Po a ina s o Slo ak Jou nal o Food Sciences
Volume 11 460 No. 1/2017
Po a ina s o Slo ak Jou nal o Food Sciences
ol. 11, 2017, no. 1, p. 460-465
doi: h ps://dx.doi.o g/10.5219/779
Recei ed: 12 Ma ch 2017. Accep ed: 19 June 2017.
A ailable online: 14 July 2017 a www.po a ina s o.com
© 2017 Po a ina s o Slo ak Jou nal o Food Sciences, License: CC BY 3.0
ISSN 1337-0960 (online)
WELFARE OF THE MEALWORM (
TENEBRIO MOLITOR
) BREEDING WITH
REGARD TO NUTRITION VALUE AND FOOD SAFETY
Anna Adámko á, Ma in Adámek, Jiří Mlček, Ma ie Bo ko co á,
Ma ina Bednářo á, Lenka Kouřimská, Jose Skácel, E a Ví o á
ABSTRACT
Li es ock wel a e is an impo an condi ion o ob aining high-quali y and sa e ood. Acco ding o he legisla ion edible
insec s a e classi ied as li es ock; and o his eason i is necessa y o comply wi h he edible insec wel a e condi ions.
This a icle ocuses on selec ed wel a e condi ions o mealwo m (Teneb io moli o ) b eeding, wi h special ocus on he a
con en in luenced by di e en b eeding empe a u e (17 °C, 23 °C and 28 °C). Maximum a con en 24.56% was
obse ed a 23 °C. To ob ain maximum a con en his appea s o be he op imal b eeding empe a u e. Ano he e alua ed
aspec was he nu i ional s ess and a way o killing, and hei impac on a con en , which showed o dec ease wi h he
nu ien s ess. The mos decline was de ec ed owa ds he end o he obse a ion pe iod. The analysis showed ha in e ms
o p ese a ion o he a con en , he bes way is killing by eezing, due o he me abolism slowdown. We also analysed
he con en o hea y me als in a mealwo m la ae using cyclic ol amme y wi h subsequen e alua ion. In he measu ed
sample concen a ions o hea y me als did no exceed he maximum allowable concen a ion o hea y me als in his
commodi y. F om his poin o iew mealwo m appea s o be a sa e ood.
Keywo ds: wel a e; Teneb io moli o ; nu i ional s ess; way o killing; hea y me al
INTRODUCTION
Animal wel a e is a condi ion, when he animal
o ganism ies o deal wi h he su ounding (B oom,
1986). Wel a e is de ined as a s a e o ul ilmen o all
ma e ial and imma e ial condi ions, which a e
p e equisi es o he heal h o he animal, and a e also in
acco dance wi h i s en i onmen (Angelo ičo á and
Polačko á, 2015; Doležal, Bílek and Dolejš, 2004).
Webs e (2016) desc ibed he i e eedoms o animal
wel a e. I is eedom om hunge , hi s , discom o , pain,
inju y, disease, ea and dis ess, and he exp ession o
no mal beha iou ( an Huis e al., 2013). Acco ding o
he Regula ion (EC) No. 1069/2009 insec b eeding is
conside ed as b eeding o common li es ock. Because o
his i is necessa y o ollow he ules o insec wel a e as
well as wi h o he li es ock. Tha ’s why Eisemann e al.
(1984) sugges ed, ha insec should be gi en he bene i o
he doub ( an Huis e al., 2013).
Among he species wi h he g ea es po en ial as ood and
eed wi hin he Eu opean Union a e mealwo m (Teneb io
moli o ), gian mealwo m (Zophobas a a us), lesse
mealwo m (Alphi obus diape inus), g ea e wax mo h
(Galle ia mellonella), silkwo m (Bombyx mo i), house
c icke (Ache a domes icus) and A ican mig a o y locus
(Locus a mig a o a mig a o ioides) (EFSA, 2015).
Mealwo m (Teneb io moli o ) in gene al belongs o he
ood pes s (Sch oeckens ein, Meie -Da is and Bush,
1990; Wang, Liao and Chen, 2012), howe e , hanks o
i s nu i ional alues, easy b eeding and minimal
en i onmen al bu den i has a po en ial o become a ully-
ledged sou ce o p o ein and a o mankind (Wang,
Liao and Chen, 2012). Nu i ionally, i is impo an in
e ms o p o ein and a , and he e is a p esump ion o
good use in he ood indus y (Pa k e al., 2014). Ano he
mealwo m bene i could be biodeg ada ion o o ganic
was e o p o eins (Veldkamp e al., 2012). Based on he
abo e ad an ages, possibili ies o ea ing his species in
space a e being explo ed (Ka ayama e al., 2008).
F om he economical poin o iew, mealwo m b eeding
is cheap and as (Wang, Liao and Chen, 2012).
Acco ding o Li, Zhao and Liu (2013) i s li e cycle is
sho , egg s age las s 3 – 9 days, la al s age 26 – 76 days
and pupal s age 5 – 17 days. Rea ing usually akes place in
b eeding anks wi h eed a he bo om (o en ce eal meal,
milk powde and bone meal) (Hů ka, 2005). G ow h a e
and size o indi iduals is a ec ed by se e al ac o s,
including empe a u e, humidi y, ligh in ensi y,
composi ion o he eed and densi y o specimens wi hin
he b eeding anks (Wu e al., 2009).
One o he main ac o s in luencing he g ow h speed is
he empe a u e (Xu e al., 2012). Wi h g owing
Po a ina s o Slo ak Jou nal o Food Sciences
Volume 11 461 No. 1/2017
empe a u e he li e cycle sho ens. In 20 °C he leng h o
he li e cycle was 97 days, and in 32 °C only 60 days (Xu
e al, 2012). Howe e , wi h g owing empe a u e he
weigh o pupae and adul specimens ends o dec ease
om ce ain empe a u e le el (Kim e al., 2015).
Ano he ac o is he insec eed. Sui able eed is
necessa y o main aining good heal h and op imal
specimen pe o mance (Dussu ou e al., 2016). Howe e ,
eely li ing animals do no necessa ily ha e he access o
he eed ha e lec s hei nu i i e needs. The in luence o
he nu i ional composi ion o eed on he nu i ional alue
o insec s had been in es iga ed (Li, Zhao and Liu, 2013).
Nu i i e s ess o small b eeding space leads o
cannibalism (Wu e al., 2009) and dec eases he b eeding
yield. Killing is ca ied ou in di e en ways, mos
commonly by eezing, di ec g inding, o cooling and
subsequen killing by boiling. Me hods o killing insec s,
howe e , should be chosen so as o a oid insec su e ing
( an Huis, 2013). P io o he slaugh e , dead indi iduals
mus be so ed ou .
Due o inadequa e sa e y e iew o edible insec s as a
no el ood o humans in he EU, i is necessa y no only
o know he ules o b eeding and p o ide su icien
wel a e, bu also o know he e ec o ea ing insec s o
human heal h and sa e y isks (EFSA, 2015). EFSA
(2015) d aws a en ion o he lack o sa e y e iews o he
insec consump ion and a ious isks, including he
con en s o hea y me als (mainly Cd, Pb, Hg, and As) and
calls o se ing limi s o sa e consump ion.
This a icle ocuses on he impac o nu ien s ess as a
wel a e aspec , and ways o killing on he nu i ional alue
( a con en ) o he inal p oduc . Fu he mo e, he a icle
deals wi h he sa e y o edible insec s in e ms o he
con en o hea y me als (Cd and Pb), which ha e a
signi ican impac on human heal h.
MATERIAL AND METHODOLOGY
Ma e ial
Insec
La ae o mealwo m (Teneb io moli o ) we e used o
he analysis (Figu e 1). Samples we e bough in he pe
supplies s o e K mi a Hos i ice.
Feed
Whea b ans wi h he ollowing nu i ional alues we e
used as eed ( alues o 100 g o p oduc ): Ene gy:
1210 kJ / 292kcal, Fa 5.3 g, o which sa u a ed a y acids
0.88 g, ca bohyd a es 24.9 g, o which suga s 2.2 g, ib e
40.2 g a p o ein 16.2 g, sal 0.1 g. Company: Coun y Li e,
s. .o., Be oun 1.
Chemicals
Pe ol e he 40/65, p.a., CAS No.: [8032-32-4], Ing.
Pe Š ec – PENTA s. .o., P aha,
HNO3 65%, p.a., CAS No.: [7697-37-2], Ing. Pe
Š ec – PENTA s. .o., P aha,
H2O2 30%, p. a., CAS No.: [7722-84-1], Ing. Pe
Š ec – PENTA s. .o., P aha,
CdCl2 p. a. – M . 183,32, CAS No.: [10108-64-2],
Fluka analy ical, Sigma Ald ich,
PbCl2 p. a. – M . 278,11, Lachema, n. p., B no, CZ,
Deionized wa e – 18.2 MOhm cm, Milli-Q,
Millipo e.
All chemicals we e o analy ical eagen g ade o
equi alen analy ical pu i y.
Me hods
Insec p ocessing
In he i s expe imen , mealwo m la ae we e di ided
in o h ee expe imen al g oups. These expe imen al g oups
we e placed in a plas ic boxes in a he mos a (HS 62A,
Chi ana) by ea ing empe a u e o 17 °C, 23 °C and
28 °C. The g oups we e ed ad libi um. Be o e analysis,
la ae in he las and penul ima e ins a de elopmen ( he
ull leng h o he body jus be o e pupa ion) we e collec ed
om b eeding. Subsequen ly he la ae we e le o s a e
o 24 hou s and hen killed wi h boiling wa e (100 °C).
The p epa ed samples we e d ied a 105 °C, homogenized
and s o ed in a cold s o age box a 4 – 7 °C un il analysis.
Fo he second expe imen , wo g oups o mealwo ms
we e b ed in oom empe a u e 22 °C ±2 °C and di ided
by he nu ien s ess. The i s g oup was ed whea b ans
ad libi um du ing he whole es . The o he g oup was in
nu i ional s ess, which means wi hou eed o 27 and 39
days. Be o e analysis, la ae in he las and penul ima e
Figu e 1 La ae o mealwo m (Teneb io moli o )
Po a ina s o Slo ak Jou nal o Food Sciences
Volume 11 462 No. 1/2017
ins a de elopmen ( he ull leng h o he body jus be o e
pupa ion) we e collec ed om b eeding. Subsequen ly he
la ae we e le o s a e o 24 hou s. Each g oup was
hen di ided in o wo sub-g oups. The i s sub-g oup was
killed by eezing (-18 °C) in he eeze and he second
one was killed by boiling wa e (100 °C). Dead la ae
we e d ied a 105 °C, homogenized and s o ed in a cold
s o age box a 4 – 7 °C un il analysis.
Fa con en de e mina ion
The a con en de e mina ion was pe o med by
ex ac ion using Soxhle me hod (Soxhle , 1879) on he
Ge ha d Sox he m SOX414 (C. Ge ha d GmbH & Co.
KG, Ge many). App oxima ely 5 g o d ied and
homogenized samples (wi h he accu acy o 0.0001 g)
we e pu in o ex ac ion himbles and ex ac ed wi h 150
ml o pe oleum e he ia cold wa e ex ac ion (p og am:
70 °C o 120 minu es). The ex ac ion lask was hen
d ied a 103 °C and weighed un il a cons an sample
weigh was a ained.
Hea y me als con en
0.1 g o homogenized sample was pu in o a ial, and
hen 2 mL HNO3 wi h 65% concen a ion was added.
Me als we e being ex ac ed o 24 hou s a oom
empe a u e and hen hea ed o each he empe a u e
110 °C o 1 hou . Subsequen ly, 200 µL 30% H2O2 was
added and he sample was kep wa m o ano he 30
minu es. A e cooling he sample was dilu ed 5 imes wi h
deionized wa e ( / ) (18.2 MOhm cm, Milli-Q,
Millipo e). P io o he analysis he sample was dilu ed 10
imes using an ace a e bu e ( / ).
De ec ion o selec ed me als (Cd, Pb) was ca ied ou
using cyclic ol amme y wi hin he ange U = <-1000;
+400 >mV wi h scanning speed 10 mV s-1. Accumula ion
ime was cond = 45 s wi h po en ial Econd = -1000 mV. To
e alua e me als, analy ic elec ochemical s a ion
µAUTOLAB, Type III/ FRA 2 was used wi h NOVA 1.11
applica ion. Ag/AgCl Re e ence Elec ode Me ohm AG,
Swi ze land was used as a e e ence elec ode. P Rod
Elec ode Me ohm AG, Swi ze land, was used as
auxilia y elec ode. Wo king elec ode was c ea ed using
he hick laye me hod on a ce amic subs a e (Al2O3).
Senso size was 25.4 mm ×7.25 mm × 625 μm. The sil e
duc ou come was c ea ed by ESL 9562-G pas e (ESL
Elec oscience, England). Wo king elec ode wi h 3 mm
diame e was c ea ed using DuPon 7102 pas e (DuPon ,
USA). ESL 4917 pas e (ESL Elec oscience, England) was
used o c ea e he p o ec i e co e laye . Measu ed
cha ac e is ics we e de i ed and analysed in Excel 2013
(Mic oso Co po a ion, USA).
S a is ical analysis
Da a ob ained om chemical analysis was p ocessed
using MS Excel (Mic oso Co po a ion, USA), o
calcula e basic pe cen age o a con en . These da a was
hen p ocessed using he S a is ica 12 (S a So , Inc., USA)
applica ion.
Figu e 2 Fa con en in mealwo m (Teneb io moli o ) -dependency on he b eeding empe a u e (boxplo ).
Table 1 Fa con en in mealwo m (Teneb io moli o ) and i s dependency on he b eeding empe a u e.
Sample
Fa (%)
TM 17 °C
14.67
TM 23 °C
24.56
TM 28 °C
23.32
M
M ± SE
M ± SD
17 °C 23 °C 28 °C
Tempe a u e
12
14
16
18
20
22
24
26
28
30
Fa (%)
Po a ina s o Slo ak Jou nal o Food Sciences
Volume 11 463 No. 1/2017
RESULTS AND DISCUSSION
B eeding empe a u e is one o he mos impo an ac o s
a ec ing he de elopmen speed (Xu e al., 2012). In ou
s udy, we examined he a con en dependency on he
empe a u e (17 °C, 23 °C and 28 °C). Table 1 and Figu e
2 show ha he a con en a 17 °C is lowe han a 23 °C,
bu u he inc ease o he empe a u e o 28 °C did no
lead o g ea e change. These a e, howe e , he ini ial
esul s, which will be u he e i ied.
While di e en s udies show he gene al in luence o
empe a u e on he edible insec nu i ional alue, a ailable
sou ces do no s a e any speci ic dependence o nu i ional
alues on he b eeding empe a u e (Oonincx and an de
Poel, 2011). Xu e al. (2012) in es iga ed he op imum
empe a u e o b eeding mealwo m (Teneb io moli o )
and compa ed i e di e en empe a u es (20 °C, 23 °C,
26 °C, 29 °C a 32 °C). Thei esul s showed ha he
mealwo m de elopmen ge s as e wi h g owing
empe a u e. Also he numbe s o laid eggs g ew (max. a
29 °C) (Xu e al., 2012), howe e , he weigh o pupa and
adul dec eased (Kim e al., 2015). The change in weigh
and size o specimens in di e en empe a u es can
sugges he change o hei nu i i e alue. Role o
nu i ion is o p o ide he needed nu ien s in o he body
ia he eed, in o de o p ese e li e, g ow h,
ep oduc ion, good heal h and pe o mance. The body can
elie e he lack o ood (nu i ional s ess) by d awing
ene gy om adipose issue, mine al sa u a ion om
skele ons, ni ogenous subs ances sa u a ion o mo e
economical exc e ion o ce ain elemen s. The deple ion o
ce ain nu ien wi hou e illing may esul in dea h o he
indi idual. Lack o a s educes he iabili y, slows
g ow h, educes ep oduc ion, pe o mance and leads o
diseases; long- e m de iciency has le hal e ec s
(Ho niako á e al., 2010). To obse e he e ec o
nu i ional s ess, insec was di ided in o wo expe imen al
g oups. The i s one was ed ad libi um; he o he was in
nu i ional s ess by s a ing o 27 and 39 days. In he
second g oup he cannibalism occu ed mo e o en, as also
men ioned by E ens e al. (2012). Subsequen ly, bo h
g oups o s a ing insec s we e di ided in o sub-g oup
killed by eezing (-18 °C) and boiling wa e (100 °C). The
esul s o he a con en show ha wi h he leng h o
s a ing he a con en dec eases (see Figu e 3). A
di e ence was de ec ed be ween he g oups o bo h ways
o killing. This end became mo e signi ican owa ds he
end o he expe imen . I ’s supposed ha he eason is
dec easing o he a deposi s in insec bodies due o hei
consumma ion by basal me abolism (Na ion, 2015).
Changes in a con en in insec bodies as well as insec
beha iou we e obse ed also by (Dussu ou , 2016) in
an s. Dec ease o he a con en was de ec ed a e
educing he nu ien concen a ion in he die , when he
a io o p o eins o ca bohyd a es was inc eased, and when
he an s we e s a ing. Reg ession model shows ha he a
con en was de e mined almos exclusi ely by he
ca bohyd a e in ake. The e was also a change in he a
con en among a ious cas es (Dussu ou , 2016).
Howe e , nu i ional s ess can be caused no only by he
lack o eed as a whole, bu also by he lack o a speci ic
nu ien . Fo example Simpson a Raubenheime (2012)
s a e ha excessi e consump ion o ca bohyd a es leads o
obesi y when eed is low in p o ein wi h a io o
ca bohyd a es, while he lack o ca bohyd a es in he die
leads o a lack o ene gy.
Figu e 3 Mealwo m (Teneb io moli o ) a con en dependency on he leng h o s a a ion and he way o killing.
0
5
10
15
20
25
30
0 5 10 15 20 25 30 35 40
Fa con en (g.100 g-1)
Lengh o s a a ion (days)
F eezing
Boiling
Po a ina s o Slo ak Jou nal o Food Sciences
Volume 11 464 No. 1/2017
Some ways o killing insec , desc ibed by E ens e al.
(2012), a e conside ed humane, bu as he s a es, some
p ocesso s ejec hem o inancial easons. Bene i o
eezing, o example, is ha by pu ing insec in o he
eeze , i s me abolism slows down (hibe na ion), un il i
eezes. F eezing should be ca ied ou quickly o p e en
issue damage (D dák, 1989). Conside ing he nu i ional
s ess, he e was no di e ence be ween he ways o killing.
Howe e , Figu e 3 shows ha he g oup killed by eezing
had a highe a con en han he g oup killed by boiling
wa e . We suppose ha he loss o a in he second g oup
may be caused by a ex ac ion in o he boiling wa e .
When using he a o p o ec ion om he cold and eeze,
he losses we e smalle han wi h boiling. Hea y me al
concen a ion in ood and eed o animal b eeding is an
impo an opic o heal h sa e y and has an impac on he
consume s’ heal h (Cho anco á e al., 2014; Lukáčo á
e al., 2014). In ou esea ch we ocused on he de ec ion
o cadmium and lead in edible insec using ca bon
elec ode c ea ed wi h he echnology o hick laye s. A e
c ea ing he calib a ion cu es he cadmium and lead
concen a ion was e alua ed in mealwo m la ae
(Teneb io moli o ) in las and penul ima e ins a
de elopmen , b ed in 23 °C and ed by whea b ans ad
libi um. Bo h cadmium and lead concen a ion was below
he limi o de ec abili y o he used senso (de ec ion limi
is 2 µg.L-1 o lead and 3 µg.L-1 o cadmium). The senso
can be used o de ec he le els o cadmium and lead,
s a ed as a maximum limi in Regula ion (EC) No.
1881/2006 (Pb 0.5 mg.kg-1 ha is 2.41 µg.L-1 and Cd 4.46
µg.L-1). Al hough hese a e ini ial esul s, gained wi h
using senso wi h de ec ion limi s sligh ly below he
maximum allowable concen a ion in his commodi y, he
con en o cadmium and lead seems o be sa e o using
insec as human ood.
Poma (2017) e alua ed nine mine al elemen s in his
s udy. In mealwo m (Teneb io moli o ) he con en he
de ec ed was: Cd 0.06 mg.kg-1 and con en o Pb was
lowe han he de ec ion limi . The le el o hea y me als
e alua ed in his s udy was lowe han eques ed by he
Regula ion (EC) No. 1881/2006 and lowe o compa able
wi h o he commodi ies o animal o igin.
CONCLUSION
Ou wo k was ocused on he impac o wel a e on he
nu i ional alue and sa e y o he mealwo m (Teneb io
moli o ), as a po en ial ood sou ce. As an analysis o a
con en indica es, b eeding empe a u e – as one o he
wel a e ac o s – signi ican ly a ec s he a con en . O he
e alua ed wel a e ac o was nu i ional s ess, while he
expe imen al g oup loaded wi h nu i ional s ess had
lowe a con en . I can be concluded, ha nu i ional
dep i a ion a ec s no only he animal wel a e, bu also
nu i ional yield wi h a u he impac on he economic
aspec s o b eeding. Fo comme cially aised li es ock he
momen o dea h is an impo an pa o animal wel a e,
ha ing an impac on he nu i ional alue and quali y o he
mea ob ained. The way o killing also in luenced he
nu i ional alues o mealwo m la ae in ou s udy. F om
he iewpoin o a yield, killing by eezing can be
ecommended.
Al hough he ques ion o hea y me als con en is no pa
o wel a e, i is an impo an aspec o he ood sa e y.
Based on ou s udy, we can conclude ha hea y me al
con en o he analysed species was lowe han he
maximum pe mi ed le els o hea y me als in ood. F om
his poin o iew, he consump ion o mealwo m la ae is
sa e.
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Acknowledgmen s:
The a c icle was suppo ed by p ojec no. FEKT-S-17-3934
U iliza ion o no el indings in mic o and nano echnologies
o complex elec onic ci cui s and senso applica ions.
Con ac add ess:
Anna Adámko á, Czech Uni e si y o Li e Sciences P ague,
Facul y o Ag obiology, Food and Na u al Resou ces,
Depa men o Quali y o Ag icul u al P oduc s, Kamýcká
129, 165 21 P ague 6 – Suchdol, Czech Republic, E-mail:
[email p o ec ed]
Ma in Adámek, B no Uni e si y o Technology, Facul y o
Elec ical Enginee ing and Communica ion, Depa men o
Mic oelec onics, Technická 3058/10, 616 00 B no, Czech
Republic, E-mail: [email p o ec ed]
Jiří Mlček, Tomas Ba a Uni e si y in Zlin, Facul y o
Technology, Depa men o Food Analysis and Chemis y,
Va ecko a 275, 760 01 Zlin, Czech Republic, E-mail:
[email p o ec ed]
Ma ie Bo ko co á, Mendel Uni e si y in B no, Facul y o
Ag onomy, Depa men o Zoology, Fishe ies, Hyd obiology
and Ag icul u e, Zemědělská 1, 613 00 B no, Czech
Republic, E-mail: ma ie.bo ko co [email protected]
Ma ina Bednářo á, Mendel Uni e si y in B no, Depa men
o In o ma ion Technology, Zemědělská 1, 613 00 B no,
Czech Republic, E-mail: bedna o [email protected]
Lenka Kouřimská, Czech Uni e si y o Li e Sciences
P ague, Facul y o Ag obiology, Food and Na u al Resou ces,
Depa men o Quali y o Ag icul u al P oduc s, Depa men
o Mic obiology, Nu i ion and Die e ics, Kamýcká 129, 165
21 P ague 6 – Suchdol, Czech Republic, E-mail:
[email p o ec ed]
Jose Skácel, B no Uni e si y o Technology, Facul y o
Elec ical Enginee ing and Communica ion, Depa men o
Mic oelec onics, Technická 3058/10, 616 00 B no, Czech
Republic, E-mail: [email p o ec ed]
E a Ví o á, B no Uni e si y o Technology, Facul y o
Chemis y, MRC-labo a o y o bio echnology and
bioma e ials esea ch, Pu kyňo a 118, 612 00 B no, Czech
Republic, E-mail: [email p o ec ed]