International Journal of Environmental Studies

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Efficacy of three vegetal powders against Sitophilus

granarius in stored wheat and the evaluation of
their effect on grain parameters

Mokhtaria Chelef, Houari Hemida, Abdelkrim Hassani & Keltouma Mazrou

To cite this article: Mokhtaria Chelef, Houari Hemida, Abdelkrim Hassani & Keltouma Mazrou
(2021) Efficacy of three vegetal powders against Sitophilus�granarius in stored wheat and the
evaluation of their effect on grain parameters, International Journal of Environmental Studies, 78:4,
679-695, DOI: 10.1080/00207233.2020.1845556

To link to this article: https://doi.org/10.1080/00207233.2020.1845556

Published online: 30 Nov 2020.

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 INTERNATIONAL JOURNAL OF ENVIRONMENTAL STUDIES
2021, VOL. 78, NO. 4, 679–695
https://doi.org/10.1080/00207233.2020.1845556

ARTICLE

Efficacy of three vegetal powders against Sitophilus granarius

in stored wheat and the evaluation of their effect on grain
parameters
Mokhtaria Chelef a, Houari Hemida b
, Abdelkrim Hassania
and Keltouma Mazrou a
a
Laboratory of Agro-Biotechnology and Nutrition in Semi-Arid Zones, Faculty of Nature and Life Sciences,
University of Tiaret, Tiaret, Algeria; bDepartment of Biomedicine, Institute of Veterinary Sciences, University
of Tiaret, Tiaret, Algeria

ABSTRACT KEYWORDS
Doses of 5,10,15, 20 and 25 g of three plant powders, Durum wheat; Atractylis
Atractylisgummifera rhizome (AGRP), Daphne gnidium (DGP) and gummifera; Thapsia
Thapsiagarganica (TGP), were added to 100 g of durum wheat to garganica; Daphne gnidium;
Sitophilus granarius
study their insecticidal effect and ability to preserve the agro­
nomic characteristics of stored grains against the attacks of
Sitophilus granaries durum wheat pest overa storage period of
6 months inTiaret district. Algeria. Our results showed that AGRP
and DGPcaused 100% mortality, andTGP induced 90%. LD50 and
LD90 values of 7.24, 8.51, 10.71 and12.88, 15.48, 26.91 g/100 g of
wheat were recorded respectively with AGRP, DGP and TGP. We
observed a highly significant reduction in the number of eggs laid
and offspring emergence, a decrease in weight loss and grain
damage, anda high germination percentage in the treated grains.
The three powders represent a promising alternative against
Sitophilusgranarius.

Introduction
In Maghreb countries, nutrition depends on various cereals and their derivatives. Cereals
form a major sector in Algeria’s agriculture. Wheat is the strategic cereal product in
Algeria for its importance in human and animal nutrition as well as in the national
economy. The production of cereals occupies about 80% of the agricultural area of the
country fallow lands included [1]. Secure post-harvest storage is the only way to ensure
the balance between the year’s harvest and continued consumption [2].
Inadequate storage conditions of grains lead to the presence of moulds, insects, and
pest rodents. Moulds can produce mycotoxins. Insects can reduce the quantity of stored
grain and damage what is left. Damage may occur in shipment also. Insects and pests
infest 11 to 26% of the world’s crops. They affect 8% of global grain production [3].
According to Shaaya and Kostyukovsky [4], 10 to 40% of stored grains are infested by
pest insects, decreasing the quality of the grain. According to an Algerian report of 2017,

CONTACT Mokhtaria Chelef mokhtaria.chelef@univ-tiaret.dz Laboratory of Agro-Biotechnology and Nutrition in

Semi-Arid Zones, Faculty of Nature and Life Sciences, University of Tiaret, Tiaret, Algeria
© 2020 Informa UK Limited, trading as Taylor & Francis Group

Published online 30 Nov 2020

680 M. CHELEF ET AL.

the Algerian Inter-professional Cereals Office (O.A.I.C.) recorded 35% losses in recent
years [2].
Sitophilus granarius (L.) (wheat weevil) is a beetle that causes extensive damage to
stored grains and economic losses worldwide. Although it feeds on several varieties of
cereals, wheat and barley are its main food sources [5,6]. Furthermore, Sitophilus
granarius is a universal primary pest that not only damages stored grains, but also
opens the door to a whole set of secondary and tertiary pests [7].
Generally, the protection of stored grains is carried out by applying insecticides or
fumigants [8]. Insecticides such as methyl bromide and phosphine are the primary
method of controlling Sitophilus granarius. Despite their rapid efficacy against dense
populations of insect pests, they can have adverse effects such as developing insecticide
resistance to pests, leaving toxic wastes in stores, causing the emergence of new pests and
causing pollution [9,10]. Therefore, it is vital to develop environment-friendly techniques
that can replace the highly toxic chemicals. Natural insecticides can be found.
Nature offers a real reservoir of potential compounds rich with secondary metabolites.
These potential compounds are able to serve as natural pest control solutions due to their
richness with secondary metabolites. Hence, the derivatives of aromatic plants can act as
bio-pesticides. Numerous studies have confirmed the efficacy of certain plants against
a wide variety of insects that damage stored grain [11]. The powdered leaves of aromatic
plants have confirmed their efficacy in reducing losses caused by insect pests of stored
grains [12].
The present work tries to valorise the powders of three local Algerian aromatic plants
(Atractylis gummifera, Daphne gnidium and Thapsia garganica) as bio-insecticide against
Sitophilus granarius.

Material and methods

Study area
The study area is the district of Tiaret in the west of Algeria. It is located in the Tell Atlas
in Algeria, which extends from the North of Algeria to the highlands in the centre and the
South (35 ° 22′15 N 1° 19′01E). It has a semi-arid climate. Agricultural activity is
dominant.

Place and duration of the study

This research was conducted at both the Agro-Biotechnology and Nutrition Research
Laboratory in semi-arid zones and the Plant Protection Laboratory of the University of
Ibn Khaldoun (Tiaret-Algeria) from July 2019 to January 2020.

Plant material
After harvesting, the selected plants (Table 1) were identified at the Faculty’s Plant
Improvement Laboratory. The freshly harvested samples were washed and shade dried
in a dry and ventilated place. Finally, the plants were reduced to a vegetable powder by an
electric grinder and stored in paper bags until use.
 INTERNATIONAL JOURNAL OF ENVIRONMENTAL STUDIES 681

Table 1. The evaluation of insecticidal properties of the selected plants.

Common
Scientific name Local name name Family Parts used Harvest period
Atractylis Addad Chardon à glu Asteraceae Rhizome December to January 2019
gummifera Choûk
el-eulk
Daphne gnidium Lazzaz Daphné garou Thymelaeaceae stems and leaves February to March 2019
Thapsia Adheryis Thapsia Apiaceae stems and leaves February to March 2019
garganica Bounafaâ Faux fenouil

Animal
The wheat weevil or Sitophilus granarius (Linnaeus, 1758) is a species of beetle belonging
to the family Dryophthoridae (Coleoptera: Curculionidae). We collected this pest from
seed stocks of affected durum wheat to conduct the biological tests. The breeding of the
targeted pest was accomplished in glass jars filled with durum wheat and covered with
a thin piece of muslin cloth. The jars were kept in a breeding chamber under
a temperature of 28 ± 3 °C and relative humidity of 75 ± 4% with alternating light-
dark periods of 12 h shifts. After 15 days, the adults were removed and placed in new jars
in order to have new offspring and ensure the homogeneity of the generations.

Treatments and experimental design

The research project was based on the findings of several authors who tested the
efficacy of plant-derived bioactive substances such as plant powders [13–16]. We
experimented with the efficacy of our chosen plants in a completely randomised design
(CRD) with three replicates for each plant powder to simulate the protection of the
uninfected grains against the weevil. Thus, we prepared ninety (90) jars; fifteen (15)
jars for each powder (Atractylis gummifera rhizome (AGRP)), Daphne gnidium (DG)
andThapsiagarganica (TG)):forty-five (45) jars in total, in addition to another 45 jars
serving as a control sample, where each powder has fifteen (15) jars. The jars contained
the same amount of durum wheat, a hundred (100)g but each one received a different
dose of each powder; 5, 10, 15, 20.25 g. Thereafter, we gently shook the jars for 2 to
4 minutes to ensure the distribution of the powder. Ten (10) pairs of Sitophilus
granaries aged 7 days were previously starved for 48 hours and used to infest each
treated jar. The control jars contained only durum wheat and 10 pairs of the insects.
The jars were stored in the breeding chamber at an ambient temperature of 28–30 °C
over a period of 6 months of experimentation. The temperature was monitored and
measured using a thermometer. In cold weather, the radiator was used to maintain the
ambient temperature.

Analyses and measurements

Biological parameters
Adult mortality. We calculated the adult mortality monthly for six months after the
initiation of treatment. The mortality percentages were corrected by Abbott’s for­
mula [17]
682 M. CHELEF ET AL.

CM ¼½ðMo MtÞ=ð100 MtÞ� � 100

(CM: Corrected mortality rate, Mo: Mortality rate in the treated jars. Mt: Mortality
rate in the control jars.)

Fecundity. To estimate the fecundity, grain staining of the seeds with Fuschinic acid
(distilled water solution containing 5% acetic acid and 0.5% of Fuschine acid) was
performed according to the method described by Holloway [18] to calculate the
number of egg-laying holes. The female fecundity was expressed by the number of
eggs laid.

The reduction percentage of egg-laying. The number of eggs laid in the treated and
untreated jars was calculated in order to estimate the reduction percentage of egg-laying.
The egg-laying reduction is a criterion for evaluating the efficacy of the powders tested in
reducing the infestation caused by Sitophilus granarius.The reduction percentage was
calculated according to the formula cited by Sabbour [19]:
Reduction rate ð%Þ¼ Ntr=Nc � 100
(Ntr: Number of eggs laid from the treated batch; Nc: Number of eggs laid from the
control batch.)

The emergence rate. The calculation of newly emerged adults was done monthly. They
were removed at each count from the jars until the end of the emergence of new offspring
from the last egg-laying.

The agronomic parameters

The percentage of grain weight loss. The weight loss was calculated after 6 months of
treatment using the following formula:
WL ð%Þ¼ðinitial weight-final weightÞ=ðinitial weightÞ � 100

The percentage of grain damage. The number of healthy and attacked grains was
calculated manually after six months of storage. We calculated the percentage of damage
according to the formula described by Pointel and Coquard [20].
PD ð%Þ ¼ ðNaÞ=ðNh þ NaÞ�100
(Na: Number of attacked grains. Ns: Number of healthy grains).

The germination capacity of the treated grains. To estimate the germination capacity of
the treated grains, 10 wheat seeds from each treatment were placed in Petri dishes
containing moistened cotton. The Petri dishes were kept in the laboratory at an ambient
temperature of 25 ± 5 °C and a humidity of 70%. After 12 days, the germination
percentage was expressed by the following formula:
ð%Þ seed germination ¼ ðNumber of germinated seedsÞ=ðtotal number of seedsÞ�100:
 INTERNATIONAL JOURNAL OF ENVIRONMENTAL STUDIES 683

Statistical analysis
The data obtained were statistically analysed using SPSS v.20 software and expressed as
the average ± standard error. The data were also statistically analysed using one-way
analysis of variance (ANOVA) followed by a Dunnett post hoc test for multiple compar­
isons between the control group and the treated groups. The reduction rate was analysed
using Tukey test. P values(p ≤ 0.05) were considered significant and highly significant
when (P < 0.01). The effect size (R) was calculated based on the mortality caused by the
three powders AGRP, DGP and TGP. The measure of the effect size (R) for two
independent groups according to Cohen [21] was carried out in post hoc analyses. The
Cohen effect size scale is: R = 0.8 (strong), R = 0.5 (medium), R = 0.2 (weak).

Results
Biological parameters
The effect on the mortality rate
Our results showed that the three powders affected the mortality rate. They confirmed
their insecticidal properties in a highly significant manner (p˂0.01) according to the dose
and the duration of the treatment compared to the control group (Table 2). From the

Table 2. Effect of different doses of AGRP, DGP and TGP powder on the mortality of Sitophilus
granarius.
Period (day)
30d 60d 90d 120d 150d 180d
AGRP
C. group 0,83 ± 0,00AA 0,00 ± 0,00AA 0,00 ± 0,00AA 0,00 ± 0,00AA 0,83 ± 0,00AA 0,83 ± 0,00AA
Dose 5 0,00 ± 0,00AA 5,00 ± 2.88AA 20,00 ± 2.88 BA 25,00 ± 2.88 BA 26,31 ± 3.03 BA 40,00 ± 2.88 BA
Dose 10 0,00 ± 0,00AA 10,00 ± 2.88AA 25,00 ± 5.00CA 40,00 ± 5.77CA 45,00 ± 2.88CA 50,00 ± 2.88CA
DA
Dose 15 25,00 ± 5.77 40,00 ± 2.88 DA 50,00 ± 5.00 DA 60,00 ± 5.00 DA 70,00 ± 5.00 DA 75,00 ± 2.88 DA
Dose 20 36,84 ± 3.03EA 45,00 ± 2.88EA 65,00 ± 7.63EA 80,00 ± 2.88EA 90,00 ± 5.00EA 100,00 ± 0,00EA
Dose 25 40,00 ± 5.77FA 60,00 ± 2.88FA 90,00 ± 2.88FA 95,00 ± 2.88FA 100,00 ± 0,00FA 100,00 ± 0,00FA
F value 28,86** 88,80** 52,16** 90,00** 130,187** 356,16**
R 0,96 0,98 0,98 0,98 0,99 0,99
DGP
AA AA
C. group 0,00 ± 0,00 0,00 ± 0,00 0,83 ± 0,00AA 0,83 ± 0,00AA 0,00 ± 0,00AA 0,83 ± 0,00AA
Dose 5 0,00 ± 0,00AA 5,00 ± 2.88AA 15,00 ± 2.88AA 15,00 ± 0,00AA 25,00 ± 2.88AA 30,00 ± 2.88AA
Dose 10 0,00 ± 0,00AA 5,00 ± 2.88AA 20,00 ± 2.88 BA 35,00 ± 5.00 BA 35,00 ± 2.88 BA 40,00 ± 5.00 BA
Dose 15 15,00 ± 2.88AA 25,00 ± 5.00AA 40,00 ± 5.00 BA 55,00 ± 5.00 DA 65,00 ± 5.00 DA 68,41 ± 5.26 DA
Dose 20 30,00 ± 5.77 DA 45,00 ± 5.00 DA 60,00 ± 2.88CA 75,00 ± 5.00 DA 82,81 ± 6.08 DA 95,00 ± 2.88FA
Dose 25 35,00 ± 2.88 BA 50,00 ± 2.88CA 70,00 ± 2.88 DA 85,00 ± 5.00EA 95,00 ± 2.88FA 100,00 ± 0,00FA
F value 30,80** 38,13** 75,38** 66,57** 92,01** 131,21**
R 0,96 0,97 0,98 0,98 0,98 0,99
TGP
AA AA
C. group 0,00 ± 0,00 0,83 ± 0,00 0,83 ± 0,00AA 0,83 ± 0,00AA 0,83 ± 0,00AA 0,83 ± 0,00AA
AA AA
Dose 5 0,00 ± 0,00 0,00 ± 0,00 5,00 ± 0,00AA 10,00 ± 2.88AA 15,00 ± 0,00 BA 20,00 ± 2.88 BA
Dose 10 0,00 ± 0,00AA 0,00 ± 0,00AA 5,26 ± 3.03AA 25,00 ± 5.77CA 30,00 ± 2.88CA 35,00 ± 2.88CA
Dose 15 5,00 ± 2.88AA 25,00 ± 2.88 DA 26,31 ± 6.07 DA 45,00 ± 2.88 DA 50,00 ± 5.77 DA 60,00 ± 5.00 DA
Dose 20 25,00 ± 2.88EA 40,00 ± 2.88EA 60,00 ± 5.00EA 65,00 ± 5.77EA 68,42 ± 3.03EA 85,00 ± 5.00EA
Dose 25 20,00 ± 2.88FA 30,00 ± 2.88FA 65,00 ± 0,00FA 80,00 ± 2.88FA 89,47 ± 0,00FA 90,00 ± 2.88FA
F value 45,60** 76,56** 70,39** 63,82** 131,64** 103,25**
R 0,97 0,98 0,98 0,98 0,99 0,99
According to the results of Dunnett’s test the means with the same letters in columns are not statistically significantly
different from the control group which carried the letter A. The means with different letters in the columns are
significantly different from the control group (lowercase letters statistically significant at (p < 0.05), capital letters
statistically significant at (p < 0.01)).
684 M. CHELEF ET AL.

third month and at the highest dose, the mortality averages recorded by AGRP, DGP and
TGP were 90 ± 5, 70 ± 5 and 65 ± 00 respectively.This toxicity persisted and increased
throughout the storage period to reach a mortality average of 100 ± 00 in the jars treated
with AGRP and DGP. Nevertheless, only TGP resulted in a rate of 90 ± 00 under the same
conditions. Moreover, according to the Cohen effect size scale, our plant powders
demonstrated significant efficacy against Sitophilus granarius with R = 0.99.

The effect on the emergence rate

The number of adults that emerged in the grains treated with the three powders indicated
a highly significant decrease (p˂0.01) depending on the dose and the storage time
compared to the control group (Table 3). A total emergence inhibition was reported
with AGRP (00 ± 00) after 150 days of storage, followed by DGP with (00 ± 00) and TGP
(1 ± 1) after 180 days of storage, where the adults in the control group were
(17.80 ± 0.83). The results revealed that the powders can slow down the biological
cycle of the insect expressed by a total absence of new offspring at the highest dose
(25 g/100 g of wheat). This effect differs from one plant to another depending on dose
and time except, for the AGRP, which demonstrated a strong efficacy. In the latter case,
the dose of 25 g/100 g of wheat annihilated the new offspring in the treated grains. The

Table 3. Effect of different doses of AGRP, DGP and TGP powder on the emergence of Sitophilus
granarius.
Period (day)
30d 60d 90d 120d 150d 180d
AGRP
C. group 17,40 ± 0.60AA 17,20 ± 0,37AA 16,80 ± 0,37AA 16,80 ± 0,37AA 17,20 ± 0,37AA 17,80 ± 0,37AA
Dose 5 11,40 ± 0.57 BA 9,00 ± 1.00 BA 9,00 ± 0,00 BA 8,00 ± 0.57 BA 6,00 ± 1.00 BA 5,00 ± 0.57 BA
Dose 10 10,00 ± 0.57CA 8,00 ± 0,00CA 8,00 ± 1.00CA 6,00 ± 0.57CA 6,00 ± 0,00CA 4,00 ± 0.57CA
Dose 15 7,00 ± 1.15 DA 7,00 ± 0.57 DA 5,00 ± 0.57 DA 4,00 ± 0.57 DA 4,00 ± 0,00 DA 3,00 ± 0.57 DA
Dose 20 5,00 ± 1.15EA 4,00 ± 0,00EA 3,00 ± 0,00EA 3,00 ± 0.57EA 1,00 ± 0.57EA 0,00 ± 0,00EA
Dose 25 4,00 ± 0,00FA 3,00 ± 1.00FA 2,00 ± 0.57FA 0,00 ± 0,00FA 0,00 ± 0,00FA 0,00 ± 0,00FA
F value 50,091** 89,025** 131,020** 182,972** 209,417** 303,211**
R 0,97 0,98 0,98 0,99 0,99 0,99
DGP
C.group 17,80 ± 0.58AA 17,20 ± 0,37AA 17,20 ± 0,37AA 17,40 ± 0,24AA 17,00 ± 0.44AA 18,20 ± 0,37AA
Dose 5 12,40 ± 0.57 BA 10,00 ± 0.57 BA 11,00 ± 1.00 BA 9,00 ± 1.15 BA 7,00 ± 1.15 BA 6,00 ± 0.57 BA
Dose 10 11,00 ± 0.57CA 10,00 ± 0.57CA 9,00 ± 0.57CA 8,00 ± 0,00CA 7,00 ± 0,00CA 6,00 ± 1.00CA
Dose 15 9,00 ± 1.00 DA 8,00 ± 1.00 DA 8,00 ± 0.57 DA 7,00 ± 0.57 DA 5,00 ± 0,00 DA 4,00 ± 0.57 DA
Dose 20 6,00 ± 0.57EA 5,00 ± 0.57EA 4,00 ± 0.57EA 3,00 ± 0,00EA 2,00 ± 0.57EA 1,00 ± 0.57EA
Dose 25 5,00 ± 0,00FA 5,00 ± 1.00FA 3,00 ± 0.57FA 2,00 ± 0,00FA 0,00 ± 0,00FA 0,00 ± 0,00FA
F value 63,894** 56,700** 88,025** 155,250** 146,160** 173,108**
R 0,97 0,97 0,98 0,99 0,99 0,99
TGP
C. group 18,20 ± 0,37AA 17,20 ± 0,37AA 16,80 ± 0,37AA 16,80 ± 0,37AA 17,00 ± 0.44AA 17,80 ± 0,37AA
Dose 5 14,00 ± 0.57 BA 13,00 ± 0.57 BA 13,00 ± 0.57 BA 12,00 ± 1.15 BA 12,00 ± 0.57 BA 11,00 ± 0.57 BA
Dose 10 13,00 ± 0.57CA 11,00 ± 1.15CA 10,00 ± 0.57CA 10,00 ± 0,00CA 9,00 ± 0.57CA 8,00 ± 0.57CA
Dose 15 11,00 ± 1.15 DA 11,00 ± 0.57 DA 9,00 ± 1,00 DA 8,00 ± 1,00 DA 7,00 ± 1.15 DA 6,00 ± 0.57 DA
Dose 20 8,00 ± 1.15EA 7,00 ± 0.57EA 5,00 ± 0.57EA 5,00 ± 1,00EA 3,00 ± 0.57EA 2,00 ± 0,00EA
Dose 25 6,00 ± 1,00FA 6,00 ± 0.57FA 3,00 ± 0.57FA 2,00 ± 0.57FA 2,00 ± 0,00FA 1,00 ± 0.57FA
F value 35,365** 47,987** 80,400** 58,817** 95,387** 198,528**
R 0,96 0,97 0,98 0,97 0,98 0,99
According to the results of Dunnett’s test the means with the same letters in columns are not statistically significantly
different from the control group which carried the letter A. The means with different letters in the columns are
significantly different from the control group (lowercase letters statistically significant at (p < 0.05), capital letters
statistically significant at (p < 0.01).
 INTERNATIONAL JOURNAL OF ENVIRONMENTAL STUDIES 685

effect size of the three powders demonstrates their efficiency in the elimination of the new
offspring of the insect with an R equal to 0.99.

The effect on the fecundity rate

Similarly, to the effect on mortality, the three powders tested caused a highly significant
reduction (p˂0.01) in the number of eggs laid. Owing to the dose and the duration of
the treatment, we noted a significant reduction in the number of eggs laid compared to
the control group (Table 4) after six months of storage. The lowest averages were
recorded at the dose of 25 mg/100 g of wheat. The averages were 5 ± 2, 10 ± 2.6 and
16 ± 2 in the jars treated with AGRP, DGP and TGP respectively.This decrease in egg-
laying was expressed by a decrease in fecundity of females where fecundity of 0.5, 1.4
and 1.6 was noted in the insects treated with AGRP, DGP and TGP under the same
conditions.

The effect on the reduction percentage of egg-laying

The reduction percentage in the number of eggs laid after 180 days showed a highly
significant decrease (p˂0.01) with averages of 3.34 ± 1.38, 7.12 ± 1.74 and
10.99 ± 1.11 in the jars treated with AGRP, DGP and TGP respectively (Table 4).
Hence, the tested powders ensured an egg-laying deterrence and a decrease in the
Sitophilus granarius offspring. These promising results were expressed by the pro­
tection and persistence provided by the powders during the storage period.
According to the Cohen scale [21], the three powders showed a large regressive
effect of fecundity expressed by the lower number of eggs laid with R between 0.97
and 0.99.

Agronomic parameter
Percentage of grain weight loss
According to Table 5, there is a highly significant reduction (p˂0.01) in the weight loss of
the grains treated with the three vegetable powders at different doses. It is also reported
that AGRP shows the highest efficacy with an average loss of (8 ± 1) at the dose of 25 g/
100 g of wheat. DGP and TGP recorded averages of (15 ± 2) and (28 ± 4) respectively
under the same treatment conditions. The recorded results were very low compared to
the control group where the grains lost 74.08 ± 3.43 of their weight. Therefore, these
results demonstrate that the effect size of these bio-pesticides is very significant according
to the Cohen scale with R = 0.99.

The percentage of grain damage

The results showed that the three powders were very effective in preserving the grains
against the Sitophilus granarius attacks. It was noted that the average number of perfo­
rated seeds in the different jars treated with AGRP, DGP, TGP was very significantly low
(p˂0.01) with averages of 9.27 ± 0.09, 11.27 ± 0.27, 14.54 ± 0.09 respectively, compared to
the control group (50.66 ± 1.94) (Table 5).The components of these powders were
responsible for the efficacy observed. The insecticidal propertiesrecorded wereattributed
to these powders with an effect size of R = 0.99.
 686
M. CHELEF ET AL.

Table 4. Effect of different doses of AGRP, DGP and TGP powder on fecundity and reduction percentage (RP) of fecundity in Sitophilus granarius.
Control group Dose 5 Dose 10 Dose 15 Dose 20 Dose 25 F value R
AGRP
Fertility 14,72 ± 0,26AA 3,00 ± 0,11 BA 2,80 ± 0,17CA 1,80 ± 0,17 DA 1,00 ± 0,11EA 0,50 ± 0,11FA 890,118** 0,99
Reduction ND 20,26 ± 0.63A 20,26 ± 0.92A 12,31 ± 1,08B 6,48 ± 0.71 C 3,34 ± 0.79D 83,89** 0,98
DGP
Fertility 13,98 ± 0,33AA 3,50 ± 0,05 BA 3,10 ± 0,15CA 2,40 ± 0,20 DA 1,40 ± 0,11EA 1,00 ± 0,15FA 510,152** 0,99
RP ND 25,93 ± 0,57A 23,57 ± 0.68A 16,89 ± 1.33B 9,26 ± 0.69 C 7,12 ± 1,00 C 85,403** 0,98
TGP
Fertility 13,92 ± 0,44AA 5,00 ± 0,20 BA 4,50 ± 0,05CA 3,00 ± 0,15 DA 2,00 ± 0,11EA 1,60 ± 0,11FA 281,023** 0,99
RP ND 38,43 ± 1.16A 35,00 ± 1,00B 21,40 ± 0.78 C 13,14 ± 0.58D 10,99 ± 0.64D 208,453** 0,99
According to the results of Dunnett’s test the means with the same letters in columns are not statistically significantly different from the control group which carried the letter A. The means with
different letters in the columns are significantly different from the control group (lowercase letters statistically significant at (p < 0.05), capital letters statistically significant at (p < 0.01).
Table 5. Effect of different doses of AGRP, DGP and TGP powder on weight loss (LWP)), damage percentage (DP) and germination percentage (GP).
Control group Dose 5 Dose 10 Dose 15 Dose 20 Dose 25 F value R
AGRP
LWP 72,80 ± 1.99AA 22,00 ± 1.15 BA 17,00 ± 1.52CA 12,00 ± 0.57 DA 10,00 ± 1.15EA 8,00 ± 0.57FA 332,311** 0,99
DP 58,85 ± 1.21AA 13,63 ± 0,26 BA 12,91 ± 0, 20CA 11,54 ± 0,10 DA 10,18 ± 0,21EA 9,27 ± 0,05FA 777,055** 0,99
GP 50,66 ± 1.94AA 83,33 ± 3.33 BA 86,66 ± 3.33CA 90,00 ± 0,00 DA 93,33 ± 3.33EA 96,66 ± 3.33FA 50,195** 0,97
DGP
LWP 74,93 ± 1.43AA 30,00 ± 1.15 BA 24,93 ± 1.15CA 20,00 ± 1.73 DA 17,00 ± 0.57EA 15,00 ± 1.15FA 370,675** 0,99
DP 65,34 ± 1.59AA 18,18 ± 0,10 BA 16,54 ± 0,15CA 14,54 ± 0,10 DA 12,91 ± 0,15EA 11,27 ± 0,15FA 528,122** 0,99
GP 45,33 ± 2.26AA 80,10 ± 5.75 BA 83,33 ± 3.33CA 86,66 ± 3.33 DA 90,00 ± 0,00EA 93,33 ± 5,05FA 37,581** 0,96
TGP
LWP 74,53 ± 1.18AA 45,00 ± 1.73AA 41,00 ± 2.30AA 36,00 ± 1.73AA 32,00 ± 1.73AA 28,00 ± 2.30AA 115,097** 0,98
DP 68,79 ± 1.94AA 23,63 ± 0,10 BA 20,45 ± 0,15CA 19,54 ± 0,10 DA 16,82 ± 0,10EA 14,54 ± 0,05FA 349,543** 0,99
GP 50,00 ± 1.05AA 73,00 ± 3.33 BA 76,66 ± 3.33CA 83,33 ± 3.33 DA 86,66 ± 3.33EA 90,00 ± 5.77FA 25,279** 0,94
According to the results of Dunnett’s test the means with the same letters in columns are not statistically significantly different from the control group which carried the letter A. The means with
different letters in the columns are significantly different from the control group (lowercase letters statistically significant at (p < 0.05), capital letters statistically significant at (p < 0.01).
INTERNATIONAL JOURNAL OF ENVIRONMENTAL STUDIES
687
688 M. CHELEF ET AL.

The germination capacity of the grains

According to Table 5, AGRP recorded the highest germination percentage with an
average of 96.66 ± 5.77. Secondly, TGP resulted in 93.33 ± 5.05 on average. Finally, the
DGP recorded an average of 90 ± 10. The results showed that the germination rate
increased in a highly significant manner (p˂0.01) compared to the control group, which
had the lowest germination rate. Hence, the tested powders had a positive impact on the
germination of the stored wheat grains. These powders demonstrated their ability to
protect the germination power of the grains with a strong effect expressed by large effect
size R = 0.99.

Discussion
The use of plant products as insecticides is a common practice in African countries
including Algeria. Such practices have encouraged researchers to study many plants for
their biological properties in particular the plants with insecticidal properties against
pests of stored grains. These kinds of plants are still used traditionally in Africa, Latin
America, and South-East Asia as an insecticide to protect stored products [22,23].
In this study, the obtained results demonstrate that the selected plant powders (AGRP,
TGP, and DGP) have a considerable toxic effect against Sitophilus granarius with toxicity
that varies according to several factors including the selected plant, the dose used, and the
exposure time. Accordingly, the rhizome powder of the Atractylis gummifera plant seems
to be the only plant that caused 100% mortality rate at the 20 g/100 g dose in the storage
period of 150 days. Daphne gnidium presented the same percentage after 180 days at
a dose of 25 g/100 g, whereas Thapsia garganica caused 90% mortality under the same
conditions. Consequently, these results suggest the possible application of these three
plants as an alternative for controlling the insect pests in stored grains, in particular
Sitophilus granarius.
Obeng-Ofori et al. [24] noted similar results in their study on the toxic effects of the
extracts of three medicinal plants Ocimum kilimandscharicum, Ocimum suave and
Ocimum keneyense. Obeng-Ofori et al [24] tested three plant powders against insects in
stored products throughout six months of storage. After their experiments, they concluded
that the three compounds camphor, eugenol,and 1.8 cineol were toxic against Sitophilus
granarius and Sitophilus zeamais [24]. The protective effect of Chenopodium ambrosioides
leaf powder was effective against Sitophilus granarius with a dose of 6.4% [22].
Gbaye et al [25] also reported that the powder of Eugenia aromatica caused 100%
mortality, whereas Piper guineense powder caused 90% mortality against Sitophilus
oryzae. The high concentrations of the Piper guineense and Zingiber officinale powders
increased the mortality rate of the rice weevil [26].
In the same manner, Akob and Ewete [27] demonstrated that the ash of the Eucalyptus
grandis leaves had a good effect against Sitophilus zeamais at a dose of 20 g/2 kg. Pegalepo
et al [28] studied the efficacy of Piper guineense powder against adults and larvae of
Sitophilus oryzae. The leaf powder of the wild sage Lippia geminata had a repellent effect
against Sitotroga cerealella, which can last nine months in India [29].
Similarly, Jawalkar [30] tested the effect of five organic extracts of Vitex negundo on
the larvae and the adults of Sitophilus granarius. He found that all the extracts were
efficacious against the fecundity of the insect and the emergence rate with an increased
 INTERNATIONAL JOURNAL OF ENVIRONMENTAL STUDIES 689

mortality rate up to 100% after 96 hours of storage. Besides, he noted a significant

decrease in the rate of attacked grains.
Adler et al [31] and Isman [32] noted that the chemical insecticide compounds
extracted from plants strengthen the biological activities of plants such as toxicity, growth
inhibition, persistence and the protective capacity of grains against insect pests.
There are some notable features to our tested plant AGRP of the Asteraceae family: the
plant’s underground part is found to be rich in secondary metabolites such as polyphe­
nols, flavonoids, catechetical tannins and anthocyanins. These secondary metabolites
have important biological activities such as toxicity without any existence of alkaloids in
the plant [33]. Bouabid et al [34] proved that the toxicity of Atractylis gummifera is not
caused by alkaloids but rather by two glycosides, atractyloside (ATR) and carboxy
atractyloside (CATR).
The use of the Atractylis gummifera has been reported since 1943 according to
Tattersfield et al. [35], who noted that the plant has been used in Morocco as a remedy
for malaria and as an insecticide. Similar observations were made on the powder of
certain Asteraceae against stored grain insects. In Egypt, certain asteraceae proved to be
toxic. Nenaah [36] noted that Sitophilus oryzae’s mortal efficacy on grains mixed with the
powders of three Egyptian Asteraceae (Achillea bibersteinii, A. Fragrantissima and
Ageratum conyzoides) increases the mortality rate up to 88.2, 73.6 and 64.4% respectively
at a dose of 20 g/kg. Glitho [37] noted that the Asteraceae species such as Laggeraalata, L.
pterodonta, Tageteserecta, Tridaxprocumbens, Piper guineense have been reported by the
African Network for their insecticidal effect against bruchids in tropical regions.
According to our results, the thymelaeaceae (Daphne gnidium) came second for its
toxicity against Sitophilus granarius. The thymelaeaceae obtained such toxicity because of
diterpene esters of tigliane, daphnane and its fungicidal, bactericidal, molluscciid and
especially larvicidal properties [38].The toxicity of Daphne gnidium against the insects
and its efficacy in reducing the fecundity and the egg-laying were an effect of the
Flavonoids [39]. But Bellakhdar [40] noted that the efficacy of Daphne gnidium was
owing to the effect of a resin composed of diterpene esters contained in the bark of the
plant.
Several authors have demonstrated the insecticidal power of Daphne gnidium. For
instance, Zineb [41] noted that the aqueous extract of the leaves of Daphne gnidium
reduced the activity of the four larval stages of Culex pipiens followed by the death of the
specimens at different extract concentrations: a very toxic treatment.
In a study conducted by Benhissen [42] on the larvicidal effect and reproductive
performance of Culex pipiens, the aqueous extract from the leaves of Daphne gnidium
(with a concentration of 100 g/L) caused larval mortality of 84.26%, with a decrease in
female fecundity of 50% compared to the control group where it reached 80%.
Kosini and Nukenine [43] have demonstrated the toxic and protective effects of the
thymelaeaceae Gnidia kaussiana seeds against Callosobruchus maculatus. Gnidia kaussi­
ana caused a total elimination of offspring emergence. These researchers also reported
that this protective effect lasted at least two months.
Concerning the Apiaceae Thapsia garganica, it has been shown in our study that
this plant is remarkably toxic against Sitophilus granarius. Likewise, Bouimeja et al
[44] noted that the phytochemical study of Thapsia garganica revealed the presence of
secondary metabolites, which are responsible for its different biological activities.
690 M. CHELEF ET AL.

These authors have also demonstrated the presence of flavonoids, saponins, tannins,
coumarins, terpenes but with an absence of alkaloids in the leaves of Thapsia
garganica in Morocco. But Alghazeer et al [45] noted the presence of alkaloids and
anthraquinones in addition to the metabolites found in the leaves of Thapsia garga­
nica from Libya, which confirms that the chemical composition of plants differs from
one region to another [46].
Alkaloids can exert an inhibitory effect on the larval development of stock pests such
as Tribolium Castaneum [15]. Flavonoids, alkaloids and tannins affect the digestion and
reproduction of insects by inhibiting the pests’ fecundity [47,48].
Moreover, the main biomolecules synthesised by Thapsia garganica are thapsivillo­
sins, thapsigargine, thapsigargicine and notrilobolide [49,50]. Thapsigargarine and thap­
sigargicine are the two major compounds of T. garganica for their important biological
properties such as cellular toxicity [51].
The insecticidal activity of our tested Apiaceae can be demonstrated in a comparison
with the toxic effect of other Apiaceae species on insects found in stored grains.
Ziaeeand Moharramipour [52] reported that the powder of the two Apiaceae,
Cuminumcy minum and Curum copticum was toxic against Sitophilus granarius
depending on the dose and time of exposure. Ebadollahi and Mahboubi [53] also
proved that the application of essential oil of Aziliaeryn gioides was toxic against
Tribolium Castaneum and Sitophilus granarius.
We studied the agronomic properties of the treated wheat grains with the powder of
the three tested plants to investigate their efficacy. We aimed to examine the efficacy of
the three powders in protecting the stored wheat. We observed whether these powders
protected the treated grains without causing any loss of weight or damage and whether
they affected the grains’germination capacity.
Our results demonstrated a highly significant reduction (p˂0.01) of weight loss in the
treated jars, compared to the control group, owing to the dose and storage time. But we
noted a low weight loss caused by AGRP at the doses of 5, 10, 15, 20, 25 g/100 g of wheat
after 6 months of storage. The AGRP generated percentages of 22, 17, 12, 10 and 8% of
weight loss, followed by DGP, which caused losses of 30, 24, 20, 17 and 15%. Finally, TGP
caused weight loss of 45, 41, 36, 32 and 24% under the same conditions. On the other
hand, the germination percentages of AGRP, DGP, TGP were 96.66 ± 5.77, 93.33 ± 5.05,
90.00 ± 10.00 respectively.
In the same context, several researchers studied the efficacy of local plants in protecting
stored grains and evaluated their impact on the grains’ agronomical parameters. Significant
mortality was recorded after the use of the Zingiber officinale, Garcinia kola and Ficus
exasperate powders as a bio-pesticide against Trogoderma granarium. These powders
protected the grains without damaging them or their germination capacity and with
a low percentage of weight loss [54]. Asawalam and Igwe [55] Asawalam and Onu [54]
and Islam et al. [56] noted that plant extracts such as plant powder have a remarkable effect
in reducing the weight loss of treated grains compared to the control groups. Carica papaya
powder was used as an insecticide for the protection of maize kernels against Sitophilus
zeamais and found to be toxic. It caused a decrease in egg-laying and insect population,
which confirms that it has components of toxicity against Sitophilus zeamais. It also reduced
the weight loss of the treated grains compared to the control groups with a percentage from
2 to 1.4% [57]. In another study, and during the application of the two powders of Piper
 INTERNATIONAL JOURNAL OF ENVIRONMENTAL STUDIES 691

guineense and Zingibar officinale, a low percentage of weight loss and damaged grains was
noted with an emergence inhibition, which confirms absolute protection of the maize
kernels against Sitophilus zeamais after forty-five (45) days of treatment [58].

Conclusion
The three vegetal powders have proved to be very effective in protecting the stored wheat
grains against Sitophilus granarius with persistent efficacy over time depending on the
dose applied and the plant used. The doses of 20 and 25 g/100 g of wheat are the optimal
doses. They recorded the highest mortality rate with the reduction of females’fecundity
and total emergence inhibition of new adults. Further, they did not alter the germination
capacity of the grains; they protected the grains from losing weight and from any damage
that may be caused by the insect. Therefore, the AGRP, DGP and TGP powders reduced
the harmful effects of the Sitophilus granarius on stored wheat with persistent toxicity.
These natural insecticides also preserved the grains’ agronomic characteristics.These
promising results show that the studied powders are an environment-friendly alternative
to synthetic insecticides, a bio-insecticide alternative.
It is desirable to reduce the dependence of agriculture on chemical pesticides,
because of their reported dangers. For example, Malathion and diazinon, two recently
introduced synthetic chemicals, are now classified as carcinogenic by the IARC and
the WHO. Therefore, research on bio-pesticides as alternatives to synthetic chemicals
and on the economics of scaling up bio-pesticides to commercial level should be
expanded.

Acknowledgments
The authors would like to thank Dr Labdelli Fatiha for helping to identify the insects; and also the
anonymous reviewers. .

Disclosure statement
The authors declare no conflict of interest associated with this publication and there has been no
financial support for this work that could have influenced its outcome.

ORCID
Mokhtaria Chelef http://orcid.org/0000-0001-5108-2008
Houari Hemida http://orcid.org/0000-0002-6353-008X
Keltouma Mazrou http://orcid.org/0000-0002-1004-6008

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