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Effect of population density and photoperiod on larval growth and

reproduction of Tenebrio molitor (Coleoptera: Tenebrionidae)

Article  in  International Journal of Tropical Insect Science · January 2022

DOI: 10.1007/s42690-021-00707-0

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International Journal of Tropical Insect Science
https://doi.org/10.1007/s42690-021-00707-0

ORIGINAL RESEARCH ARTICLE

Effect of population density and photoperiod on larval growth

and reproduction of Tenebrio molitor (Coleoptera: Tenebrionidae)
Jamaa Zim1   · Mohammed Sarehane1 · Ahmed Mazih1 · Patrick Lhomme2,3 · Rachid Elaini4 · Rachid Bouharroud5

Received: 22 November 2020 / Accepted: 24 November 2021

© African Association of Insect Scientists 2021

Abstract
The mealworm Tenebrio molitor (Coleoptera: Tenebrionidae) is the most consumed insect in the world. This study aims
to optimize the space in the mass-rearing facilities of this insect, as well as to evaluate the effect of photoperiod on the
reproduction and growth of the larvae. The two cross-over factors studied were photoperiods regimes (8L:16D and 0L:24D)
and four density treatments (0.25; 0.75; 1; 1.5 ind/cm2) under rearing conditions of 28 ± 1 °C and 70 ± 5%relative humidity.
Statistical analysis showed that density and photoperiod (P > 0.05) had no effect on pupal development. Moreover, popula-
tion density and photoperiod had no effect on pupal development and adult survival. However, average fertility was affected
by population density and the optimal population density was 0.25 adults/cm2.Photoperiod had no effect on the fertility
of T. molitor. Regarding total fecundity, there is no interaction between the two factors. The fecundity of T. molitor was
significantly affected by population density. The highest fecundity was obtained at 1.5 adult/cm2. The optimal combination
of photoperiod and density for larval development was of 0.25 ind/cm2 with 8 h of light per day. The conversion rate was
not affected by the factors studied. These findings enable to optimize the mass-rearing of T. molitor and reduce the cost and
environmental impact of these facilities.

Keywords  Mass-rearing · Edible insects · Yellow mealworm · Insect farming

Introduction cattle, are inefficient and require unsustainable costs and

activities that are harmful to the environment (De Vries and
Since the world population is continuously increasing, de Boer 2010). Insect-based sources of proteins and foods
the demand for protein alternatives for food and feed is ris- have been proposed to reduce the detrimental effect of meat
ing (Tilman and Clark 2014). As a result, the world is under processing activities on the ecosystem while satisfying popu-
immense pressure to satisfy human nutritional needs (Stehfest lation demand (Wegier et al. 2018). Insects show high levels
et al. 2009). Animal farming pastures and animal feed crops of bioconversion of agricultural and food waste residues (Sun-
account for more than two thirds of all arable lands (Steinfeld Waterhouse et al. 2016) and therefore represent ideal sources
et al. 2006). Meat and other proteins from livestock, particularly of proteins to help improve protein conversion efficiency (van
Huis 2017).
There are more than 2000 edible species of insects world-
* Jamaa Zim wide, however, only a few are commercially (Megido et al.
[email protected] 2014; Sogari et al. 2019; Bordiean et al. 2020). produced
1 (Jongema  2015). Among them, the yellow mealworm
Agronomic and Veterinary Institute Hassan II, Agadir,
Morocco Tenebrio molitor (Coleoptera: Tenebrionidae) is the most
2 consumed insect in the world. The larvae of T. molitor are
Entomonutris, Marrakech, Morocco
already used as pet food, providing promising alternative
3
Laboratory of Zoology, University of Mons, Research for animal feed (Finke 2002; van Huis 2013). Not only are
Institute for Bioscience, Mons, Belgium
mealworms suitable as animal feed, but also often consid-
4
IPM Department, Omnium Agricole du Souss, Agadir, ered suitable for human feed (Li et al. 2013, 2015). Meal-
Morocco
worms have a higher nutritional value than beef and chicken
5
Integrated Crop Production Unit, Centre Régional de La since they contain all essential amino acids (Rumpold and
Recherche Agronomique d’Agadir (INRA), Agadir, Morocco

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Vol.:(0123456789)
 International Journal of Tropical Insect Science

Schlüter 2013). The yellow mealworm is already one of the and height = 12 cm) containing 70 g of wheat bran and 30 g
most commonly industrially reared insect species in Europe of crushed dairy cows feed (15% of crude protein content)
Mealworms are inexpensive, easy to rear and show much manufactured by (ALF ISSEN company).
less harmful effects on the environment compared to farm The boxes were amended with a piece of fresh potato to
animals (Wang and Zhang 2015). Many substrates from the provide moisture each 4 days. The rearing chamber condi-
agricultural, baking, and brewing industries can be con- tions were maintained at a temperature of 28 ± 1 °C, 70 ± 5%
verted by this species into biomass (Oonincx et al. 2015; RH and at optimal ventilation. After 5 ± 2 days, emerged
van Broekhoven et al. 2015). This insect has undergone adults were counted in each box. The eggs were collected
extensive research in order to validate its nutritious impor- every 10 days using a sieve that separates the adults from the
tance and susceptibility to toxic compounds (e.g. mycotox- substrate containing the eggs and incubated at the same con-
ins, pesticides, heavy metals) (Bordiean et al. 2020). Yellow ditions. The adults were returned to their relative boxes with
mealworms will most likely be used as food on a wide scale new substrate at the same proportions for the next egg-laying
in the near future, either as a whole or just for certain com- generation. After 40 days, the number and weight of the larvae
pounds (chitin, fatty acids, amino acids, proteins) (Bordiean as well as the weight of the unused substrate were calculated.
et al. 2020). The rearing chambers were separated by an opaque fabric
One of the major challenges for the insect-producing indus- to ensure two different photoperiod regimes 8L:16D (P1)
try in terms of achieving reliable, cost-effective, and sustain- and 0L:24D (P2) with 16 replicates per regime. For each
able insect production for food and feed has been the devel- photoperiod regimes, four insect densities were applied
opment of diets capable of sustaining and optimizing insect (D1 = 0.25; D2 = 0.75; D3 = 1 and D4 = 1.5 ind/cm2), which
growth and development (Jensen et al. 2017; Heckmann et al. respectively correspond to 20; 40; 80 and 120 individuals
2018). per box (four replicates per density).
The economic production parameters of mealworms
include reduced space need, commercial production capa-
Assessment of colony growth
bility, high conversion efficiency and relative use of organic
waste as a food source (Ramos-Elorduy et al. 2002).
The larvae were weighed in a weighing balance (SBA 32,
Adult density is a major factor impacting reproductive
0.1 mg, by SCALTEC). The experimental design adopted
success that can be easily manipulated to optimize egg pro-
was the completely randomized block.
duction in a mass rearing facility (Morales-Ramos et al.
After 40  days, larval number, larval weight and the
2012). Similarly, photoperiod is known to play an impor-
weight of remaining substrate were assessed following the
tant role affecting larval weight and larval development
experimental zootechnical parameters:
time, however this factor has been poorly investigated in
T. molitor. The aim of this research is to assess the impact Weight gain = (Final weight − Initial weight)
of both larval density and photoperiod on the reproduction
and larval growth of T. molitor to optimize the rearing sys- weight gain
Conversion rate = × 100
tem capabilities. Increasing T. molitor output efficiency will the initial weight of the feed − the final weight
benefit the different applications that are using the insect.
In addition to these zoological parameters, the duration
of pupation stage, emergence rate, total fecundity and aver-
Materials and methods age fertility (the number of eggs hatched per adult) were
monitored.
Colony maintenance total fecundity
Average fertility =
the number of adult females per box
The study was conducted in the entomology laboratory at
the Hassan II Agronomic and Veterinary Institute (Agadir, The calculation of the number of larvae and their weigh-
Morocco), with the following geographical coordinates: ing, as well as the weighing of the remaining substrate, was
30°21′12.0 "N 9°28′38.8 "W). made according to the same protocol every 10 days; the
The initial T. molitor colony was obtained from the "Inter- operation begins at 9:00 am over a period of 5–7 h and with
national Foundation for Wildlife Conservation" then mass- the help of 3 students. In order not to influence the results,
reared at the IAV-CHA entomology laboratory. To avoid we first proceed to the separation of all the larvae present in
heterogeneity in adult ages, nymphs (1–2 days old) were the boxes of the substrate.
collected from the initial stock. These homogeneous nymphs As for the collection of the eggs, the operation was done
were introduced in cylindrical plastic boxes (diameter = 10 every 10 days. First the new substrates used for oviposition

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International Journal of Tropical Insect Science

were prepared, then adults were separate at around 4:00 pm Results

using a sieve. This total operation did not exceed 2 h.
The duration of the pupal stage (from start of the trial Adult mortality rate
until adult emergence minus one day), is the average age of
the test nymphs in adults. The mortality rate ranged from 12 to 25%. The different
To determine the final emergence rate in each box, the treatments had no effect on mortality rate (GLM, 𝜒7,24
2
 =
following equation is used: 507.63, p = 0.056; Fig. 1).
Number of emerged adults per box
Emergence rate =
number of nymphs per box
∗ 100 Total fecundity

To measure egg fertility, we first harvested the eggs along Statistical analysis showed no interaction effect between
with their substrate every 10 days and incubated them in the density and photoperiod on total fecundity (GLM, 𝜒3,242
 =
rearing room for 40 days (the time for the larvae to hatch 1326.48, p = 0.11; Fig. 2). There was no significant differ-
and be visible for calculation). The sum of these harvests is ence between the photoperiod regimes (GLM, 𝜒1,29 2
=0.49,
added to calculate the number of larvae produced per adult p = 0.21) on the reproduction of T. molitor. However, a
during the cycle. strong difference was observed between densities (GLM,
The conversion rate is the ability of the insect to convert 2
𝜒3,27 = 30.29, p < 0.001; Fig. 2). The highest the densities
feed into larval biomass. A simple equation was used to cal- generated the highest number of hatched larvae.
culate it: the weight accumulated by the larvae divided by
the weight of substrate consumed. Average fecundity

Data analysis Our analysis showed no interaction effect between density

and photoperiod on the number of eggs laid per female
The statistical analyses were performed using R software (R (GLM, 𝜒3,24
2
 = 382, p = 0.34; Fig. 3) and no significant differ-
Development Core Team 2021). Data were analyzed using ence was observed between the photoperiods (GLM, 𝜒1,29 2
 =
ANOVA and generalized linear model (GLM, R function 121, p = 0.3; Fig. 3). However, there is a very highly signifi-
glm) with a Gaussian error distribution. Post hoc pairwise cant effect of density regimes on average fertility rate (GLM,
comparisons were made using Tukey’s HSD test (R function 2
𝜒3,26 = 35,110, p < 0.001; Fig. 3). The lower the density and
glht from the R package multcomp; (Hothorn et al. 2008)). the higher was the reproduction rate.

Fig. 1  Mortality rate of Ten-

ebrio molitor under different
conditions of photoperiods
(P1 = 8L:16D; P2 = 0L:24D)
and densities (D1 = 0.25;
D2 = 0.75; D3 = 1 and D4 = 1.5
ind/cm2). Box plots show the
mean (black square), median
(white line), and 25–75%
percentiles. Whiskers show all
data. No statistically signifi-
cant differences were detected
among treatments (GLM,
Tukey’s HSD test, p > 0.05)

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 International Journal of Tropical Insect Science

Fig. 2  Total number of eggs

laid by Tenebrio molitor
under different conditions of
photoperiods (P1 = 8L:16D;
P2 = 0L:24D) and densities
(D1 = 0.25; D2 = 0.75; D3 = 1
and D4 = 1.5 ind/cm2). Box
plots show the mean (black
square), median (white line),
and 25–75% percentiles.
Whiskers show all data. Letters
indicate significant differences
between treatments (GLM,
Tukey’s HSD test, p < 0.05)

Larval weight when the density was of 1.5 ind/cm2 than when the density
was of 0.25 ind/cm2 (Tukey’s HSD test, p = 0.024; Fig. 4).
Our data showed no significant interaction between density
and photoperiod on larval weight of larvae (GLM, 𝜒3,242
 = Conversion rate
768.32, p = 0.07; Fig. 4). There was no effect of photo-
period on larval weight (GLM, 𝜒1,292
 = 208.42, p = 0.16; The statistical analysis showed no interaction effect between
Fig. 4), however we observed an effect of density on larval photoperiod and density (GLM, 𝜒3,24 2
 = 0.009, p = 0.056;
weight (GLM, 𝜒3,24
2
 = 1107.64, p = 0.017; Fig. 4). Under Fig. 5) on conversion rates. We also found no significant
photoperiod P1 (8L:16D), the larvae weight was higher difference between densities (GLM, 𝜒3,24
2
 = 0.001, p = 0.091;

Fig. 3  Mean number of eggs

laid per adult female of Ten-
ebrio molitor under different
conditions of photoperiods
(P1 = 8L:16D; P2 = 0L:24D)
and densities (D1 = 0.25;
D2 = 0.75; D3 = 1 and D4 = 1.5
ind/cm2). Box plots show the
mean (black square), median
(white line), and 25–75%
percentiles. Whiskers show all
data. Letters indicate significant
differences between treatments
(GLM, Tukey’s HSD test,
p < 0.05)

13
International Journal of Tropical Insect Science

Fig. 4  Weight of larvae of
Tenebrio molitor after 30 days,
under different conditions of
photoperiods (P1 = 8L:16D;
P2 = 0L:24D) and densities
(D1 = 0.25; D2 = 0.75; D3 = 1
and D4 = 1.5 ind/cm2). Box
plots show the mean (black
square), median (white line),
and 25–75% percentiles.
Whiskers show all data. Letters
indicate significant differences
between treatments (GLM,
Tukey’s HSD test, p < 0.05)

Fig. 5) nor between photoperiods (GLM, 𝜒3,24

2
 = 0.0001, This inhibition could be explained by cannibalism asso-
p = 0.68; Fig. 5) on conversion rate. ciated with over population as shown in closely related
beetles such as the red flour beetle Tribolium castaneum
Discussion (Via 1999) and confused flour beetke Tribolium confusum
(Shostak 2014). (Morales-Ramos et al. 2012)reported that
The results indicate that increasing population density is the optimal density for mass-rearing was 0.08 ind/cm 2,
negatively correlated with fertility in mealworms. The three times less than the lowest density we used (0.25 ind/
high density inhibits reproduction or egg hatching rates. cm2). Moreover, the same study showed that fecundity was

Fig. 5  Conversion rates of
Tenebrio molitor under differ-
ent conditions of photoperiods
(P1 = 8L:16D; P2 = 0L:24D)
and densities (D1 = 0.25;
D2 = 0.75; D3 = 1 and D4 = 1.5
ind/cm2). Box plots show the
mean (black square), median
(white line), and 25–75%
percentiles. Whiskers show all
data. No statistically signifi-
cant differences were detected
among treatments (GLM,
Tukey’s HSD test, p > 0.05)

13
 International Journal of Tropical Insect Science

reduced under overcrowding conditions. The growth rate Funding  No funding was received to assist with the preparation of
of larvae is lower when density increases, which is due to this manuscript.
a reduction of food available. Low growth rate can also
be a consequence of reduced feed conversion efficiency Declarations 
(Weaver and McFarlane 1990). Our data also show that
Ethics approval  Not applicable.
increased density has a negative effect on adult fertility.
Our study contrasts with most studies usually showing an
Conflicts of interest  The authors have no competing interests to de-
opposite trend (Morales-Ramos et al. 2012; Berggreen clare that are relevant to the content of this article.
et al. 2018; Deruytter et al. 2019). However, the pattern we
observed was identified in other beetle species such as the
bark beetle Ips typographus (Anderbrant 1990) and the red
flour beetle Tribolium castaneum (Halliday et al. 2015). References
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