Comparison of functional properties of

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thereof Ewelina Zieli■ska & Monika
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 LWT - Food Science and Technology 91 (2018) 168–174

Contents lists available at ScienceDirect

LWT - Food Science and Technology

journal homepage: www.elsevier.com/locate/lwt

Comparison of functional properties of edible insects and protein T

preparations thereof
Ewelina Zielińska∗, Monika Karaś, Barbara Baraniak
Department of Biochemistry and Food Chemistry, University of Life Sciences in Lublin, Skromna Str. 8, 20-704, Lublin, Poland

A R T I C L E I N F O A B S T R A C T

Keywords: This study investigated the functional properties of three species of edible insects: Gryllodes sigillatus, Schistocerca
Edible insects gregaria, and Tenebrio molitor. The water and oil holding capacity, solubility, and foaming and emulsion prop-
Entomophagy erties were evaluated. The protein solubility showed minimum values at pH 5. The highest water and oil holding
Functional properties capacity was noticeable for the T. molitor protein preparation (3.95 g/g) and for the G. sigilltus protein pre-
Protein preparations
paration (3.33 g/g), respectively. The G. sigillatus protein preparation also showed the highest foaming capacity,
foam stability, and emulsion activity (99.0%, 92.0%, and 72.62%, respectively), while the protein preparation
from S. gregaria exhibited the highest emulsion stability (51.31%). This study has shown that whole insects and
protein preparations thereof can be suitable for development of new food formulations.

1. Introduction
In the last decade, the interest of entomophagy has been con-
tinuously growing. Currently, insects are consumed by two billion
people worldwide and even insect foods have recently become available
in the US and Europe. More than 2100 insect species have been docu-
mented in literature as edible (Jongema, 2017). Moreover, insects are
still promoted as a good source of protein and the production of edible
insects in developing countries is supported by various institutions such
as the Food and Agriculture Organization of the United Nations.
However, the use of insects in food production requires further in-
vestigations at different levels, for example to search for opportunities
to use them in various forms. This may be necessary since Western
consumers may be reluctant to accept insects as a protein source
(Shelomi, 2015). In many countries, whole insects are often consumed
but they can also be processed to pastes and powders; furthermore,
insect proteins, fats, and chitin can be isolated before use in food pro-
ducts as well. This could be a useful way for increasing acceptability
among wary consumers. Edible insects can also be processed into a
more palatable form by grinding or milling. It is an easy way to obtain
high-protein insect flour with other valuable components such as vi-
tamins or minerals (Yi et al., 2013).
Several studies have shown that edible insects are a good source of
protein (Ramos-Elorduy, Moreno, & Camacho, 2012; Rumpold &
Schlüter, 2013; Zielińska, Baraniak, Karaś, Rybczyńska, & Jakubczyk,
2015) but there are only few data about the functional properties of
insect protein. These properties could be helpful to clarify the use of
insect powder or protein extracts in different food products, for ex-
ample bread, pasta, and dairy products.
Currently, many commercial food products are fortified in order to
increase their nutritional value. For example, ham is enriched with
protein derived from legumes and fruit juices are enriched with vita-
mins. Edible insects are a great material for food fortification for several
reasons. First of all, they are rich in protein of high biological value
with a good amino acid profile and a high level of digestibility.
Moreover, insects are a good source of a variety of micronutrients such
as minerals: copper, iron, magnesium, manganese, phosphorous, sele-
nium, and zinc and vitamins: riboflavin, pantothenic acid, biotin, and
folic acid (Ramos-Elorduy et al., 2012; Rumpold & Schlüter, 2013).
Their lipid profile is desirable for humans. They are a source of un-
saturated fatty acids, for example omega-3 (Zielińska et al., 2015).
Given their nutritional value, insects can be a good product for food
supplementation and entomophagy does not have to be associated with
the consumption of whole insects any more.
In this study, three species of insects (Tenebrio molitor, Schistocerca
gregaria, Gryllodes sigillatus) were selected, which are well known and
easy to breed in Europe; each of them belongs to a different order or
family and is bred widely in Europe. These species have also been re-
ported to have the biggest potential to be used as food and feed in the
EU (EFSA, 2015). Moreover, the nutritional value of these insects was

Abbreviations: G. sigillatus, Gryllodes sigillatus; S. gregaria, Schistocerca gregaria; T. molitor, Tenebrio molitor; TNBS, picrylsulfonic acid; OHC, oil holding capacity; WHC, water holding
capacity; FC, foaming capacity; FS, foam stability; EA, emulsion activity; ES, emulsion stability
∗
Corresponding author.
E-mail address: ewelina.ziel@tlen.pl (E. Zielińska).

https://doi.org/10.1016/j.lwt.2018.01.058
Received 30 October 2017; Received in revised form 17 January 2018; Accepted 19 January 2018
Available online 20 February 2018
0023-6438/ © 2018 Elsevier Ltd. All rights reserved.
E. Zielińska et al.
studied. The most important information for determination of the
functional properties is the protein content, and the studied species
contain 52.35, 76.0, and 70.0% of protein, respectively (Zielińska et al.,
2015). The physicochemical properties of proteins, protein size, and
flexibility play an important role in determining their functional
properties, for example small molecular weight proteins give very good
emulsion-forming abilities because of rapid diffusion to the interface.
Proteins are commonly used to improve the functional properties of
food compositions. In fact, the functional properties of proteins are
dependent on pH.
The aim of this study was to determine the functional properties of
flours and protein preparations obtained from edible insects. In this
study, the solubility, water and oil holding capacity, and foaming and
emulsifying properties were determined.
2. Materials and methods
2.1. Raw materials
The mealworms Tenebrio molitor (Linnaeus, Coleoptera:
Tenebrionidae) (larvae), locusts Schistocerca gregaria (Forskal,
Orthoptera: Acrididae) (adult), and crickets Gryllodes sigillatus
(Fabricius, Orthoptera: Gryllidae) (adult) were obtained from a com-
mercial supplier from Poland. All individuals of these species were
fasted for approximately 48 h to clear their gastrointestinal tract of any
residual food. For each species tested, approximately 0.5 kg of material
was frozen and lyophilized. The insects were ground in a laboratory
grinder.
2.2. Method for obtaining the protein preparation
Proteins were isolated according to the Girón-Calle, Alaiz, and
Vioque (2010) method with slight modification. Briefly, insect flour
was stirred for 1 h with 0.2% NaOH at a ratio of 1:10 (w/v), pH 11, at
room temperature. After centrifugation at 8,000g, precipitation of
proteins was carried out at the isoelectric point pH 4.5 and room
temperature. Precipitated proteins were centrifuged at 4 °C for
20 min at 8000 g and washed with distilled water. Afterwards, the
protein preparations were lyophilized and kept at −18 °C until further
analysis.
2.3. Solubility
The protein solubility was determined according to the method of
Castellani, Martinet, David-Briand, Guérin-Dubiard, and Anton (2003)
with a slight modification. The sample was dispersed in distilled water
and the pH of the mixture was adjusted to 2, 3, 4, 5, 6, 7, 8, 9, 10, and
11 using 1 or 6 mol/L HCl and 1 or 6 mol/L NaOH. The volume of the
mixture was adjusted to obtain the final concentration of protein
(10 mg/ml). Total protein content in the sample was determined after
solubilization of the sample in 0.5 mol/L NaOH. The mixture was
stirred for 90 min and centrifuged at 8,000g for 15 min. The protein
content in the supernatant was determined using the Bradford method
(1976). Protein solubility was calculated from the formula:
Solubility (%) = (Ps/Pt) × 100
where: Ps – protein content in the supernatant, Pt – total protein content
in the sample.
2.4. Water holding capacity
Water holding capacity (WHC) was determined according to the
method of Diniz and Martin (1997) with a slight modification. The
sample (0.5 g) was dispersed in 20 ml of distilled water and stirred with
a shaker at 540 rpm for 30 min. Afterwards, the dispersion was
169
LWT - Food Science and Technology 91 (2018) 168–174
centrifuged at 8,000g for 15 min. The precipitate was weighed and the
difference in the weight was calculated. The results were presented as
gram of water absorbed per gram of the sample.
2.5. Oil holding capacity
Oil holding capacity (OHC) was determined according to the
method of Haque and Mozaffar (1992) with a slight modification. The
sample (0.5 g) was added to 10 ml of vegetable oil and mixed for 30 s in
a vortex mixer. Afterwards, the dispersion was centrifuged at 8,000g for
15 min. The precipitate was weighed and the difference in the weight
was calculated. The results were presented as gram of oil absorbed per
gram of the sample.
2.6. Foaming properties
Foaming capacity (FC) and foam stability (FS) were determined
according to the method of Guo et al. (2015). Twenty milliliter of a 1%
sample was homogenized in a high shear homogenizer mixer (pol-eko
H500, Poland) at a speed of 16,000 rpm for 2 min. The whipped sample
was immediately transferred into a cylinder. The total volume was read
at time zero and 30 min after homogenization. The foaming capacity
and foam stability were calculated from the formula:
Foaming capacity (FC) (%) = [(V0eV)/V] × 100
Foam stability (FS) (%) = (V30 /V0) × 100
Where: V – volume before whipping (ml), V0 – volume after whipping
(ml), V30 – volume after standing (ml).
2.7. Emulsifying properties
Emulsifying properties were determined according to the method of
Wu, Wang, Ma, and Ren (2009). The sample was dispersed in distilled
water (1% w/v) and 15 ml of the dispersion were homogenized (pol-eko
H500, Poland) with 15 ml of vegetable oil at a speed of 20,000 rpm for
1 min. Afterwards, the samples were centrifuged at 3000 g for 5 min
and the volume of the individual layers were read. Emulsion stability
was evaluated by heating the emulsion for 30 min at 80 °C. Then, the
samples were centrifuged at 3000 g for 5 min. Emulsion activity and
emulsion stability were calculated from the formula:
Emulsion activity (EA) (%) = (Ve/V) × 100
Emulsion stability (ES) (%) = (V30/Ve) × 100
Where: V – total volume of tube contents, Ve – volume of the emulsified
layer, V30 – volume of the emulsified layer after heating.
2.8. The sensory evaluation
The panel for sensory analysis was composed of 75 members aged
from 21 to 30 years (58 women, 17 men). The characteristics of the
flours and protein preparations, such as color, consistency, smell, and
overall acceptability were evaluated on a scale of 1–5 (1–bad, 5–very
good).
2.9. Statistical analysis
All experiments were run in triplicate and the results were presented
as means ± standard deviation. Statistical analysis was performed
using the STATISTICA v. 10.0 for one-way analysis of variance
(ANOVA) and the differences of the means between the samples were
determined using the Tukey test. P-values below 0.05 were considered
significant.
E. Zielińska et al. LWT - Food Science and Technology 91 (2018) 168–174

3. Results and discussion A

Functional properties of proteins are determined by the specific 5

properties of their molecules such as size, structure, or configuration
(Kilara & Harwalker, 1996). In an earlier study, Zielińska, Baraniak, a

water holding capacity (g/g)

and Karaś (2017) obtained the protein profile of insect flour. The pro- 4
a
teins from three insect species exhibited a varied range of molecular
mass. The Schistocerca gregaria showed two major proteins with mole-
cular mass of ∼36 kDa and ∼97 kDa, Gryllodes sigillatus had ∼55.3 kDa 3
b b bc
and ∼116 kDa proteins, while the Tenebrio molitor protein profile did
not show dominant proteins. Nevertheless, the bands observed in the T.
molitor protein profile ranged from 6.5 to 95 kDa. The differences in the 2
molecular mass clearly differentiated the functional properties of the c
studied insect species.
1
Functional properties can be also associated with a varying amount
of protein and other constituents in flours. The protein content in the
studied species was as follows: T. molitor 52.35%, G. sigillatus 70.0%, 0
and S. gregaria 76.0%. The fat content was 24.7%, 18.23%, and 12.97%, Tenebrio molitor Gryllodes sigillatus Schistocerca gregaria
respectively, and the content of carbohydrates was 2.2%, 0.1%, and
1.7%, respectively (Zielińska et al., 2015). The amino acid and fatty
acid spectra for the studied species were presented in a previous study
(Zielińska et al., 2015).
B
3.1. Solubility
4

The results for the protein solubility are presented in Fig. 1. The a ab
protein solubility of all samples showed minimum values at around pH
oil holding capacity (g/g)

5 with values of 3% for T. molitor, 4% for G. sigillatus, and 8% for S. 3 c bc

gregaria. A significant increase in protein solubility was observed
around pH 8 for T. molitor and G. sigillatus, and around pH 9 for S.
gregaria. The highest solubility of all samples was noticeable at pH 11 d
2 d
(T. molitor – 97%, G. sigillatus – 96%, and S. gregaria – 90%), but a high
solubility value was shown also at pH 2 and 3 for T. molitor (86 and
52%, respectively) and S. gregaria (87 and 69%, respectively), and at pH
2, 3, and 4 for G. sigillatus (72, 65, and 57%, respectively). These results 1
correspond well with those obtained by Zhao, Vázquez-Gutiérrez,
Johansson, Landberg, and Langton (2016) in similar assay conditions
but for defatted T. molitor protein extraction. Generally, the insect
protein solubility was similar to data reported for legumes, for example 0
kidney bean flour (Wani, Sogi, Wani, & Gill, 2013), especially the Tenebrio molitor Gryllodes sigillatus Schistocerca gregaria
kidney bean globulin fraction (Mundi & Aluko, 2012) and other plants Fig. 2. Water holding capacity (A) and oil holding capacity (B) of insect protein pre-
like the Ginko biloba seed albumin fraction (Deng et al., 2011) or fe- parations (pale) and insect flours (dark). Different letters indicate significant difference
nugreek (El Nasri & El Tinay, 2007). It should be noted that the solu- (p < 0.05).

bility of the materials mentioned above was similar although the au-
thors used different dilutions of the samples and the protein was gels in designed food products. As a result, molecules in colloidal sys-
determined with different methods. Solubility is one of the most im- tems are homogeneously dispersed, which improves the interfacial
portant physicochemical and functional properties of protein and de- properties (Zayas, 1997).
pends on hydration and the degree of hydrophobicity of protein mo-
lecules (Sathe & Salunkhe, 1981). Good solubility of proteins is
important in many uses, mainly for formation of emulsions, foams, and 3.2. Water holding capacity

100 Fig. 2 shows the result of the water holding capacity. Higher water
90 holding capacity was noticeable for the protein preparations than the
80 whole insects and the highest water holding capacity was noted in the
70 Tenebrio molitor protein preparation (3.95 g/g), while the lowest value
solubility (%)

60 was noted for the whole ground T. molitor (1.29 g/g). This is important
50
information for the use of these forms in food industry. The big dif-
40
ference in water holding capacity between protein preparations and
30
20
insect flour might be a good indicator of the applications of these forms
10 for different food products. An opposite situation was observed in the
0 case of Schistocerca gregaria – similar WHC values were noted for the
0 2 4 6 8 10 12 protein preparation and the insect flour (2.31 g/g and 2.18 g/g, re-
pH spectively). This is also important information that could be helpful in
the analysis of the cost-effectiveness and benefits brought by the use of
Fig. 1. Protein solubility with changes at pH 2–11. Tenebrio molitor (square), Gryllodes one of the presented forms of insects. Protein isolates are obviously
sigillatus (triangle), Schistocerca gregaria (circle).
richer in protein than whole insects but do not contain vitamins,

170
E. Zielińska et al. LWT - Food Science and Technology 91 (2018) 168–174

Table 1
Functional properties of studied insect species and selected plant seeds rich in protein.

Insects Form WHC (g/g) OHC (g/g) FC (%) FS (%) EA (%) ES (%)

Tenebrio molitor whole 1.29 ± 0.19 1.71 ± 0.13 31.0 ± 1.41 26.0 ± 0.94 65.96 ± 1.5 27.59 ± 1.18
protein preparation 3.95 ± 0.2 2.74 ± 0.06 32.67 ± 0.94 30.33 ± 0.47 66.6 ± 2.16 51.31 ± 0.46
Gryllodes sigillatus whole 2.34 ± 0.28 2.82 ± 0.08 41.0 ± 1.41 34.67 ± 2.82 62.0 ± 1.25 31.65 ± 0.92
protein preparation 3.44 ± 0.13 3.33 ± 0.11 99.0 ± 1.41 92.0 ± 1.88 72.62 ± 1.9 38.3 ± 0.8
Schistocerca gregaria whole 2.18 ± 0.07 1.98 ± 0.16 22.33 ± 1.41 19.33 ± 0.94 69.17 ± 0.59 48.11 ± 0.57
protein preparation 2.31 ± 0.19 3.22 ± 0.16 32.0 ± 1.88 6.17 ± 0.71 67.78 ± 1.6 50.41 ± 1.99
Plant seeds
chickpea whole 1.19 ± 0.01 1.10 ± 0.02 52.00 83.0 61.14 ± 0.61 94.19 ± 1.64
lentil whole 1.33 ± 0.02 0.93 ± 0.00 80.00 99.0 65.75 ± 0.11 91.99 ± 4.75
soy whole 1.30 0.84 70.00 nd 18.00 nd
protein isolate 4.47 1.54 235.00 nd 25.00 nd
lupin protein isolate 1.68 1.43 89.29 43.91 59.94 95.78
fenugreek protein isolate 1.68 ± 0.01 1.56 ± 0.32 70.00 55.0 61.00 ± 0.13 61.00 ± 0.13
indian kidney bean whole 2.60 2.40 109.5 ± 1.8 70.0 nd nd
red kidney whole 2.25 ± 0.13 1.52 ± 0.11 45.70 ± 1.40 41.20 ± 1.80 55.00 ± 1.80 52.40 ± 1.80
small red kidney whole 2.65 ± 0.20 1.23 ± 0.08 38.20 ± 0.90 43.30 ± 1.60 60.50 ± 1.90 62.30 ± 2.20
peanut defatted flour 1.30 0.90 51.00 96.00 57.00 nd

Source: Siddiq, Ravi, Harte, & Dolan, 2010; Du, Jiang, Yu, & Jane, 2014; Piornos et al., 2015; Ma et al., 2017; Kinsella, 1979; El Nasri & El Tinay, 2007.
WHC: Water Holding Capacity, OHC: Oil Holding Capacity, FC: Foaming Capacity, FS: Foam Stability, EA: Emulsion Activity, ES: Emulsion Stability.

minerals, fatty acids, or chitin and their production is more expensive
than milling insects. Moreover, flour from S. gregaria can be a valuable
addition enriching bread with not only protein but also vitamins, mi-
nerals, or chitin. Due to the high WHC of this flour, it can be ad-
ditionally contribute to improvement of the selected properties of bread
products.
Omotoso (2006) studied the functional properties of Cirina forda
(Lepidoptera: Saturniidae) – one of the most widely eaten insects in
Southern Nigeria. The water holding capacity of dried ground insect
was 300% and this value is the most similar to the WHC of the Gryllodes
sigillatus protein preparation (3.44 g/g). Besides, WHC for the whole T.
molitor (1.29 g/g) is similar to that determined analogically by Omotoso
(2015) for the silkworm larvae and pupae (Bombyx mori) (175% and
115%, respectively). In turn, Zhao et al. (2016) reported the WHC for a
Tenebrio molitor protein extract to be 1.87 ml/g, while our studies
showed two times higher results (3.95 g/g). Probably these differences
result from the protein extraction method used by authors as well as the
insects' origin. Moreover, Bußler, Rumpold, Jander, Rawel, and
Schlüter (2016) reported the WHC of 0.8 g/g dry mass for T. molitor
flour, while our studies showed a value of 1.29 g/g, which may be
caused by the different method of flour production and different trial
conditions.
Among the insect flours, the highest WHC was noted in the G. si-
gillatus flour (2.34 g/g) and a similar WHC value was found for the S.
gregaria flour (2.18 g/g). This is probably a result of the high content of
hydrophilic amino acids in these insects (390.6 and 371.4 mg/g, re-
spectively) (Zielińska et al., 2015).
3.3. Oil holding capacity
The fat/oil holding capacity is physical entrapment of oil (Kinsella,
1979). The oil absorbing mechanism involves capillarity interaction,
which allows the absorbed oil to be retained. Hydrophobic proteins
play the main role in oil absorption. According to Sathe, Deshpande,
and Salunkhe (1982), the OHC can be related to the protein contents,
protein types, and the amino acid composition of proteins, in particular
to hydrophobic residues that interact with hydrocarbon chains in fat
molecules. Furthermore, Kinsella (1976) investigated that more hy-
drophobic proteins show superior binding of lipids, indicating that non-
polar amino acid side chains bind the paraffin chains of fats. Therefore,
the OHC of different insect flours and protein preparations thereof are
influenced by particle sizes, contents, composition and conformation of
protein ingredient. OHC plays an important role in enhancing the
mouth feel, the flavor retention, or improvement of palatability (El
Nasri and El Tinay, 2007). OHC is required in many food applications,
e.g. in bakery products, ground meal formulation, and meat substitutes;
therefore, it is suggested that the studied species of insects could be
used in food industry due to their high OHC.
The oil holding capacity of whole insects and protein preparations is
presented in Fig. 2. The lowest water holding capacity of the insect
flour coincided with the lowest oil holding capacity (T. molitor 1.29 g/g
and 1.71 g/g, respectively). This is probably related to the fact that T.
molitor contains substantially less protein than the other insect species
tested (52.35%) and considerably more fat (24.7%) (Zielińska et al.,
2015). The differences in OHC were possibly due to the different con-
formational characteristics, surface hydrophobicity, or lipophilicity of
these proteins (Deng et al., 2011). The low OHC value for T. molitor may
be the result of the lowest non-polar amino acid content in protein
among the tested species (257.6 mg/g) (Zielińska et al., 2015). Fur-
thermore, the protein preparation from T. molitor was shown to exhibit
the lowest oil holding capacity among all the preparations (2.74 g/g).
This value corresponds well with the value for a T. molitor protein ex-
tract obtained by Zhao et al. (2016) using a similar method to that used
in this study (2.33 g/g). T. molitor was also characterized by the lowest
OHC among the whole ground insects (1.71 g/g), while OHC for the T.
molitor flour prepared by Bußler et al. (2016) using a different method
was lower (0.6 g/g dry mass). In turn, G. sigillatus was found to have the
highest OHC among the whole insects and protein preparations (2.82 g/
g and 3.33 g/g, respectively). The S. gregaria protein preparation was
found to have an equally high value (3.22 g/g). Generally, the oil
holding capacity for the studied species range from 1.71 g/g to 3.33 g/g
and can be compared to the similarly determined OHC for silkworm
(Bombyx mori) larvae and pupae (252.18% and 284.87%, respectively)
(Omotoso, 2015), or legumes such as kidney bean flour (2.2–2.3 kg/kg)
(Wani et al., 2013). The studied species show higher OHC than almost
all plant seeds rich in protein listed in Table 1, which suggests an op-
portunity to substitute these materials in food products that require
high OHC values.
3.4. Foaming properties
Foam formation is governed by transportation, penetration, and
reorganization of molecules at the air–water interface. To exhibit good
foaming, a protein must be capable of migrating rapidly to the air–-
water interface, unfolding, and rearranging at the interface (Halling,
1981). Foaming properties are dependent on the proteins and some
other components, such as carbohydrates, present in the flours
(Sreerama, Sashikala, Pratape, & Singh, 2012). The factors influencing

171
E. Zielińska et al. LWT - Food Science and Technology 91 (2018) 168–174

A A

120 74

72 a
a
100 ab a
70 ab
ab

emulsion acƟvity (%)

foaming capacity (%)

68
80
66
b
60 64

b 62
40 c c
c 60
d
58
20
56
0 54
Tenebrio molitor Gryllodes sigillatus Schistocerca gregaria Tenebrio molitor Gryllodes sigillatus Schistocerca gregaria

B B

100 60
a
90 a a
50 a
80
emulsion stability (%)

70 b
foam stability (%)

40
60 c
50 30 c

40 b
bc 20
30 c
d
20 10
10 e

0 0
Tenebrio molitor Gryllodes sigillatus Schistocerca gregaria Tenebrio molitor Gryllodes sigillatus Schistocerca gregaria

Fig. 3. Foaming capacity (A) and foam stability (B) of insect protein preparations (pale) Fig. 4. Emulsion capacity (A) and emulsion stability (B) of insect protein preparations
and insect flours (dark). Different letters indicate significant difference (p < 0.05). (pale) and insect flours (dark). Different letters indicate significant difference (p < 0.05).

foam formation include surface hydrophobicity, location of hydro- Table 2

Sensory analysis of edible insect flours and protein preparations thereof.
phobic amino acid residues on the protein surface, presence of thiol
groups, cations and anions, carbohydrates and lipids. Moreover, the Insects Form Color Consistency Smell Overall
amphiphilicity of protein structures is a prerequisite for proteins with acceptability
good surface properties, including emulsifying and foaming. In food
Schistocerca protein 3.99a 4.10a 3.12a 3.79a
technology, foams are used to improve the texture, consistency, and
gregaria preparation
appearance of foods. whole 3.15b 3.23bc 3.33a 3.38b
The results of the foaming capacity and foam stability of the whole Gryllodes protein 3.29b 3.42bc 2.45b 3.16bc
insects and protein preparations are presented in Fig. 3. The highest sigillatus preparation
value of foaming capacity among both protein preparations and whole whole 3.30b 3.15bc 2.45b 3.03c
Tenebrio molitor protein 3.19b 3.55b 2.58b 3.19bc
insects was found for G. sigillatus (99% and 41%, respectively). Gen-
preparation
erally, higher foaming capacity was noted in the protein preparations. whole 3.11b 3.05c 1.75c 2.64d
The foam stability ranged from 19.33% to 34.67% for the whole insects
and from 6.17% to 99.0% for the protein preparations. Generally, the Different letters in the same column indicate significant difference (p < 0.05).
highest value among both the protein preparations and whole insects
was found in G. sigillatus (92.0% and 34.67%, respectively) and the (Mundi & Aluko, 2012). In turn, the lower FS of T. molitor and S. gre-
lowest value was noted in S. gregaria (6.17% and 19.33%, respectively). garia is probably due to the high level of sugars (2.2 and 1.7%, re-
These results are not consistent with the highest hydrophobic amino spectively) (Zielińska et al., 2015), which reduces protein-protein in-
acid content in the protein of the studied species, but it may be de- teractions and leads to formation of weak interfacial membranes that
pendent on the location of hydrophobic amino acid residues on the are unable to stabilize the foams (Mundi & Aluko, 2012).
protein surface in the case of G. sigillatus. The differences in FC of Furthermore, the analyzed species exhibit substantially higher va-
proteins may be due to their different conformational characteristic. lues of foaming properties than Cirina forda. The foaming capacity and
Globular proteins were found to have reduced ability to unfold at the foam stability of Cirina forda were 7.1% and 3%, respectively (Omotoso,
air-water interface, which limits the capacity to encapsulate air bubbles 2006). Moreover, whole giant cricket (Gryllidae sp.) powder was

172
E. Zielińska et al.
reported to have a FC of only 6% and a FS of 3.05% after 2 h which
were determined using a similar method to that employed in this study
(Adebowale, Adebowale, & Oguntokun, 2005). Acid-extracted protein
fractions from five different insects species, including the cricket
(Acheta domesticus) protein or the mealworm (Tenebrio molitor) protein
were shown to have poor or no foam capacity, over a range of pH, but
the foaming capacity was differently determined than in our study - the
solutions were aerated with nitrogen gas (Yi et al., 2013). In turn,
crickets (Gryllodes sigillatus) heated at 50 °C for 30 min were found to
have a FC of 100% with a FS of 90% after 1 h (Hall, Jones, O'Haire, &
Liceaga, 2017), which corresponds with our results for the G. sigillatus
protein (99% and 92%, respectively) obtained using a similar assay
method.
Currently, research is directed towards exploration of alternatives
for eggs, a common foaming agent, in food products (Hall et al., 2017).
The data from this study suggests that G. sigillatus protein preparation
exhibited excellent foaming properties; hence, it can be a desirable
foaming agent and has potential for such food applications.
3.5. Emulsifying properties
The results of the emulsion activity and emulsion stability of the
whole insects and protein preparations are presented in Fig. 4. The
differences between the emulsion activities and emulsion stabilities are
related to the amphiphilicity of the protein surface, protein contents
(soluble and insoluble), and other components. For emulsion activity,
the highest value was noted in the G. sigillatus protein preparation
(72.62%) with emulsion stability of 38.3%. Similarly, Omotoso (2015)
reported EA of 75% for silkworm B. mori but with lower ES (23%). The
emulsion activities for the whole insects were similar and ranged from
62% (G. sigillatus) to 69.17% (S. gregaria). S. gregaria was also char-
acterized by the highest emulsion stability (48.11%) among the whole
insects which may be associated with the highest protein content and
the highest amount of hydrophobic amino acids (398.3 mg/g)
(Zielińska et al., 2015). Furthermore, the relatively high content of
sugars is important (1.7%) (Zielińska et al., 2015) because some types
of polysaccharides can help stabilize the emulsion by increasing the
viscosity of the system (Wani et al., 2013). Generally, higher emulsion
stability was noted in the protein preparations and the highest value
was found in the T. molitor protein preparation (51.31%). This value
corresponds well with that obtained by Kim, Setyabrata, Lee, Jones, and
Kim (2016) with the use of an analogical method for T. molitor flour
(50.28%).
Currently, casein and whey protein are the most widely used protein
emulsifiers in the food industry but still alternative protein sources are
being sought (Phillips & Williams, 2011). The studied species show
similar or higher emulsion activity than plant seeds rich in protein
listed in Table 1 and they can be an alternative protein emulsifier in
existing foods as well as in new food formulations.
3.6. Sensory evaluation
The results of the sensory evaluation of the whole insects and pro-
tein preparations are presented in Table 2. In order to introduce insects
to food, in addition to the assessment of functional properties, sensory
evaluation should be considered. Color, consistency, smell, and overall
acceptability were evaluated. The S. gregaria protein preparation was
rated the best (3.99 for color, 4.10 for consistency, and 3.79 for overall
acceptability) except for the smell where the highest score was found
for whole S. gregaria (3.33). The worst scores in all categories for which
assigned to whole T. molitor (3.11 for color, 3.05 for consistency, 1.75
for smell, and 2.64 for overall acceptability). This low result of sensory
evaluation coincided with the poor functional properties. The T. molitor
protein preparation was evaluated better and similar to G. sigillatus
protein preparation. In turn, whole G. sigillatus and protein preparation
thereof received similar ratings. Generally, the protein preparations
173
LWT - Food Science and Technology 91 (2018) 168–174
were better rated and they exhibited better functional properties, which
makes them more useful in food industry.
4. Conclusion
Good protein solubility is often associated with its good functional
properties (Kinsella, 1976). The results of our study are in agreement
with this statement. Protein from G. sigillatus exhibited good solubility
in the widest range of pH and the flour and protein preparation thereof
were generally found to have the best functional properties among the
studied species.
In this study, we demonstrated that edible insects could be con-
sidered an alternative source of protein. The good solubility of the in-
sect protein in a wide pH range facilitates the varied use in food in-
gredient formulations - as a food additive in acid and alkaline food. Our
result show that insects have high water and oil holding capacity, high
emulsion activity, and moderate foaming capacity and foam stability;
therefore, they certainly can be used in food formulations requiring
these properties. It can also be concluded that edible insects can be a
good source of protein ingredient in food systems.
Funding
This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit sectors.
Conflicts of interest
None.
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 Dürer. The Holy Family
St. Anne, attended by St. Joseph and St. Joachim, receiving from
His Mother the Infant Jesus
 Size of the original woodcut, 9¼ × 6⅛ inches
The years 1510 and 1511 were the most prolific of all, and witnessed
the publication of other connected pieces, the Beheading of John the
Baptist and Salome bringing the Baptist’s Head to Herod, and then
the three little woodcuts, Christ on the Cross, Death and the Soldier,
and The Schoolmaster, which Dürer brought out on large sheets at
the head of his own verses, signed with a large monogram at the
end of all. The single sheets of 1511 include, besides the marvelous
Trinity already mentioned, the large Adoration of the Magi, the Mass
of St. Gregory, a St. Jerome in his Cell, which is the best, after the
celebrated engraving of 1514, of Dürer’s repeated versions of that
delightful subject; the Cain and Abel, which is one of the great
rarities; two rather unattractive Holy Families; and the beautiful
square Saint Christopher, of which many fine impressions are extant
to bear witness to its technical virtues. The average level of all the
work of the year 1511 is so astonishingly high, that it must be
regarded as the culminating period of the woodcuts, just as a slightly
later time, the years 1513-14, witnesses the climax of the
engravings. In the next few years Dürer’s time was much taken up
with carrying out the emperor’s important but rather tiresome
commissions for the Triumphal Arch and two Triumphal Cars, the
small one which forms part of the Procession, and the much bigger
affair, with the twelve horses and allegorical retinue, which did not
appear till 1522. All this group offers a rich field of research to the
antiquary, but is simply unintelligible without a learned commentary,
and appeals much less than the sacred subjects to the average
collector and lover of art, who cannot unearth the heaps of pedantic
Latin and German literature in which the motives by which Dürer was
inspired, if I may use the word, lie buried. Inspiration certainly
flagged under the influence of Wilibald Pirkheimer and other learned
humanists who encouraged Maximilian in his penchant for allegory,
and compelled Dürer, probably somewhat against his will, to use a
multitude of symbols, intelligible only to the learned, instead of
speaking directly to the populace in the familiar pictorial language
derived from old tradition but enriched and ennobled by his own
matchless art.
The later woodcuts are comparatively few in number. They include a
few that are primarily of scientific interest, such as the celestial and
terrestrial globes and the armillary sphere, besides the numerous
illustrations to Dürer’s own works on Measurement, Proportion, and
Fortification. But among them are the two splendid portraits made
from drawings now in the Albertina, the Emperor Maximilian of 1518
and the Ulrich Varnbüler of 1522. Of the former several varieties
exist, from no less than four different blocks, and it is now
established that the only original version is the very rare one in which
the letters “ae” of the word “Caesar” are distinct, not forming a
diphthong, and placed within the large “C.” The other cuts are all
copies, produced probably at Augsburg, the fine large one, with an
ornamental frame and the imperial arms supported by griffins, being
indisputably the work of Hans Weiditz. Only three impressions of the
original are known, in the British Museum, the Berlin
Kupferstichkabinett, and the Hofbibliothek at Vienna, in addition to
which the École des Beaux-Arts at Paris possesses a fragment
damaged by fire at the time of the Commune, when it was still in
private hands. It is more generally known that the handsome
chiaroscuro impressions of the Varnbüler date, like those of the
Rhinoceros, from the seventeenth century, the color blocks having
been added in Holland. The brown and green varieties belong to
different editions, distinguished by the wording of the publisher’s
address at the foot, which in the majority of cases has been cut off.
 Dürer. Saint Christopher
Size of the original woodcut, 8⁵⁄₁₆ × 8¼ inches
 Dürer. The Virgin with the many Angels
Size of the original woodcut, 11¹³/₁₆ × 8⅜ inches
The Virgin with the many Angels, of 1518, is one of Dürer’s most
accomplished woodcuts, and quite good impressions of it are
comparatively common to-day. The latest of his compositions of this
class, the Holy Family with Angels, of 1526, is, on the other hand,
extremely rare. Some critics doubt its being an authentic work of
Dürer, but in spite of certain rather eccentric and unpleasant
peculiarities in the drawing, I consider this scepticism unfounded.
Quite at the end of Dürer’s life comes that rather fascinating subject,
The Siege of a Fortress, unique among Dürer’s woodcuts in the tiny
scale on which its countless details are drawn. Of the many heraldic
woodcuts and ex-libris attributed by Bartsch and others to Dürer,
very few can be regarded as his genuine work, and most of these
are very rare. The best authenticated are his own coat of arms; the
arms of Ferdinand I in the book on Fortification; those of Michel
Behaim, of which the block is extant with a letter written by Dürer on
the back; the arms of Roggendorf, mentioned in the Netherlands
Journal, of which only one impression is known, and the arms of
Lorenz Staiber, of which the original version is also unique. There
can be no doubt that the Ebner book-plate of 1516 is by Dürer; the
much earlier Pirkheimer book-plate is intimately connected with the
illustrations to the books by Celtes, and cannot be regarded as a
certain work of the master himself, while the arms of Johann
Tschertte are also doubted.
It is a fortunate circumstance for the museums and collectors of to-
day that Dürer’s prints have always been esteemed, and his
monogram was held in such respect and so generally recognized as
the mark of something good that they have been preserved during
four centuries, while so much that was interesting was allowed to
perish because it was unsigned or its signature was not recognized
as the work of any one important. It may be paradoxical to say that
Dürers are common; few of them are to be had at any particular
moment when one wants to get them; but they are commoner than
any other prints of their period, and a large number of impressions of
some subjects must come into the market in the course of every ten
years. But the sort of Dürer the collector wants, the really beautiful,
fresh, clean impression, with the right watermark and genuine,
unbroken border-line, is not, and never has been, common. It is
surprising how few, even of the famous museums of Europe, have a
really fine collection of the woodcuts, perhaps because so many of
them were formed some generations ago in uncritical times, when
people were apt to think it enough if the subject was represented, in
whatever condition it might be. The first-rate proofs are scarce, and
getting scarcer every year; when they are to be had, they should be
grasped and treasured.
 SOME EARLY ITALIAN ENGRAVERS
BEFORE THE TIME OF
MARCANTONIO
By ARTHUR M. HIND
Of the Department of Prints and Drawings, British Museum
Author of “Catalogue of Early Italian Engravings in the British Museum,”
“Short History of Engraving and Etching,” “Rembrandt’s Etchings:
an Essay and a Catalogue,” etc.

F
IFTEENTH-CENTURY Italian engraving is not an easy hunting-
ground for the collector, but it is one of the most fascinating not
less for its own sake than for the difficulty of securing one’s prize.
From the time of Raphael onward Italian engraving presents an
overwhelmingly large proportion of reproductions of pictures, and
loses on that account its primary interest. But in the fifteenth and the
early sixteenth century, the engravers, though for the most part less
accomplished craftsmen, were artists of real independence. We may
in some cases exaggerate this independence through not knowing
the sources which they used, but the mere lack of that knowledge
adds a particular interest to their prints. Treated not only in virtue of
their special claim as engravings, but merely as designs, we find
something in them which the paintings of the period do not offer us.
In general, the presence and influence of one of the greater artistic
personalities of the time may be recognized, but seldom definitely
enough for us to trace the painter’s immediate direction. Mantegna is
the most brilliant exception of a painter of first rank who is known to
have handled the graver at this period. But forgetting the great
names it is remarkable how in the early Renaissance in Italy even
the secondary craftsmen produced work of the same inexpressible
charm that pervades the great masterpieces.
One of the most beautiful examples I can cite is the Triumph of
Bacchus and Ariadne, which is known only in the British Museum
impression. It has all the fascination of Botticelli’s style without being
quite Botticelli—unless the engraver himself is to account for the
coarsening in the drawing of individual forms. Mr. Herbert P. Horne,
the great authority on Botticelli and his school, thinks it is by
Bartolommeo di Giovanni (Berenson’s “Alunno di Domenico”). But
whether immediately after Botticelli or after some minor artist of the
school, there is the same delightful flow and rhythmic motion in the
design that one thinks of in relation to Botticelli’s Spring.

Triumph of Bacchus and Ariadne

After a design by a close follower of Botticelli, possibly by Bartolommeo di
Giovanni
“But whether immediately after Botticelli or after some minor
artist of the school, there is the same delightful flow and
rhythmic motion in the design that one thinks of in relation to
Botticelli’s Spring.... We could ill afford to lose the charm of
the early Florentine Triumph of Bacchus and Ariadne for all
the finished beauty of Marcantonio’s Lucretia, and it is still the
youth of artistic development, with its naïve joy and freshness
of outlook, which holds us with the stronger spell.”
Arthur M. Hind.
Reproduced from the unique impression in the British Museum
Size of the original engraving, 8⅛ × 22 inches
 The Assumption of the Virgin
Florentine engraving, in the Broad Manner, after a design by Botticelli
“Most important of all the contemporary engravings after
Botticelli is the Assumption of the Virgin.... An original study
 by Botticelli for the figure of St. Thomas, who is receiving the
girdle of the Virgin, is in Turin, and clinches the argument in
favor of Botticelli’s authorship. The view of Rome, a record of
Botticelli’s visit, is an interesting feature of the landscape.”
Arthur M. Hind.
Size of the original engraving, 32⅝ × 22¼ inches

Botticelli was in early life under the immediate inspiration, if not in the
very service, of the great goldsmith Pollaiuolo (witness his picture of
Fortitude in Florence). One almost expects in consequence that he
may at some period have tried his hand at engraving, but there is no
proof that he did anything besides supplying the engravers with
designs. His chief connection with the engravers was in the series of
plates done for Landino’s edition of Dante’s “Divine Comedy”
(Florence, 1481). Altogether nineteen plates (and a repetition of one
subject) are known, but although spaces are left throughout the
whole edition for an illustration to each canto, it is only in rare copies
that more than two or three are found. Even the fine presentation
copy to Lorenzo de’ Medici (now in the National Library, Florence) is
without a single plate, showing perhaps the small regard that was
paid to engraving for book decoration at that period. This lack of
appreciation and the difficulties (or double labor) the printers
experienced in combining copperplate impressions with type led
soon after this and a few other experiments of the period to the use
of woodcut as the regular mode of book illustration for well over a
century. Apart from the plates to this edition, Botticelli’s devotion to
Dante is shown in the beautiful series of pen drawings—in the most
subtly expressive outline—preserved at Berlin and in the Vatican. It
seems on the whole probable that they are later than the 1481
edition, so that we cannot point to the original drawings for the prints.
Most important of all the contemporary engravings after Botticelli is
the Assumption of the Virgin, the largest of all the prints of the period
(printed from two plates, and measuring altogether about 82.5 × 56
cm.). An original study by Botticelli for the figure of St. Thomas, who
is receiving the girdle of the Virgin, is in Turin, and clinches the
argument in favor of Botticelli’s authorship. The view of Rome, a
record of Botticelli’s visit, is an interesting feature of the landscape.
This engraving is produced in what has been called the Broad
Manner in contradistinction to the Fine Manner, e.g. of the Dante
prints. In the Broad Manner the lines are laid chiefly in open
parallels, and generally the shading is emphasized with a lighter
return stroke laid at a small angle between the parallels. Its aim is
essentially the imitation of pen drawing after the manner of such
draughtsmen as Pollaiuolo and Mantegna. The Fine Manner on the
other hand shows shading in close cross-hatching (somewhat patchy
and cloudy in effect in most of the early Florentine prints), and gives
the appearance of imitating a wash drawing.
The two manners may be well compared in the series of “Prophets
and Sibyls,” which exists in two versions, the earlier being in the
Fine, and the later in the Broad Manner. The first series shows a
craftsman who drew largely from German sources (putting a St. John
of the Master E. S. into the habit of the Libyan Sibyl). In the second
we have an artist who discarded all the ugly and awkward features
which originated in the German originals, and showed throughout a
far truer feeling for beauty and a much finer power of
draughtsmanship than the earlier engraver. Mr. Herbert Horne
suspects, rightly I think, that Botticelli himself directly inspired this
transformation of the “Prophets and Sibyls.”
Through our lack of knowledge of the engravers of this early period
in Florence we are driven to a rather constant use of the somewhat
unattractive distinctions of the Fine and Broad Manners. We may
claim, however, to have advanced a little further in the elucidation of
questions of authorship, though the great German authority on this
period, Dr. Kristeller of Berlin, would still keep practically all the early
Florentine engravings in an unassailable anonymity. This is of course
better than classing all the engravings of the period and school, both
in the Fine and Broad Manners, under the name of Baccio Baldini,
which has long been the custom. A certain “Baccio, orafo” has been
found in documents as buried in 1487, but there is practically nothing
to connect his name with the substance of our prints. We would not
on that account regard him as a myth, but are reduced at the
moment to Vasari’s statement that “Baldini, the successor of
Finiguerra in the Florentine school of engraving, having little
invention, worked chiefly after designs by Botticelli.” Considering the
fact that both Broad and Fine Manners (in all probability the output of
two distinct workshops) show prints definitely after Botticelli, we are
still in entire darkness as to the position of Baldini.
The Libyan Sibyl
From a series of the “Prophets and Sibyls,” engraved in the Fine
Manner of the Finiguerra School
Size of the original engraving, 7 × 4¼ inches
 The Libyan Sibyl
From a series of the “Prophets and Sibyls,” engraved in the
Broad Manner of the Finiguerra School
Size of the original engraving, 7 × 4¼ inches
With regard to an important group of Fine Manner prints, Sir Sidney
Colvin has given strong reasons for the attribution to Maso
Finiguerra, made famous by Vasari as the inventor of the art of
engraving. Considering Vasari’s evident error in regard to the
discovery of engraving (for there were engravings in the north of
Europe well before the earliest possible example of Finiguerra),
modern students have been inclined to regard Finiguerra as much in
the light of a myth as Baldini. But there is no lack of evidence as to
his life and work, and without repeating the arguments here, which
are given in full in Sir Sidney Colvin’s “Florentine Picture-Chronicle”
(London, 1898), we would at least state our conviction that a
considerable number of the early Florentine engravings, as well as
an important group of nielli, must be from his hand. Vasari speaks of
him as the most famous niello-worker in Florence, and he also
speaks of his drawings of “figures clothed and unclothed, and
histories” (the “figures” evidently the series traditionally ascribed to
Finiguerra in Florence, but now for a large part labeled with an
extreme of timidity “school of Pollaiuolo”; the “histories,” probably the
“Picture-Chronicle” series, acquired from Mr. Ruskin for the British
Museum). Then considering Vasari’s fuller statement that Finiguerra
was also responsible for larger engravings in the light of a group of
Florentine engravings which correspond closely in style with many of
the only important group of Florentine nielli (chiefly in the collection
of Baron Édouard de Rothschild, Paris) as well as with the Uffizi
drawings, we can hardly escape the conviction that Vasari was
correct in his main thesis. A curiously entertaining side-light is given
by one of these engravings, the Mercury for the series of “Planets.”
Here we see the representation of a goldsmith’s shop in the streets
of Florence, stocked just as we know from documents Finiguerra’s to
have been. And the goldsmith is evidently engaged in engraving, not
a niello, but a large copperplate.
 The Planet Mercury
Florentine engraving in the Fine Manner, attributed to
Maso Finiguerra, or his school
“A curiously entertaining side-light is given by one of these
engravings, the Mercury for the series of ‘Planets.’ Here we
see the representation of a goldsmith’s shop in the streets of
Florence, stocked just as we know from documents
Finiguerra’s to have been. And the goldsmith is evidently
engaged in engraving, not a niello, but a large copperplate.”
Arthur M. Hind.
Size of the original engraving, 12¾ × 8⁹⁄₁₆ inches