquaculture and the limited resources available from the sea, it is necessary to nd
substitutes for sh meal for use in aquaculture. We believe that the use of insect meals as an alternative source
of animal protein may be an option. To use insects for this purpose, it is necessary to determine the nutritive
characteristics of these insects. To determinate the potential of insects as a substitute for sh meal in sh food
used in aquaculture, we examined 16 different species, 5 of them as different stage of development, of the orders
Coleoptera (4), Diptera (7) and Orthoptera (5). The insect analysed have a higher proportion of fat and less
protein than sh meal. With the exceptions of histidine, threonine and lysine, the insects present an amino
acid prole similar to sh meal, with Diptera b being the most similar group to sh meal. However, the fatty
acid content of insects is very different from that of sh meal which is rich in n-3, especially 14% EPA, 16%
DHA, practically absent in insects. The insects have higher ratios of omega 6 and monounsaturated fat.
2013 Elsevier B.V. All rights reserved.

1. Introduction
Fish have been a key source of food for humans (Ayoola, 2010), but
the global catch of wild sh declined approximately 3% from 2004 to
2009 at a rate of 0.5% per year (FAO, 2010). Currently, aquaculture is
playing an essential role in the seafood market, meeting the demand
for sh that cannot be met with the wild catch. As a consequence, in
recent years (from 2004 to 2009), aquaculture production has grown
by 32%, a growth rate of approximately 5.6% per year (FAO, 2010).
Fishmeal is one of the major components of the feed used in aquaculture. It is generally added to animal diets to increase feed efciency
and animal growth through better feed palatability; it also enhances
the uptake, digestion, and absorption of nutrients (Mile and Chapman,
2006). It is estimated that approximately 30% of the total sh catch is
converted to sh meal and sh oil for use in animal and sh feeds
(Ogunji et al., 2006).
The percentage of sh meal that is used for aquaculture feeds has increased from 10% in 1988 to approximately 45% in 2002. The increasing
global demand for and decreasing availability of sh meal has led to
sharp increases in the price of sh meal, and hence, the cost of aquaculture production has increased as well (Ayoola, 2010). The price of
producing sh through aquaculture has risen from US $600/metric ton

Corresponding author at: Department of Applied Biology, E.S.I. University of Almera,

Carretera de Sacramento s/n, 04120 Almera, Spain. Tel.: +34 950015918; fax: + 34
950015476.
E-mail address: fbarroso@ual.es (F.G. Barroso).
0044-8486/$ see front matter 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.aquaculture.2013.12.024

in 2005 to US $2000/metric ton in June 2010, and this trend is likely to

continue (International Monetary Fund, 2010).
The present shortage of sh meal motivates researchers to seek new
protein sources with nutritional values similar to sh meal, in particular
those with similar contents of the essential amino acids, phospholipids,
and fatty acids (docosahexaenoic acid and eicosapentaenoic acid) that
promote optimum development, growth, and reproduction (Ayoola,
2010), which would allow aquaculture production to remain economically and environmentally sustainable over the long term.
From vegetable sources, soybean meal is the best available vegetable
protein source in terms of protein content and EAA prole. However, it
is potentially limiting in sulphur-containing amino acids (methionine
and cysteine) and contains some antinutrient substances such as trypsin
inhibitor, haemagglutinin, and antivitamins (Tacon, 1993).
Regarding sources of animal origin mostly of them are forbidden by
prescription of food security, which have made more urgent the search
for alternatives to sh meal in aquaculture diets (Ogunji, 2004).
Edible insects are a natural renewable resource used as food by
humans (Ramos-Elorduy and Conconi, 1994). Since ancient times,
insects have been one alternative protein source used to compensate
for the periodic or seasonal scarcity of other sources (RamosElorduy,
1997). The most existing studies have focused on the insects that have
played an important role in human nutrition in Africa, Asia, and Latin
America. Thus, we can highlight the studies conducted in Nigeria
(Akinnawo and Ketiku, 2000; Banjo et al., 2006), Mexico (Ramos
Elorduy, 1997; Ramos-Elorduy and Conconi, 1994; Ramos-Elorduy
et al., 1997, 2006), Thailand (YhoungAree et al., 1997) and Zaire
(Kitsa, 1989).

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F.G. Barroso et al. / Aquaculture 422423 (2014) 193201

Although insects began to be evaluated as a potential foodstuff for

animals 40 years ago (Calvert et al., 1969; Hale, 1973; Ichhponani and
Malik, 1971; Newton et al., 1977; Phelps et al., 1975; Teotia and Miller,
1974), the incorporation of insects into sh feed has not received much
attention until recently (Ogunji et al., 2006). In the last 10 years there
have been several studies of feeding experiments performed in vivo
with diets based on insect meal in Clarias anguillaris (Achionye-Nzeh
and Ngwudo, 2003), Clarias gariepinus (Alegbeleye et al., 2012; Aniebo
et al., 2011; Fasakin et al., 2003), Orcorhychus mykiss (Sealey et al.,
2011; St-Hilaire et al., 2007) Oreochromis niloticus (de Haro et al.,
2011a,b,c,d,e; Ogunji et al., 2006, 2008) and Psetta maxima (Kroeckel
et al., 2012). In general, percentages of substitution higher than 30%
decreased the growth depending on the sh and insect species.
From the nutritional point of view, depending on species and/or
stage, insects are rich in protein and lipids, nevertheless the presence
of chitin a priori indicates a negative characteristic. However, chitin
also is present in crustacean, which are widely consumed by sh.
To evaluate the potential of insects, it is necessary to consider other
advantages such as environmental benets; the insects can be fed with
waste generated by humans, having an important role in recycling
materials in the terrestrial biosphere (Katayama et al., 2008). The
great diversity of insect species (7075% of animal species), from
different ecosystems, with different diets and stages of development
(larval, pupa, ninpha or imago) provokes a huge variability in body
composition.
The aims of this study are: (1) to determine the nutritive valour of
the most frequent rearing insects and some of the common species of
Almeria (Spain), and (2) to establish the most similar to sh meal.

2. Materials and methods

2.1. Sampling
The insects and stages of its development (larval, pupa, ninpha
or imago) studied were chosen according to the following criteria:
easy to rearing, stage with mayor biomass and low exoskeleton.
The wild species were chosen in terms of their availability in the
environment.
The insects used in the study were obtained from pet shops
(captivity*), reared by the research group "Bionomy, Systematic and applied research on insects from University of Alicante & technologybased company Bioytech (captivity **) or captured in the eld close
to our environment (wild-rearing). Table 1 summarises the insects studied, which belong to three orders, Diptera, Orthoptera and Coleoptera.
The nutritional contents of insects were compared with those of sh
meal and soybean meal because they are the most common ingredients
used in aquafeed production.

2.2. Analytical methods

2.2.1. Determination of proximate composition
The nutritional values obtained were derived from three replicate
samples for each species of insecta, sh meal and soy meal. Moisture,
crude protein, total lipids and ash were determined using AOAC
(2005) techniques.
The insects were sacriced by freezing (Finke et al., 1989). All
samples, insects, shmeal and soy meal were lyophilised (Cryodos,
Ima-Telstar, Terrassa, Spain), and ground and freezing until to be
analized. Total nitrogen (N) was determined using the Kjeldahl
procedure, and crude protein was estimated as N x 6.25. Crude lipid
was determined following the Soxhlet extraction of dried samples
with petroleum ether. Moisture was determined after oven drying the
samples at 105 C to a constant weight. The ash was determined
eliminating the organic matter at 500 C during 12 h.

2.2.2. Determination of amino acid prole

The amino acid prole was determined after hydrolysing the sample
with 6 N HCl for 22 h at 110 C, followed by a sequence of ltering,
derivatisation, and separation in a gas chromatograph. Tryptophan
was not determined.
2.2.3. Analysis of fatty acids
For the FA analyses, all samples were transmethylated following the
method of Lepage and Roy (1984) with the minor modications of
Venegas-Venegas et al. (2011): for each sample, 1 ml of freshly
prepared transesterication reagents (methanol/acetyl chloride, 20:1,
v/v) was added to 50 mg of freeze-dried insect meal in a glass tube
along with 100 l of a solution of internal standard (heptadecanoic
acid 17:0, 10 mg/ml). The tubes were shaken and then placed in a hot
block (100 C, 30 min). Next, the mixture was cooled to room temperature, and 1 ml of distilled water was added to each tube. The samples
were shaken again and centrifuged (3,000 rpm, 3 min). The upper
hexane phase was collected for GLC analysis.
The resulting FA methyl esters (FAMEs) were analysed in a Focus
GLC (Thermo Electron, Cambridge, UK) equipped with a ame injection
detector (FID) and an Omegawax 250 capillary column (30 m 9
0.25 mm i. d. 9 0.25 lm lm thickness; Supelco, Bellefonte, PA, USA).
The temperature programme was 1 min at 90 C, heating to 200 C at
a rate of 10 C/min, constant temperature at 200 C (3 min), heating
to 260 C at a rate of 6C/min and constant temperature at 260 C
(5 min). The injector temperature was 250 C with a split ratio of
50:1. The injection volume was 4 l. The detector temperature was
260 C. Nitrogen was used as the carrier gas (1 ml/min).
Total saturated, monounsaturated, polyunsaturated, n-3 and n-6
fatty acids were calculated as the sums of saturated fatty acids (SFA),
monounsaturated fatty acids (MUFA), polyunsaturated fatty acids
(PUFA), n-3 and n-6 fatty acids, respectively.
2.3. Data analysis
To better understand the applied value of the study's results, in addition to a descriptive approach to the nutritional value of the insects, the
compositions of the insect meals were compared with the compositions
of sh meal and soybean meal.
To determine the similarity between the compositions of sh meal,
soybean meal and the different species of insects, a hierarchical cluster
analysis was used.

Table 1
Order, stage of developement and origin of the species of insect analised.
Order

Scientic name

Stage

Abbreviation

Origin

Coleoptera
Coleoptera
Coleoptera
Coleoptera
Diptera
Diptera
Diptera
Diptera
Diptera
Diptera
Diptera
Diptera
Diptera
Diptera
Diptera
Diptera
Orthoptera
Orthoptera
Orthoptera
Orthoptera
Orthoptera

Phyllognathus excavatus
Rhynchophorus ferrugineus
Tenebrio mollitor
Zophoba morio
Calliphora vicina
Chrysomya megacephala
Chrysomya megacephala
Eristalis tenax
Hermetia illucens
Hermetia illucens
Lucilia sericata
Lucilia sericata
Musca domestica
Musca domestica
Protophormia terraenovae
Protophormia terraenovae
Acheta domestica
Anacridium aegyptium
Gryllus assimilis
Heteracris litoralis
Locusta migratoria

Adult
Larvae
Larvae
Larvae
Larvae
Larvae (L3)
Pupae
Larvae (L3)
Larvae (L5)
Pupae
Larvae (L3)
Pupae
Larvae (L3)
Pupae
Larvae (L3)
Pupae
Adult
Adult
Adult
Adult
Adult

PeA C
RfL C
TmL C
ZmL C
CvL D
CmL D
CmP D
EtL D
HiL D
HiP D
LsL D
LsP D
MdL D
MdP D
PtL D
PtP D
AdA O
AaA O
GaA O
HlA O
LmA O

Free-ranging
Free-ranging
Captivity*
Captivity*
Captivity*
Captivity**
Captivity**
Captivity**
Captivity**
Captivity**
Captivity**
Captivity**
Captivity**
Captivity**
Captivity**
Captivity**
Captivity*
Free-ranging
Captivity*
Free-ranging
Captivity*

F.G. Barroso et al. / Aquaculture 422423 (2014) 193201

Clustering is a multivariate technique of grouping together rows that

share similar values. Cluster analysis is an exploratory data analysis
technique for solving classication problems. Its purpose is to sort the
different food sources (sh meal, soybean meal and insect meals) into
groups (clusters) so that the degree of association/similarity between
members of the same cluster is stronger than the degree of association/similarity between members of different clusters. Each cluster is
described as the class to which its members belong. This analysis
provides a dendrogram grouping the meals according to the distance
between them.
The similarities were evaluated using hierarchical cluster analysis in
the Past (Paleontological Statistics, Version 2.17). The analysis was performed using hierarchical option clusters based on Ward's method
(Ward, 1963) with standardised data. Bootstrapping has previously
been used to obtain condence intervals.
Specically, there were two cluster analyses based on different
characteristics:
The proportion of essential amino acids.
The proportion of fatty acids
We observed that the cluster analysis classied different insect
species according to their taxonomic order. Therefore, to analyse the
differences between orders, we grouped the data by order regardless
of the species. An analysis of variance with the taxonomic order as
main factor was performed with the JMP (Version 9.0.0) statistical
package (SAS Institute, Inc.) to evaluate the relationship between the
compositions of amino acids and fatty acids. Signicant differences in
the mean response were determined with the TukeyKramer HSD test.
3. Results
The proximate analysis of the insect samples is summarised
in Table 2. As expected, most insect species analysed have a high
proportion of protein, between 40 and 60% in similar to soy meal levels
(50% CP) and lower than shmeal (73.0% CP). The lowest levels were
measured in Rhynchophorus ferrugineus (35%) and Hermetia illucens
larvae (36%). The protein content of Orthoptera (73% CP) is similar to
sh meal (73.0%), particularly Heteracris littoralis (74%) and Acheta
domestica (73%).

195

The lipid levels in sh meal (8.2%) and soy meal (3.0%) are lower
than in insects. The lipid contents of most of the insects reached 20%.
The highest values were obtained for Locusta migratoria, Musca
domestica larvae and Tenebrio mollitor with 30% lipids and Zophoba
morio with 38.0% lipids.
These insects contain between 5 and 20% of nitrogen free extract
(NFE). Only three of the species had nitrogen free extracts above 35%.
NFE involve carbohydrates, sugars, starches, bre and chitin (primarily
a nitrogen-containing polysaccharide).
Regarding ash, sh meal contains a higher percentage (18.0%) than
insect meals (except for Hermetia pupae, 19.7%) or soybean meal.
The amino acid analyses are summarised in Table 3. In general, the
amino acid patterns were quite different among species.
The dendrogram in Fig. 1 illustrates the similarity of the essential
amino acid proles of the insects, sh meal and soybean meal. As
shown in Fig. 1, two major groups or cluster were formed; (1) sh
meal and Diptera, (2) Orthoptera, soybean meal and Coleoptera. Thus,
Diptera appears to be the most similar to sh meal in terms of its
amino acid composition, especially the larvae of Hermetia, Musca and
Eristalis, whereas Coleoptera is the most different from sh meal in
amino acid composition. Soybean meal is closer to Orthoptera in the
dendrogram. These results veried the relationship between similarity
in amino acid composition and insect taxonomy, as each order was
grouped into a different cluster.
Fig. 2 presents the signicant differences in the proportion of
essential amino acids among the three orders of insects, sh meal and
soybean meal for all essential amino acids. Relative to sh meal, the
insect meals are decient in the amino acids histidine, lysine and
threonine, but better in lysine methionine and tyrosine than soy meal.
Diptera shows a histidine, lysine and threonine proportion similar to
sh meal (Fig. 2 and Table 3). Diptera also has a similar proportion of
methionine and a higher proportion of phenylalanine compared to
sh meal and soy meal. However, Diptera exhibits a relative decit in
leucine that does not occur in Orthoptera or Coleoptera. The percentages of tyrosine and valine were higher in all analysed insects than in
sh meal.
These data reveal that Diptera has similar amino acids prole to sh
meal. Ortopthera and Coleoptera, although not so similar to sh meal,
have better amino acids prole than soy meal.

Table 2
Proximate analysis (% dry matter) of selected insects, sh meal and soybean meal.
Specie
Phyllognathus excavatus
Rhynchophorus ferrugineus
Tenebrio mollitor
Zophoba morio
Calliphora vicina
Chrysomya megacephala
Chrysomya megacephala
Eristalis tenax
Hermetia illucens
Hermetia illucens
Lucilia sericata
Lucilia sericata
Musca domestica
Musca domestica
Protophormia terraenovae
Protophormia terraenovae
Acheta domestica
Anacridium aegyptium
Gryllus assimilis
Heteracris littoralis
Locusta migratoria
Fish meal
Soybean meal

ASH %
PeA C
RfL C
TmL C
ZmL C
CvL D
CmL D
CmP D
EtL D
HiL D
HiP D
LsL D
LsP D
MdL D
MdP D
PtL D
PtP D
AdA O
AaA O
GaA O
HlA O
LmA O
FM
SM

7.8
6.6
3.5
2.5
8.0
7.2
6.1
13.9
9.3
19.7
4.9
4.9
6.5
8.4
3.9
8.8
5.6
3.7
4.8
5.1
4.0
18.0
7.8

EE %
0.2
0.6
0.2
0.3
0.1
0.1
0.1
0.4
0.3
0.1
0.9
0.2
1.5
2.9
0.1
0.1
0.0
0.1
0.1
0.1
0.0
0.2
0.0

15.9
11.8
30.1
38.0
20.1
27.0
16.5
5.8
18.0
15.6
28.4
26.6
31.3
33.7
28.3
23.6
15.9
17.6
23.2
8.8
29.9
8.2
3.0

Values are means SD of triplicate determinations. EECrude fat. CPCrude protein. NFENitrogen-free extract.

CP %

1.4
1.5
0.7
0.3
0.7
3.2
0.0
0.6
1.6
0.1
1.5
1.0
1.6
0.7
0.6
0.3
0.2
0.2
0.6
0.0
0.5
0.0
0.0

65.7
34.6
58.4
53.5
48.3
61.8
46.8
40.9
36.2
40.7
53.5
59.0
46.9
40.1
46.3
56.0
73.1
66.0
64.9
74.4
58.5
73.0
50.4

NFE %
1.3
0.3
0.4
0.4
0.9
0.3
1.1
0.9
0.3
0.4
4.4
1.5
4.1
0.4
0.6
2.0
3.3
5.0
0.5
1.0
0.5
0.8
0.2

10.6
47.0
8.0
6.0
23.6
4.0
30.6
39.4
36.5
24.0
13.2
9.5
15.3
17.8
21.5
11.6
5.4
12.7
7.0
11.7
7.6
0.8
38.8

0.1
1.3
0.2
1.1
0.1
3.4
1.1
1.1
1.0
0.7
4.6
0.1
4.0
0.3
0.1
2.2
0.3
4.8
0.3
1.0
0.1
0.7
0.3

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F.G. Barroso et al. / Aquaculture 422423 (2014) 193201

Table 3
Amino acid (as a percentage of total amino acids) of selected insects, sh meal and
soybean meal.
Specie

ARG

HIS

ILE

LEU

LYS

MET

PHE

PRO

THR

TYR

VAL

PeA C
RfL C
TmL C
ZmL C
CvL D
CmL D
CmP D
EtL D
HiL D
HiP D
LsL D
LsP D
MdL D
MdP D
PtL D
PtP D
AdA O
AaA O
GaA O
HlA O
LmA O
FM
SM

5.76
4.82
6.14
5.72
8.57
7.83
8.99
7.69
8.24
8.05
8.84
7.67
6.83
8.76
7.49
7.71
8.53
9.63
9.23
7.93
7.58
7.42
8.03

4.19
3.62
3.64
3.87
5.02
5.08
5.20
4.22
5.29
5.16
5.12
5.18
4.68
5.17
5.48
5.35
2.93
4.04
3.03
2.69
2.98
7.86
3.28

5.71
5.85
5.87
6.36
5.09
4.85
5.23
6.16
5.76
5.34
5.05
5.10
4.89
5.20
5.20
5.08
5.31
5.16
5.05
5.34
5.27
5.04
5.47

7.59
6.63
8.65
8.25
6.69
6.89
6.96
7.62
6.87
6.83
6.43
6.96
6.75
6.57
6.29
6.77
8.69
7.28
8.06
8.88
8.31
7.81
8.01

6.34
6.18
6.03
5.82
7.99
8.53
7.87
8.45
7.60
7.31
7.66
7.91
8.36
7.57
8.23
7.89
6.16
5.73
6.46
6.01
6.33
8.78
6.34

1.42
0.45
0.64
0.76
2.16
2.22
2.76
2.37
1.50
3.26
3.36
3.08
3.00
3.44
2.30
2.55
1.49
2.36
1.10
1.02
0.54
2.93
1.01

4.17
5.81
4.29
5.00
7.12
7.17
6.73
6.64
6.88
6.22
7.42
7.02
7.01
6.86
8.10
7.15
4.23
5.00
4.10
3.63
3.84
5.38
5.79

5.80
7.38
7.17
5.62
4.71
4.56
4.76
5.06
6.16
5.56
4.95
4.83
5.33
5.37
4.91
4.98
5.84
7.21
6.20
6.75
7.46
4.76
4.99

4.10
4.00
4.49
4.33
4.86
4.51
5.02
5.02
5.39
4.95
5.38
4.60
4.87
5.28
4.78
4.83
4.10
4.49
4.11
3.90
4.28
6.26
4.17

4.26
9.84
4.18
6.28
6.36
6.68
6.02
5.21
6.35
7.14
6.64
6.29
5.79
5.91
7.43
7.10
4.91
5.75
4.31
4.51
4.48
3.91
2.93

7.15
6.69
7.61
7.55
5.93
5.77
6.14
6.52
6.31
6.34
5.88
6.03
6.08
6.08
5.99
6.05
6.99
6.64
6.60
7.48
7.01
5.56
5.45

larger; sh meal contains only 2.5% n-6, and soy meal 55,4%, whereas insects have a intermediate proportion, in some species reaching over
than 30% (e.g., Tenebrio mollitor, Gryllus assimilis and Acheta domestica).
Eristalis tenax is the only studied species that had a proportion (1.9%) of
n-6 similar to that of sh meal.
The variability of fatty acid proles among species (Fig. 3) was
greater than the variation in essential amino acids, with signicant
differences in only some fatty acids. The Orthoptera exhibited a higher
proportion of n-3, especially for ALA 18:3 n3. No differences between
groups for n-6 acids were observed except for the lower proportion of
linoleic acid (18:2 n6) in Diptera compared to Orthoptera.
The dendrogram (Fig. 4) illustrates the similarities of the fatty acid
compositions among insects, sh meal and soybean meal. The results
of the cluster analysis show several groups and the distances are higher
than the amino acids. Farthest group is composed of sh meal, Eristalis
tenax and Hermetia ilucens larvae. Soybean meal and the other insects
(Diptera, Coleoptera and Orthoptera) are mixed in more distanced
groups.
4. Discussion
The results obtained of nutrients composition of insect show
differences regarding shmeal and among species and/or stage.
4.1. Proximal composition

Table 4 and Fig. 3 show fatty acids composition of insect sh meal

and soy meal. The most notable difference was the higher percentage
of n-3 fatty acid in sh meal, up to 37% of the total fatty acids, containing
14% EPA (20:5 n3) and 16% DHA (22:6 n3). In contrast, the insects have
a much lower proportion of n-3, while soy mal a rich in n-6. Some species of Orthoptera show a higher proportion (Hetteracris littoralis, 19.8%
and Anacridium aegyptium, 17.9%), but the n-3 in those species consists
primarily of ac-linolenic acid (ALA 18:3 n3). Chrysomya megacephala
and Calliphora vicina (Diptera) only contain EPA, but it does not exceed
1.5% of total FAs, a low percentage compared with the sh meal values.
The saturated fatty acid compositions of the insect meals are similar
to sh meal; nevertheless, insects have nearly twice monounsaturated
fatty acid than sh meal and soy meal. The difference in n-6 is much

Most of the insects species analysed have a high proportion of

protein, similar to the levels of soy meal but lower than sh meal. In
general, the order Orthoptera exhibits a higher CP, between 60 and
70%, but it must be taken into account that all samples of this order
are adults with more chitin (and chitin nitrogen) and less fat that
enhances CP levels. In Diptera, the levels of CP range from 40 to 50%,
with higher values for the larvae of Chrysomya megacephala, pupae of
Lucilia sericata and pupae of Protophormia terraenova (5062%). The
CP values vary among published works, the CP value obtained for larvae
of Musca domestica was 46.9%, similar to that reported by Ogunji et al.
(2008), 47.1%, whereas other authors have obtained more diverse
results, including 37.5% (Aniebo and Owen, 2010) and 56.8% (Bernard

Fig. 1. Cluster analysis of amino acids similarity among insect species, sh meal and soybean meal.

F.G. Barroso et al. / Aquaculture 422423 (2014) 193201

et al., 1997). In pupae of Musca domestica, Bernard et al. (1997) obtained

a higher proportion, 58.3%, than that observed in this experiment, 40.1%.
The percentage of CP obtained in larvae of Hermetia illucens (36.2%) is
similar to those obtained by Sheppard (2002) (37.8%) and Arango
et al. (2004) (37%) and slightly lower than the value of 40.6% described
by Newton et al. (1977). The CP content obtained in Eristalis tenax,
40.9%, is similar to that observed by Ramos-Elorduy et al. (1998) in
Eristalis sp. (40.7%).
In the order Coleoptera, the species with the least CP is Rhynchophorus
ferrugineus (35%). The larvae of the genus Rhynchophorus are not very
protein-rich; Banjo et al. (2006) reported that Rhynchophorus phoenicis
was only 28.4% protein, and Cerda et al. (1999) reported 25.8% protein
for Rhynchophorus palmarum. In Tenebrio mollitor larvae, the observed
CP was 58.4%, and in Zophoba morio, 53.5%. Both the Tenebrio and
Zophoba values are slightly higher than those observed by other authors:
between 47 and 53% for Tenebrio mollitor (Bernard et al., 1997; Finke,
2002, 2007; Ramos-Elorduy et al., 2006) and 46.8% for Zophoba morio
(Finke, 2002).
These differences may be due to the phase of development of the
insect, variations in dietary habits between populations, the method of
processing or differences in ecotypes (Banjo et al., 2006; Fasakin et al.,
2003; Teguia and Beynen, 2005), and this makes it difcult to draw
solid conclusions related to differences between orders.
Nevertheless the results of this study indicate that the protein
content of insects is generally less than that of sh meal and it is similar
to soybean meal. There are substantial differences between the protein
contents reported by different authors, even for the same species of
insect. This must be investigated to know the species and stages appropriate to be used in sh feeding.
On the other hand, an additional problem to CP determination in
insect is the nitrogen contained within nacetylglucosamine, a subunit
of the chitin polymer, digestibly unavailable (Finke et al., 1989). Finke
(2002) suggests that the amount of nitrogen contained in chitin is
relatively small, and thus, nitrogen content may provide a reasonable
estimate of total protein in most invertebrates.
The fat content of insects is highly variable and it seems to vary between stages, usually ranging between 15 and 30%. Zophoba morio is
the species with the highest proportion of fat (38%) of all of the analysed
species; this value is slightly lower than that obtained by Finke (2002),
42%. The larvae of coleopterans generally have a large amount of fat,
often exceeding 25%, the high proportion of fat was recorded for
Tenebrio mollitor (30%), lower than levels (38 to 43%) reported by
other authors (Finke, 2002, 2007; Ramos-Elorduy et al., 2006). A
lower proportion was obtained in this study for the larvae of Eristalis

197

tenax (5.8%), lower than that obtained by Ramos-Elorduy et al. (1998)

in Eristalis sp. (11.9%). Fat levels in both, larvae (31.3%) and pupae
(33.7%) of Musca domestica are greater than those observed by other authors: from 13.5 to 25% in larvae (Aniebo and Owen, 2010; Bernard
et al., 1997; Ogunji et al., 2006, 2008; Sheppard, 2002) and 15.8% in
pupae (Bernard et al., 1997). As reported by Arango et al. (2004), the
percentage obtained for the larvae of Hermetia illucens, 18%, is lower
than the values observed by Newton et al. (1977) and Sheppard
(2002), both greater than 30%.
The stage of development may also affect the fat content. In general,
the larval stages contained signicantly more fat than adults (Barker
et al., 1998). In Acheta domestica varies between 14 and 22% (Bernard
et al., 1997; Finke, 2002, 2007) at different stages of development.
Probably the differences in lipids among the same species, reported by
different authors, could be related not only to the stage of development
but also to the age.
Diet appears to be another factor that inuences the fat content of
insects. A comparison of the fat content of the wild orthopteran
Heteracris littoralis, at 8.2%, with captive-bred orthopterans (Acheta
domestica, Gryllus assimilis and Locusta migratoria), with a higher
proportion of fat, suggests that diet could affect lipid content.
As it occurs with CP, the lipids content varies enormously. Because of
this, it is difcult to obtaine a clear conclusion regarding relation between lipids content and taxon, stage or feeding. Supplementary studies
are needed.
On the other hand, the lipid levels in sh meal and soy meal are
lower than in insects, which could complicate the use of insect meals
in shfeeds.
The ash contents obtained for all analysed insects were less than that
of sh meal (18.0%), with the exception of Hermetia illucens pupae
(19.7%). Arango et al. (2004) (17.5%) and Newton et al. (1977) also
found elevated levels (14.6%) of ash in this species.
4.2. Amino acid prole
A balanced essential amino acid (EAA) prole is one of the characteristics that dene the quality of protein. The development of commercial
aquatic feeds has traditionally been based on FM as the primary protein
source due to its high protein content and balanced essential amino acid
prole (Nguyen et al., 2009) with high level of digestible essential
amino acids such as lysine, methionine and leucine, which are often decient in grains, the typical base for most animal feeds (Hall, 1992;
Keller, 1990). Currently, the specic amino acid composition of most insect species is unknown. In this work the amino acids prole of different

Fig. 2. Differences between insect orders studied in the percentage of essential amino acids (using sh meal and soybean reference).

198

F.G. Barroso et al. / Aquaculture 422423 (2014) 193201

Table 4
Fatty acid content (as a percentage of total fatty acid) of selected insects, sh meal and soybean meal.
Specie

12:0

14:0

16:0

PeA C
RfL C
TmL C
ZmL C
CvL D
CmL D
CmP D
EtL D
HiL D
HiP D
LsL D
LsP D
MdL D
MdP D
PtL D
PtP D
AdA O
AaA O
GaA O
HlA O
LmA O
FM
SM
Mean

0
0
0
0
0
0
0
4.8 0.6
43.4 0.6
0
0
0
0
0
0
0
0
0
0
0
0
0
4.1 1.3
S.D.

0
1.6 0.1
2.2 0.0
1.1 0.1
1.6 0.1
1.5 0.1
1.8 0.1
17.2 0.8
7.9 0.1
2.4 0.2
3.7 0.1
2.9 0.1
2.4 0.1
2.5 0.1
2.4 0.1
2.4 0.1
0.5 0.0
1.9 0.4
0.4 0.6
1.1 0.1
2.3 0.1
7.9 0.4
0

24.2
37.8
16.6
30.2
19.4
24.7
25.6
18.1
13.2
16.6
21.7
22.6
23.1
22.6
21.9
22.8
24.9
24.1
26.4
17.5
28.4
23.0
15.1

3.0
0.4
0.1
0.4
0.1
1.1
0.4
0.1
0.1
0.1
0.1
0.3
0.5
1.1
0.1
0.3
0.1
1.5
0.0
0.5
0.1
0.6
0.2

17:0

18:0

0
0
0
0
0
0
0
0
0
3.4 0.0
0
0
0
0
0
0
0
0
0
0
0
0
0

4.5
3.2
3.4
7.6
7.6
9.7
8.1
1.7
2.8
43.5
2.5
3.3
7.2
4.9
2.8
1.4
8.8
4.4
7.2
9.2
5.8
5.3
4.8

0.1
0.1
0.0
0.2
0.1
0.0
0.1
0.0
0.1
0.2
0.1
0.1
0.8
0.1
0.0
2.0
0.0
0.2
0.0
0.1
0.1
0.1
0.4

16:1 n7

18:1 n7

18:1 n9

20:1 n9

18:2 n6

18:3 n6

20:4 n6

22:4 n6

2.0 0.0
4.2 0.1
2.2 0.0
1.0 0.0
12.8 0.1
5.4 0.3
7.5 0.5
45.4 0.3
2.3 0.1
2.2 0.0
19.3 0.4
17.3 0.1
15.1 0.8
15.4 0.7
11.0 0.1
10.4 0.2
0.9 0.0
1.4 0.1
1.7 0.0
0.9 0.2
2.5 0.1
7.9 0.3
0

0
0
0
0
2.6 0.0
0.7 0.1
0.6 0.1
0.3 0.4
0
30.4 0.1
0.3 0.0
0.5 0.0
0.3 0.1
0.3 0.1
0
0.2 0.3
0
0
0
0
0
4.0 0.7
0.8 0.0

55.1 0.5
40.3 0.1
43.6 0.1
34.7 0.4
24.9 0.1
24.6 0.2
27.1 0.1
4.6 0.1
14.6 0.3
0
35.3 0.5
36.5 0.4
37.1 0.7
38.3 1.4
33.8 0.0
33.0 0.6
20.4 0.1
37.4 0.9
25.8 0.4
26.8 0.1
45.3 0.6
8.4 0.1
14.3 0.3

0
0
0
0
0.4
0
0.3
0
0
0
0.2
0
0.2
0.1
0
0
0
0
0
0
0
0.3
0

11.0 0.4
11.2 0.4
30.4 0.1
22.6 0.0
10.8 0.1
15.1 0.1
12.5 0.2
1.6 0.0
15.2 0.4
0
8.1 0.2
7.5 0.1
6.5 0.0
6.6 0.2
16.1 0.1
16.2 0.2
41.4 0.1
12.1 0.3
34.4 0.2
22.3 0.1
11.2 0.2
1.1 0.1
48.5 0.6

0
0
0
0
0.9
1.4
1.3
0
0
1.1
0
0.2
0.2
0.1
0.4
0.5
0
0
0
0
0
0
0

0
0
0
0
12.5 0.2
12.0 0.4
9.3 0.1
0
0
0
0.7 0.1
2.7 0.1
0.4 0.0
0.4 0.1
2.8 0.1
2.6 0.1
0
0
0
0
0
1.4 0.0
0

0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0.7 0.0
0
0
0
0

Specie

18:3 n3

18:4 n3

20:5 n3

22:5 n3

22:6 n3

Other

PeA C
RfL C
TmL C
ZmL C
CvL D
CmL D
CmP D
EtL D
HiL D
HiP D
LsL D
LsP D
MdL D
MdP D
PtL D
PtP D
AdA O
AaA O
GaA O
HlA O
LmA O
FM
SM

0.9 0.1
1.9 0.1
1.1 0.0
1.4 0.0
0.2 0.3
0.6 0.0
0.5 0.0
0
0.7 0.1
0
0.4 0.0
0.3 0.0
0.3 0.0
0.3 0.0
0.8 0.0
0.8 0.0
1.8 0.0
17.9 0.4
1.8 0.0
19.4 0.1
4.7 0.1
0.2 0.3
6.9 0.2

0
0
0
0
1.3
0.4
0.7
0
0
0
0.2
0
0.1
0.2
1.1
0.8
0
0
0
0
0
1.9
0

0
0
0
0
1.4 0.0
1.3 0.1
1.5 0.1
0
0
0
0.1 0.0
0.4 0.0
0.1 0.1
0.1 0.1
0.8 0.0
0.9 0.0
0
0
0.7 0.1
0.4 0.0
0
14.1 0.2
0

0
0
0
0
0.7
0.6
0.4
0
0
0
0
0
0
0
0
0
0
0
0
0
0
2.7
0

0
0
0
0
0.4 0.0
0
0.2 0.2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
16.1 0.1
0

1.5
0.1
0.6
1.6
2.9
2.3
3.0
6.5
0.1
0.6
7.8
6.0
7.2
8.5
6.3
8.3
1.3
1.0
1.0
2.7
0.1
6.0
5.6

0.1
0.0
0.1

0.0

0.0
0.0
0.1
0.0

0.0

0.1
0.1
0.0

0.1

species and stages have been studied. The results show that the prole
of amino acids is related to the taxonomic group (Fig. 1) and Diptera
are most similar, in terms of essential and limiting amino acids, to sh
meal (Fig. 2). This group has a similar proportion of methionine to sh
meal and higher values of histidine, lysine and threonine. Orthoptera
and Coleoptera have a higher proportion of leucine.
These results are consistent with several studies in which low levels
of methionine have been observed in Orthoptera (Bernard et al., 1997;
Finke, 2002, 2007) and Coleoptera (Cerda et al., 1999; Finke, 2002,
2007; Ramos-Elorduy et al., 2006) and high levels in Diptera (Newton
et al., 1977; Ogunji et al., 2006). Regarding lysine, the proportions
obtained for both Coleoptera and Orthoptera, 6%, are similar to those
described by Finke (2002, 2007). In Diptera, the lysine level obtained
in this work, 8%, coincided with the value previously reported by
Newton et al. (1977).
The proportions of arginine have been shown to be adequate for
Diptera and Orthoptera; however, the Coleoptera are in decit. These
results differ somewhat from earlier studies, which found that the
proportion of arginine in Orthopterans was approximately 7% (Finke,
2002, 2007) and those in Diptera (Newton et al., 1977; Ogunji et al.,

Satura.
2.1
0.0
0.0
0.1
0.0
0.6
1.1
1.2
0.2
0.0
0.3
0.0
0.0
0.1
0.1
1.9
0.1
0.0
0.7
0.3
0.1
0.4
0.8

28.7
42.5
22.2
38.8
28.5
35.9
35.4
41.7
67.1
65.8
27.8
28.8
32.6
30.0
27.1
26.6
34.2
30.3
34.0
27.7
36.4
36.1
24.0

3.0
0.4
0.1
0.2
0.2
1.2
0.6
1.4
0.6
0.1
0.1
0.4
0.1
1.1
0.2
1.6
0.1
1.7
0.6
0.6
0.1
1.1
1.9

0.1
0.0

0.0
0.0
0.1

0.4

Monoun.

-6

58.1
44.4
45.8
35.7
40.7
30.6
35.4
50.3
16.9
32.6
55.0
54.3
52.7
54.1
44.8
43.5
21.3
38.7
27.5
27.6
47.8
20.6
15.1

11.8
13.0
31.5
24.0
24.1
28.5
23.0
1.6
15.2
1.1
8.8
10.3
7.1
7.0
19.2
19.2
43.2
30.0
36.9
41.7
15.9
2.7
55.4

0.5
0.0
0.1
0.4
0.4
0.1
0.7
0.2
0.2
0.1
0.1
0.2
0.2
0.8
0.1
0.1
0.1
1.0
0.4
0.3
0.5
0.7
0.3

0.4
0.4
0.1
0.0
0.1
0.5
0.3
0.0
0.4
0.0
0.4
0.1
0.0
0.4
0.1
0.2
0.1
0.7
0.2
0.1
0.4
0.2
0.8

0.0
0.0
0.0

0.0

0.0
0.0
0.1
0.0
0.1

-3

Polyuns.

0
0
0
0
3.9 0.3
2.9 0.4
3.2 0.4
0
0.7 0.1
0
0.7 0.0
0.7 0.0
0.5 0.1
0.6 0.1
2.7 0.1
2.5 0.0
0
0
0.7 0.1
0.4 0.0
0
34.7 0.2
0

11.8
13.0
31.5
24.0
28.0
31.3
26.2
1.6
15.9
1.1
9.5
11.0
7.6
7.5
21.9
21.7
43.2
30.0
37.5
42.1
15.9
37.3
55.4

0.4
0.4
0.1
0.0
0.1
0.7
0.1
0.0
0.6
0.0
0.4
0.1
0.1
0.4
0.2
0.2
0.1
0.7
0.3
0.1
0.4
0.0
0.8

2006) and Coleoptera (Finke, 2002, 2007; Ramos-Elorduy et al., 2006)

were approximately 5%.
In terms of similarity to sh meal, the amino acid prole of the
Diptera is superior to that of soybean meal, thus Diptera could be a
better replacement than soybean meal in the formulation of sh feed.
Although each species is decient in some essential amino acids, it is
possible to design a feedstuff that is balanced in amino acids by combining several species of insect.
4.3. Fatty acids
According to Ramos-Elorduy (2008) insects contain higher quantities of polyunsaturated fats (PUFAs) n-6 than sh meal, but lower
than soy meal. As in soy, lower levels of polyunsaturated fats n-3 were
observed in insect meal analysed regarding sh meal. Bukkens (1997)
reported signicant quantities of linoleic acid in the fatty acid content
of all analysed species of insect. As observed by other researchers
(Akinnawo and Ketiku, 2000; Beenakkers and Scheres, 1971;
Ekpo and Onigbinde, 2007; Finke, 2002, 2007; Katayama et al., 2008),
terrestrial insects do not contain EPA or DHA except for Chrysomya

F.G. Barroso et al. / Aquaculture 422423 (2014) 193201

199

Fig. 3. Differences between insect orders studied in the percentage of fat acids (using sh meal and soybean reference).

megacephala and Calliphora vicina, which have between 1.3 and 1.5%
EPA, far lower proportions than sh meal, which contains up to 14 to
16% EPA.
The lack of EPA and DHA in insects is one of the most important
limitations to its use in seawater sh feed, since it involves a limit in
their inclusion in aquafeed.
Nevetheless there are evidences that the fatty acid proles of insects
most likely reect the fatty acid composition of their food. In wild
Hetteracris Littoralis and Anacridium aegyptium individuals that
consume plants in the eld have a high amount of a-linolenic acid
(ALA, 18:3 n3), a precursor of the n-3 series, whereas three other
species of orthopterans, bred in captivity and fed only with our and
bran cereals, present with lower ALA, 18:3 n3. Finke (2002) has
achieved FA proles virtually identical to those obtained in this work
in Zophoba morio and Tenebrio mollitor, species bred in captivity. The
fatty acid content of Locusta migratoria determined in this experiment
is very different from that obtained by Beenakkers and Scheres

(1971), who measured 26% oleic acid (18:1 n9) and 21% ALA
(18:3 n3), whereas the results of this experiment show 45% oleic acid
and 5% ALA. These differences could be related to diet; Locusta used
in this experiment are from pet stores, whereas in the work of
Beenakkers and Scheres (1971), Locusta were provided with a diet of
reed, endive, or pear (supplemented with some reed). In addition,
these authors obtained a fair correlation between the percentages on
oleic and linoleic acid in the tri- and diglycerides of both diet and
body fat. These results indicate that lipid quality could be manipulated
by feeding, which amplies the nutritive values of insects meal. On
the other hand in this work we have not sampled any aquatic insect.
Freshwater insects have a high proportion of EPA because they ingest
freshwater algae, which generally contain ALA. EPA levels above 15%
as have been observed by Bell et al. (1994).
The data obtained in this experiment agree with Justi et al. (2003):
fatty acids content of insects is more dependent on diet, in contrast
with amino acids, more related to the taxon.

Fig. 4. Cluster analysis of fatty acids similarity among insect species, sh meal and soybean meal.

200

F.G. Barroso et al. / Aquaculture 422423 (2014) 193201

The comparison with sh meal and soy meal reveals lower levels of
n-3 and n-6 in insect meal.
Finally, it is interesting to note the following considerations:
The utilisation of insects has other advantages that cannot be ignored; insects do not compete with human resource and can be
reared on by-products or human waste as efcient biotransformers
to convert abundant low-cost organic wastes into animal biomass
that is rich in proteins and suitable for use in animal nutrition
(Ramos-Elorduy, 1999, 2005). Regarding soybean production,
which is largely oriented toward animal feed, insects require fewer
natural resources (i.e., land, water, fertiliser) than soybean, the
production of which could compete with human food production.
The current aquaculture production system, supported by sh meal,
is clearly unsustainable. As reported by the FAO (2010), capture
sheries have been rather stagnant or even declining in some
countries, particularly sheries of wild marine sh stocks; 3% are
under-exploited, 12% are moderately exploited, 53% are fully
exploited, 28% are over-exploited, 3% are depleted and 1% is recovering from depletion. This situation, together with the increase in
demand for sh, indicates that sh meal will become a more limiting
ingredient in both production and price. Therefore, it is essential to
obtain potential alternatives.

5. Conclusion
The data obtained in this work indicate an adequate nutritional composition of the insect meals evaluated, for inclusion in sh food. The
great variety of insect species, habitats, development stages, feeding
habits and other characteristics most likely affects insect nutritional
value and makes insect meal very interesting to study as an alternative
to sh meal.
Although insects generally present some characteristics that do not
match with the sh meal, the amino acid prole of the Diptera shows
that this group of insects could be a possible alternative protein source
to be used in aquaculture. Nevertheless, more studies are needed to
know the digestibility, chitin content and digestive effect, presence of
toxic, meal treatments (such as degreasing), adequate mixtures of different insect species or to modify the nutritional value of insects by
changing their diet or rearing condition. Insects can potentially play a
fundamental role in animal nutrition, so further studies are required
on their nutritional value in the context of their use in animal feed.
Acknowledgements
The authors are very grateful to the Consejera de Innovacin y
Ciencia, Junta de Andaluca (project AGR5273), Fondos Europeos de
Desarrollo Regional (FEDER Funds) and Campus de Excelencia
Internacional Agroalimentario y del Mar, Ministerio de Educacin,
by nancial support. The authors are thankful to Bioytech
(www.bioytech.com) for y samples (Diptera) analyzed in this
paper.
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