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Biology and life table parameters of Callosobruchus maculatus (F.) on Vigna

unguiculata (L.) Walp. fertilized with some mineral- and bio-fertilizers

Article  in  Journal of Stored Products Research · May 2022

DOI: 10.1016/j.jspr.2022.101978

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 Journal of Stored Products Research 97 (2022) 101978

Contents lists available at ScienceDirect

Journal of Stored Products Research

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

Biology and life table parameters of Callosobruchus maculatus (F.) on Vigna

unguiculata (L.) Walp. fertilized with some mineral- and bio-fertilizers
Fatemeh Hamzavi, Bahram Naseri *, Mehdi Hassanpour, Jabraeil Razmjou, Ali Golizadeh
Department of Plant Protection, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Adrabil, Iran

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

Keywords: Callosobruchus maculatus (F.) (Coleoptera: Chrysomelidae), a major pest of stored cowpea Vigna unguiculata (L.)
Cowpea Walp., causes critical losses by decreasing the grain weight, germination ability and nutritional quality.
Life cycle Improving host plant resistance by the application of appropriate fertilizers would be effective in reducing
Life table
C. maculatus infestation. The effects of some mineral- (triple superphosphate (TSP) and urea) and bio-fertilizers
Induced resistance
Fertilizer
(Bradyrhizobium japonicum, Pseudomonas putida, mycorrhizal fungi, and a mixture of them) were evaluated on the
susceptibility of stored cowpea grains to C. maculatus. Cowpeas fertilized with examined fertilizers were culti­
vated at farm conditions. Then, the mature, dry grains were harvested and used to investigate the pest’s life cycle
and life table characteristics under 28 ± 1 ◦ C, 65 ± 5% R.H., and total darkness. Developmental time of
C. maculatus on TSP-treated grains was shorter than on control and P. putida treated ones. However, the lowest
immature survival and fecundity (number of deposited eggs) was on TSP-fertilized grains. The intrinsic rate of
increase (r) and net reproductive rate (R0) were the lowest on the grains treated with TSP. The highest tannins
and starch content in the grains fertilized with TSP may be the critical reasons for their resistance to C. maculatus
in storage. Application of TSP fertilizer can be recommended to increase cowpea resistance to this pest.

1. Introduction
Cowpea Vigna unguiculata (L.) Walp., is a common legume produced
in tropical and subtropical zones of the world. It is a rich supply of
critical nutritional components and a low-cost protein source for people
in Asia and Africa (Phillips et al., 2003). Callosobruchus maculatus (F.)
(Coleoptera: Chrysomelidae), a widespread and oligophagous insect
pest of stored cowpeas, causes economic losses by reducing the cowpea
grain weight and quality (Khashaveh et al., 2011; Badii et al., 2013;
Castro et al., 2013). In storage, C. maculatus eggs are laid on the legume
grain surface, and hatching larvae feed on the inner endosperm, leaving
a hole where adult insects emerge. The whole life of the larvae and
pupae is spent inside a single grain (Furk and Hines, 1993). As a result of
the feeding damage caused by this insect, secondary pests or fungi may
enter the grain, lowering its nutritional quality (Hagstrum et al., 2012).
All stored grains can be lost in a few months due to the rapid develop­
ment, high reproductive capacity, short life cycle, and continual gen­
erations of C. maculatus (Turaki, 2012).
Farmers often use chemical insecticides and fumigants to protect
cowpea grains against C. maculatus during storage. However, these
compounds may have deleterious effects on human, stored grains, and
the environment (Isman, 2008). So, in recent years, a serious approach
has been developed to use safe alternative methods to manage stored
product pests such as C. maculatus. One of the eco-friendly alternatives is
the application of appropriate fertilizers, especially biofertilizers, to
induce plant resistance to herbivore insects (Hertlein et al., 2011; Naseri
and Hamzavi, 2021). A combination of genetic and environmental fac­
tors can determine plant resistance to phytophagous insects. For
instance, non-protein antimetabolites, such as phenols and tannins, are
crucial in plants because they provide a family of multigenic factors that
make it difficult for the insect to evolve resistance (Venugopal et al.,
2000). Tannins are found in large quantities at the grain coat of legumes
and are in excellent antifeedant agent (Stapopoulos, 1987). Plants
fertilization may affect the production of their secondary metabolites
(Hugentobler and Renwick, 1995; Agrawal et al., 2012). From the point
of view of pest control, improving host plant resistance by the applica­
tion of a suitable fertilizer would be beneficial in reducing C. maculatus
infestation in storage (Naseri and Hamzavi, 2021).
Phosphorus deficiency is one of the major limiting factors in a crop
growth and its nitrogen fixation (Bhattacharjee and Dey, 2014).

* Corresponding author. Department of Plant Protection, University of Mohaghegh Ardabili , Ardabil, Iran.
E-mail address: bnaseri@uma.ac.ir (B. Naseri).

https://doi.org/10.1016/j.jspr.2022.101978
Received 19 February 2022; Received in revised form 14 April 2022; Accepted 21 April 2022
Available online 2 May 2022
0022-474X/© 2022 Elsevier Ltd. All rights reserved.
F. Hamzavi et al.
However, a balanced and adequate level of the soil phosphorus can in­
crease plants growth and photosynthesis (Gao et al., 1989). The in­
teractions between the soil phosphorus and biofertilizers are important
since they have an enlivening influence on the symbiosis and biological
nitrification (Somani et al., 1994). Plant growth-promoting rhizobac­
teria and mycorrhizal fungi, as eco-friendly and cost-effective bio­
fertilizers, can not only amend plants growth, but also induce their
resistance to some insect pests and plant diseases (Megali et al., 2014;
Sattari Nasab et al., 2018; Naseri and Hamzavi, 2021).
Several studies have identified negative impacts of chemical or
physical traits of stored grains on post-harvest insects’ survival, devel­
opment, longevity, and fecundity (Arong and Usua, 2006; Adam and
Baidoo, 2008; Bidar et al., 2021; Naseri et al., 2022). Studying the effects
of nitrogen fertilization or rhizobium inoculation on the loss caused by
C. maculatus on harvested cowpea grains, Torres et al. (2016) noted that
C. maculatus fed on the grains treated with rhizobial strains had the
lowest cumulative insect emergence and population growth. Recently,
Naseri and Hamzavi (2021) evaluated the influence of some mineral-
and bio-fertilizers on the resistance of cowpea (cultivar Mashhad) green
pod and its immature grain to C. maculatus. They found that the treat­
ment of farm-grown cowpeas by Bradyrhizobium japonicum can reduce
the infestation of the green pods by C. maculatus, resulting in less
infested grains being transferred to storage. However, since most of the
damage caused by C. maculatus occurs on stored grains, in this study, we
examined the effect of cowpea (cultivar 1057) fertilization with some
mineral- and bio-fertilizers on the resistance of the mature grains to this
pest under storage conditions. For this purpose, we evaluated the
biology and life table parameters of C. maculatus infesting stored cowpea
grains and their association with some biophysical and biochemical
features of tested grains. Our findings could be helpful in selecting the
proper fertilizer to increase cowpea resistance to C. maculatus during
storage.
2. Materials and methods
2.1. Tested grains and fertilizers
The Plant and Seed Improvement Research Institute (Karaj, Iran)
donated the cowpea grains (V. unguiculata; cultivar 1057). The Soil and
Water Research Institute (Karaj, Iran) provided tested biofertilizers:
Bradyrhizobium japonicum (108 colony-forming units/g), Pseudomonas
putida (107 colony-forming units/g), and mycorrhizal fungi (a combi­
nation of Glomus etunicatum, G. mosseae, and Rhizophagus irregularis).
The cowpea grains were covered with Arabic gum and thoroughly mixed
with the bacteria solution (Seyed Sharifi and Khavazi, 2011). Triple
superphosphate (TSP) fertilizer was provided from Shanghai Good Year
International Trade Co., Ltd. (China), and nitrogen (urea) fertilizer was
purchased from Khorasan Petrochemical Co. (Iran).
2.2. Fertilizer treatments and cultivation of grains
The cowpea grains were planted in a research farm of Faculty of
Agriculture and Natural Resources, Moghan Campus (Parsabad Moghan,
Iran). A randomized complete block design was used to allocate exam­
ined fertilizers and a control with no fertilizer. The plots were built up of
seven rows (10 m in length, 70 cm row spacing) with 15 cm between
plants in each row. For the mineral fertilizer plots, TSP (200 kg/ha) was
used prior to planting, and urea (70 kg/ha) was applied 7 days after
planting at the first watering. The grains were treated with each bio­
fertilizer on the farm before being planted in the plots. Weeds were
cleared using a hoe after the grains were sown by hand. To irrigate the
plants, a trickle irrigation system was used every 10 days. The yellow
and ripe pods were gathered separately for each treatment and control
by hand. To eradicate any insect pests that had developed in the field,
the grains were packed in plastic bags and preserved at − 20 ◦ C for one
month.
2
Journal of Stored Products Research 97 (2022) 101978
2.3. Insect rearing
The initial population of C. maculatus was obtained from Department
of Plant Protection, University of Mohaghegh Ardabili (Ardabil, Iran),
and kept on cowpea grains in plastic containers (diameter 18.5 cm,
depth 7 cm). The containers lids were cut and coated with silk mesh to
allow ventilation. Rearing of C. maculatus and all tests were carried out
in a dark growth chamber (28 ± 1 ◦ C and 65 ± 5% R.H.).
2.4. Grain features
2.4.1. Hardness, weight and moisture content
The grain hardness (ten replicates) of cowpeas derived from each
fertilizer treatment and control was tested using a universal testing de­
vice (SANTAM Engineering Design Co. Ltd, Tehran, Iran). An individual
grain from each treatment or control was put in the center of fixed plate.
The speed of the moving plate was set at 5 mm per minute, and the first
break created by applying pressure to each grain, in Newton (N), was
considered as the hardness index. The mean thousand-grain weight
(three replicates) was calculated by weighing 1000 cowpea grains from
each fertilizer treatment or control.
The moisture content (MC) of cowpea grains taken from each fer­
tilizer treatment (three replicates) was determined on a wet-weight basis
(AACC, 2000). An electric coffee grinder was used to mill the grains into
flour, and 5 g of the resulting flour was dried in an oven (130 ◦ C for 3 h).
The percentage of the grain MC was determined using the following
equation:
MC =
5− ​ weight ​ of ​ dried ​ grains ​ (g)
× 100
5
2.4.2. Protein and starch concentration
Protein and starch contents (each in three replicates) of the cowpea
grains from each fertilizer treatment and control were determined using
bovine serum albumin (Bradford, 1976) and iodine reagent (Bernfeld,
1955), respectively. In brief, 200 mg of milled grains was homogenized
in distilled water, and the absorbance was read by a spectrophotometer
(Unico UV/Vis 2100, New Jersey, USA).
2.4.3. Phenolic and tannin content
The Folin-Ciocalteau method was used to assess total phenolics (in
three replicates) of tested grains (Makkar, 2003). Briefly, 200 mg of the
grain flour was homogenized in methanol 99.0%. The supernatant was
vaporized after centrifugation, and the residue was mixed with 5 mL
distilled water and utilized as a total phenolic. The absorbance was
measured at 725 nm after adding 10% Folin-Ciocalteau reagent and 5%
Na2CO3 solution to 2.5 ml of the extract. The tannin content of the grain
samples (in four replicates) was determined using the vanillin-HCL
technique (Broadhurst and Jones, 1978). A quantity of 0.5 mg of the
extract was mixed with 3 ml vanillin reagent and 1.5 ml HCL. After 15
min, the absorbance of the combination was measured at 500 nm.
2.5. Life cycle of Callosobruchus maculatus
For each treatment, ten pairs of 1-d-old male and female adults were
placed in separate plastic containers (diameter 18.5 cm, depth 7 cm),
each containing 100 grains from the treatment or control. After 24 h,
71–89 grains with the egg were selected and placed in a 6 cm Petri plate.
Each Petri plate included a grain infested with an egg. The develop­
mental time of immature stages and their viability were measured. After
the emergence of adult weevils, female (17–42 replicates) and male
(17–43 replicates) insects were paired in 6 cm Petri plates containing
three cowpea grains as oviposition substrates. Every 24 h, the number of
eggs deposited by each female was counted, and the grain having the egg
was replaced with a new uninfested grain. The grains were carefully split
open when no adult insects had emerged, and the number of dead insects
F. Hamzavi et al. Journal of Stored Products Research 97 (2022) 101978

(larvae, pupae, or adults) was counted.

TSP: triple superphosphate. Mycorrhizal fungi: a mixture of Glomus etunicatum, Glomus mosseae and Rhizophagus irregularis. Combined biofertilizers: a mixture of Pseudomonas putida, mycorrhizal fungi and Bra­
<0.001
<0.001
<0.001
<0.001

<0.001
0.005

0.859
2.6. Life table parameters of Callosobruchus maculatus

6, 53
6, 14

6, 14
6, 14
6, 21
6, 14
6,14
The life cycle and life table experiments were studied in a completely

Df
randomized design with 71–89 replicates and seven treatments. The
computer program TWOSEX-MSChart (Chi, 2020) was used to measure

14.34
39.66
2.58
9.02

5.26
2.80
0.41
the life table parameters of C. maculatus based on the age-stage, tow-sex

F
life table model (Chi and Liu, 1985; Chi, 1988). The program was loaded

217.27 ± 1.19 bc
164.38 ± 3.60 bc
with raw data of the pest’s biological characteristics including devel­

11.53 ± 0.13 ab

0.151 ± 0.000 c
30.83 ± 1.74 b

0.618 ± 0.03 a

12.33 ± 1.67 a
opmental time, adult longevity and daily number of eggs laid (fecun­
dity). Then, the age-specific survival rate (lx) was calculated as:

Control
∑
k
lx = sxj
j=1

Combined biofertilizers
where, k is the number of stage and sxj is the probability that a new

0.164 ± 0.002 bc
236.67 ± 2.60 a
154.98 ± 5.16 c
11.00 ± 0.11 bc
0.479 ± 0.01 bc
produced progeny survives to age x and stage j. The age-specific

55.13 ± 3.12 a

13.84 ± 2.67 a
fecundity (mx) was also calculated as:
∑k
j=1 sxjfxj
mx = ∑k
j=1 sxj

220.60 ± 1.40 abc

168.93 ± 1.60 abc
Mycorrhizal fungi

0.168 ± 0.000 b
where, fxj (age-stage-specific fecundity) is the number of progeny pro­

40.20 ± 1.96 ab
11.06 ± 0.17 bc
0.627 ± 0.02 a

12.38 ± 1.64 a
duction by a female. The lx and mx values were used to calculate the
intrinsic rate of increase (r) as:
∑
∞
r(x+1)
1= e− lx mx
x=0

228.53 ± 4.08 abc

181.90 ± 8.23 ab
0.192 ± 0.006 a
0.544 ± 0.00 ab
The net reproductive rate (R0), finite rate of increase (λ), and mean

55.30 ± 8.28 a

12.28 ± 2.64 a
10.60 ± 0.11 c
generation time (T) were respectively measured as R0 = Σlxmx, λ = er, Mean (±SE) physical and biochemical features of stored cowpea grains treated with tested mineral- and bio-fertilizers.

B. japonicum

Mean values followed by different letters within a row are significantly different according to Tukey test (P ≤ 0.05).
and T = (ln R0)/r (Chi and Liu, 1985; Carey, 1993).

2.7. Data analysis

226.67 ± 1.53 abc

0.156 ± 0.002 bc
42.12 ± 5.49 ab

0.573 ± 0.01 ab

152.33 ± 4.84 c
12.00 ± 0.30 a
Kolmogorov-Smirnov test was used to ensure that the data of the

9.51 ± 2.27 a
grain physicochemical parameters were normally distributed. The one-
P. putida

way ANOVA was utilized to analyze the data using Minitab version
16.0. The variances and standard errors of the life cycle and life table
data were estimated using the bootstrap technique, and the means were
separated by the paired-bootstrap test (Chi and Liu, 1985; Chi, 2020).
234.33 ± 2.62 ab
0.203 ± 0.002 a

187.93 ± 1.02 a
45.49 ± 3.58 ab
11.13 ± 0.06 bc

12.74 ± 1.16 a
0.404 ± 0.03 c

Pearson correlation coefficient was used to assess the simple corre­

lations between physicochemical features of the grains and C. maculatus
population parameters (Kitch et al., 1991; Naseri and Majd-Marani,
TSP

2022). According to the life cycle and life table data of the insect fed
on the grains from each treatment and control, a hierarchical clustering
Fertilizer treatmentδ

was performed by Ward’s method using SPSS 16.0 (Majd-Marani et al.,

0.157 ± 0.002 bc
46.32 ± 4.99 ab

214.77 ± 7.56 c
146.98 ± 5.83 c
0.649 ± 0.01 a

12.07 ± 1.79 a
10.73 ± 0.06 c

2018; Naseri et al., 2022).

3. Results
Urea

3.1. Grain features

Tannin content (mg catechin/100g sample)
Phenolic content (mg gallic acid/g sample)

The physical and biochemical properties of the grains treated with

tested fertilizers and control are shown in Table 1. The grains treated
with B. japonicum and combined biofertilizers were harder than control
(F = 2.58; df = 6, 53; P < 0.001). Mean 1000-grain weight of tested
Hardness index (Newton)

grains ranged from 236.67 g in combined biofertilizers to 214.77 g in

Thousand-seed weigh (g)
Protein content (mg/ml)
Starch content (mg/ml)

dyrhizobium japonicum.

urea treatment (F = 5.26; df = 6, 14; P = 0.005). The moisture content of

Moisture content (%)

the grains fertilized with P. putida was higher than B. japonicum- and
urea-treated ones (F = 9.02; df = 6, 14; P < 0.001).
The protein content of the grains treated with urea, mycorrhizal
Parameter

fungi and control was about 1.5-fold more than that of TSP-treated ones
Table 1

(F = 14.34; df = 6, 14; P < 0.001). However, the starch content of the

grains fertilized with B. japonicum and TSP was about 1.3–1.5 times
δ

3
F. Hamzavi et al. Journal of Stored Products Research 97 (2022) 101978

Fig. 1. Age-specific survival rate (lx) and fecundity (mx) curves of Callosobruchus maculatus fed on Vigna unguiculata grains obtained from tested fertilizers.

higher than the control, respectively (F = 39.66; df = 6, 14; P < 0.001). P. putida, and combined biofertilizers. The amount of phenolic com­
The highest tannin concentration was observed in the grains obtained pounds showed no significant differences among fertilizer treatments
from TSP fertilizer (F = 2.80; df = 6, 21; P < 0.001). In contrast, the and control (F = 0.41; df = 6, 14; P = 0.859).
lowest tannin concentration was seen in the grains acquired from urea,

Table 2
Mean (±SE) life cycle parameters of Callosobruchus maculatus on cowpea grains treated with tested fertilizers.
Parameter Fertilizer treatmentδ

Urea TSP P. putida B. japonicum Mycorrhizal fungi Combined Control

biofertilizers

Immature Survival (%) 76.71 ± 4.95 38.63 ± 5.16 96.59 ± 1.94 a 71.79 ± 5.09 73.86 ± 4.70 94.38 ± 2.43 ab 87.32 ± 3.94
cd (73) e (88) (88) d (78) d (88) (89) bc (71)
Developmental time (day) 25.71 ± 0.15 24.61 ± 0.11 25.88 ± 0.11 a 25.82 ± 0.19 ab 25.36 ± 0.40 bc 25.58 ± 0.07 b 26.09 ± 0.14 a
ab (56) c (34) (85) (56) (65) (84) (61)
Fecundity (eggs laid per 102.65 ± 2.67 79.58 ± 3.49 100.90 ± 2.08 a 91.96 ± 2.96 b 99.27 ± 3.34 ab 104.14 ± 2.36 a 97.06 ± 3.13
reproductive period) a (42) c (17) (42) (30) (37) (41) ab (29)
Oviposition period (day) 8.06 ± 0.29 ab 6.70 ± 0.22 7.88 ± 0.15 ab 7.23 ± 0.16 cd 7.35 ± 0.23 bc 8.12 ± 0.20 a (41) 7.24 ± 0.20 cd
(42) d (17) (42) (30) (37) (29)
Female longevity (day) 9.72 ± 0.32 ab 8.76 ± 0.41 9.38 ± 0.20 abc 8.43 ± 0.23 8.94 ± 0.29 bcd 9.80 ± 0.21 a (41) 8.82 ± 0.24 cd
(42) cd (17) (42) d (30) (37) (29)
Male longevity (day) 8.66 ± 0.29 b 7.76 ± 0.27 c 9.58 ± 0.26 a 8.46 ± 0.43 bc 9.60 ± 0.36 a 9.51 ± 0.27 a (43) 8.75 ± 0.30 ab
(32) (17) (43) (26) (28) (32)

Mean values in a row followed by different letters are significantly different (P ≤ 0.05) according to paired-bootstrap test.
Numerals in the parentheses show the sample size for each parameter.
δ
TSP: triple superphosphate. Mycorrhizal fungi: a mixture of Glomus etunicatum, Glomus mosseae and Rhizophagus irregularis. Combined biofertilizers: a mixture of
Pseudomonas putida, mycorrhizal fungi and Bradyrhizobium japonicum.

4
F. Hamzavi et al.
3.2. Age-specific survival rate and fecundity of Callosobruchus maculatus
Fig. 1 shows the age-specific survival rate (lx) and daily fecundity
(mx) of C. maculatus growing on fertilized and control grains. At the first
day of their emergence, survival rate of the females was 0.76, 0.38, 0.96,
0.71, 0.73, 0.94, and 0.87, on the grains treated with urea, TSP,
P. putida, B. japonicum, mycorrhizal fungi, combined biofertilizers and
control, respectively. In the same order of treatments, the maximum age
of the female weevil was recorded in days 39, 37, 39, 42, 43, 40, and 39,
and the highest daily fecundity of the pest was 10.1, 7.6, 9.0, 8.2, 13.5,
9.8, and 7.8 offspring.
3.3. Life cycle of Callosobruchus maculatus
Table 2 shows the life cycle of C. maculatus on the grains treated with
tested fertilizers and control. The immature survival of C. maculatus fed
on P. putida-treated grains was higher than on TSP-treated ones (P <
0.05). Developmental times of C. maculatus on the grains obtained from
P. putida and control were longer than those obtained from TSP (P <
0.05). Fecundity (number of eggs produced by each female) of
C. maculatus on the grains from urea, P. putida and combined bio­
fertilizers was more than on those from TSP (P < 0.05). The oviposition
period on the grains from combined biofertilizers was longer than those
from TSP fertilizer (P < 0.05). Female and male longevities were
significantly different (P < 0.05) when the insect was reared on the
grains from different treatments. The female longevity on the grains
treated with combined biofertilizers was longer than on B. japonicum
treatment. Male longevity was the longest on the grains obtained from
mycorrhizal fungi, P. putida, and combined biofertilizers, and shortest
on those obtained from TSP.
3.4. Life table parameters of Callosobruchus maculatus
The life table parameters of C. maculatus fed on the treated grains and
control are shown in Table 3. Among various fertilizer treatments, the
net reproductive rate (R0), intrinsic rate of increase (r), finite rate of
increase (λ), and mean generation time (T) of the pest were the lowest
when C. maculatus was fed with the grains treated with TSP (P < 0.05).
3.5. Correlation analysis
Pearson correlation results between physiochemical features of the
treated grains and C. maculatus population parameters are given in
Table 4. Soluble starch in tested grains had significant negative corre­
lations with immature survival (Pearson’s r = − 0.84, P < 0.05),
fecundity (Pearson’s r = − 0.86, P < 0.05), R0 (Pearson’s r = − 0.82, P <
0.05), r (Pearson’s r = − 0.80, P < 0.05) and T (Pearson’s r = − 0.84, P <
0.05). Furthermore, tannin content of the grains negatively correlated
with immature survival (Pearson’s r = − 0.78, P < 0.05), fecundity
(Pearson’s r = − 0.87, P < 0.01), female longevity (Pearson’s r = -0.85, P
< 0.05), R0 (Pearson’s r = − 0.81, P < 0.05), and r (Pearson’s r = − 0.77,
P < 0.05).
Table 3
Mean (±SE) two-sex life table parameters of Callosobruchus maculatus on cowpea grains treated with tested fertilizers.
Parameter Fertilizer treatmentδ
Urea TSP P. putida
R0 (offspring) 40.78 ± 5.99 a 15.37 ± 3.41 b 48.15 ± 5.46 a
r (day¡1) 0.1294 ± 0.005 a 0.1005 ± 0.008 b 0.1348 ± 0.004 a
λ (day¡1) 1.138 ± 0.006 a 1.105 ± 0.009 b 1.144 ± 0.004 a
T (day) 28.64 ± 0.20 a 27.17 ± 0.22 b 28.72 ± 0.18 a
Mean values in a row followed by different letters are significantly different (P ≤ 0.05) according to paired-bootstrap test.
R0: net reproductive rate, r: intrinsic rate of increase, λ: finite rate of increase, T: mean generation time.
δ
TSP: triple superphosphate. Mycorrhizal fungi: a mixture of Glomus etunicatum, Glomus mosseae and Rhizophagus irregularis. Combined biofertilizers: a mixture of
Pseudomonas putida,mycorrhizal fungi and Bradyrhizobium japonicum.
Journal of Stored Products Research 97 (2022) 101978
3.6. Cluster analysis
The dendrogram obtained from the cluster analysis of C. maculatus
population parameters on the grains treated with different fertilizers and
control is shown in Fig. 2. The grains were grouped into two clusters A
(grains from tested biofertilizers, urea and control) and B (grains from
TSP).
4. Discussion
This study demonstrated that the life cycle and life table parameters
of C. maculatus were significantly affected by its feeding on cowpea
grains treated with examined mineral- and bio-fertilizers. The viability,
development and fecundity performance of C. maculatus mainly depend
on food resources acquired by larval feeding (Sarwar, 2012). High
concentration of starch and tannins in TSP-treated grains may be a
possible reason for the poor survival of C. maculatus immature stages.
Several traits were reported as sources of resistance in garden pea, Pisum
sativum L. grains like the higher sugar and lower starch content (Kel­
lenbarger et al., 1951; Kooistra, 1962), and the proportion of amylose to
amylopectin in the grain starch (Badenhuizen, 1963). Podoler and
Applebaum (1971) reported that high-amylose starch in P. sativum
grains can prevent the development of Callosobrucus chinensis (L.) larvae.
Condensed tannins in legume grains are noxious to C. maculatus larvae
(Boughdad et al., 1986), and considerably decrease its feeding perfor­
mance and potential population growth (Stapopoulos, 1987). In our
study, although no correlation was evident between the protein content
and C. maculatus population parameters, this content in TSP-treated
grains was lower than the other treatments. Leguminous grains have
higher protein content than non-leguminous ones (Danielsson, 1949). As
C. maculatus immature stages spend whole life in a single host grain, the
low protein content of the grain plays a key role in their survival and
development (Mohamed and Abd-El Hameed, 2014; Naseri et al., 2022).
However, surviving larvae fed with TSP-treated grains could complete
their development faster than those fed with control or P. putida treat­
ment. So, it is possible that these larvae were able to overcome the
toxicity of the grain tannins, and optimally consumed the low protein in
the grain. The grains treated with P. putida fertilizer, with the interme­
diate amount of protein, provided optimal conditions for survival of the
immature stages. Moreover, high moisture content in the grains fertil­
ized with P. putida may be another factor responsible for high survival of
C. maculatus larvae and pupae. Grain moisture content is required for the
development, adult emergence, and potential damage caused by stored
product insects (Yakubu et al., 2011; Naseri et al., 2022).
Because C. maculatus adults do not feed, their reproductive ability
depends upon the food reserves during the larval feeding. Callosobruchus
maculatus fed on nutrient-poor diet produces fewer eggs than that fed on
nutrient-rich diet (Fox and Czesak, 2000). The highest fecundity of
C. maculatus was on the grains treated with urea, P. putida, and com­
bined biofertilizers, and the lowest fecundity was on TSP-treated grains.
High protein content and low tannins in the grains treated with urea
fertilizer could explain the high fecundity of the pest fed on them.
B. japonicum Mycorrhizal fungi Combined biofertilizers Control
35.37 ± 5.18 a 41.73 ± 5.41 a 47.97 ± 5.61 a 39.64 ± 5.79 a
0.1254 ± 0.005 a 0.1300 ± 0.004 a 0.1344 ± 0.004 a 0.1279 ± 0.005 a
1.336 ± 0.006 a 1.138 ± 0.005 a 1.143 ± 0.004 a 1.136 ± 0.006 a
28.41 ± 0.26 a 28.69 ± 0.21 a 28.78 ± 0.11 a 28.76 ± 0.23 a
5
F. Hamzavi et al. Journal of Stored Products Research 97 (2022) 101978

Table 4
Pearson correlation coefficient (r) obtained between Callosobruchus maculatus population parameters and properties of cowpea grains treated with tested fertilizers.
Parameter Soluble starch Protein content Hardness index Thousand-seed weight Moisture content Tannins content

r P-value r P-value r P-value r P-value r P-value r P-value

IS − 0.838 0.018 0.508 0.245 − 0.084 0.859 − 0.207 0.655 0.391 0.386 − 0.779 0.039
DT − 0.728 0.064 0.690 0.087 − 0194 0.676 − 0.492 0.262 0.216 0.642 − 0.308 0.502
Fc − 0.859 0.013 0.648 0.115 − 0.008 0.987 − 0.369 0.416 0.115 0.805 − 0.873 0.010
OP − 0.700 0.080 0.392 0.385 0.265 0.566 − 0.139 0.767 0.049 0.917 − 0.915 0.400
FL − 0.570 0.182 0.092 0.845 0.206 0.657 0.018 0.969 0.112 0.810 − 0.854 0.015
ML 0.676 0.095 0.435 0.329 0.064 0.892 − 0.095 0.839 0.364 0.422 − 0.643 0.120
R0 − 0.820 0.024 0.592 0.162 0.007 0.988 − 0.262 0.571 0.255 0.583 − 0.809 0.028
r − 0.802 0.030 0.657 0.109 − 0.001 0.998 − 0.330 0.470 0.177 0.705 − 0.774 0.041
λ 0.345 0.449 0.053 0.910 0.520 0.232 0.098 0.835 − 0.470 0.287 0.337 0.460
T − 0.842 0.018 0.742 0.056 − 0.126 0.787 − 0.454 0.307 0.147 0.754 − 0.740 0.057

IS: immature survival, DT: developmental time, Fc: fecundity, OP: oviposition period, FL: female longevity, ML: male longevity, R0: net reproductive rate, r: intrinsic
rate of increase, λ: finite rate of increase, T: mean generation time.

Fig. 2. Dendrogram of life cycle and life table parameters of Callosobruchus maculatus fed on Vigna unguiculata grains obtained from tested fertilizers (Ward’s
method).
Pp: Pseudomonas putida, Cb: Combined biofertilizers including Pseudomonas putida + mycorrhizal fungi + Bradyrhizobium japonicum, Ur: Urea, Mf: Mycorrhizal fungi:
a mixture of Glomus etunicatum, Glomus mosseae and Rhizophagus irregularis, Co: Control, Bj: Bradyrhizobium japonicum, TSP: triple superphosphate.

However, the lowest fecundity, oviposition period and male longevity of
C. maculatus fed with TSP-fertilized grains may be related to the high
concentration of tannins, and the low protein levels in these grains.
Despite the high concentration of starch in the grains treated with TSP
fertilizer, due to the nutritional imbalance in the levels of starch and
protein, the lowest fecundity was observed on this treatment. Extended
male longevity of C. maculatus on the grains treated with P. putida,
mycorrhizal fungi, and combined biofertilizers provides more time for
mating with females, which can lead to increase in egg production
(Credland and Wright, 1989) and offspring viability (Fox, 1993).
The results of correlation analysis showed that the amount of soluble
starch and tannins negatively correlated with immature survival and
fecundity of C. maculatus. However, varying the protein content in the
grains treated with different fertilizers had no correlation with tested
parameters of the pest. Imbuhila (2020) stated that protein levels of
cowpea lines were positively correlated with C. maculatus infestation,
but tannin content was negatively correlated with its infestation.
Deepika et al. (2020) found a significant positive association between
protein content and starch content of chickpea lines with the grain loss
caused by C. chinensis.
Analysis of an insect’s life table is a worth technique for determining
its population buildup (Krisp et al., 1998), and identifying the most
effective management strategy (Kakde et al., 2014). The lowest R0, r,
and λ values of C. maculatus fed on the grains obtained from TSP fer­
tilizer can be attributed to high mortality of pre-adult stages due to poor
protein and high concentration of starch and tannins in TSP-treated
grains. So, the use of TSP fertilizer could increase the resistance of
stored cowpea grains to C. maculatus. According to Naseri and Hamzavi
(2021), green pods and immature grains from cowpea (cultivar Mash­
had) fertilized with a biofertilizer, B. japonicum, were relatively resistant
to C. maculatus attack and population growth. They suggested that
B. japonicum can be used to minimize C. maculatus infestation in cowpea
farms. However, our study also emphasized the importance of
TSP-fertilized grain in inducing its resistance to C. maculatus. Differences
in the examined cultivars, rearing conditions and growth stage of the
tested grains can explain the differences between our results with those
reported by above-mentioned researchers. However, it can be suggested
that the combined application of TSP and B. japonicum on cowpea plants
may enhance the resistance of farm-grown green pods and stored grains
to C. maculatus, which should be investigated in subsequent works. The r
values of C. maculatus, in this study, are higher than those reported for
C. maculatus fed with immature grains (Naseri and Hamzavi, 2021),
indicating that the potential population increase and damage caused by
the pest on stored grains are much greater than farm-grown immature
grains (Hill, 1990).
Cluster analysis results revealed that the control grains and those
treated with urea, P. putida, mycorrhizal fungi, B. japonicum, and com­
bined biofertilizers (cluster A) were the most favorable, and TSP-
fertilized grains (cluster B) were the least favorable to C. maculatus
population buildup. The insects reared on TSP-treated grains had lower
immature survival and fecundity than those in the control or other
treatments, which resulted in a notable reduction in the life table pa­
rameters. By contrast, high values of r, R0, and λ in C. maculatus fed on
control grains and those obtained from urea and tested biofertilizers led
to the grouping of them as favorable grains for C. maculatus. Reuveni and
Reuveni (1998) stated that phosphorus application can reduce plant
diseases or insects damage. However, urea fertilizer enhances cowpea
vulnerability to C. maculatus attacks (Naseri and Hamzavi, 2021).
Phosphorus fertilizer stimulates nodulation of host pulses more via its
impacts on phosphate-solubilizing bacteria than on the host (Pathak
et al., 2003). In the presence of sufficient phosphorus, the motility of
bacterial cells would be increased, leading to the great development of

6
F. Hamzavi et al.
the nodules (Jat and Ahlawat, 2006). According to the results of this
study, application of TSP increased the concentration of starch and
tannins in stored cowpea grains. So, it can be concluded that starch and
tannin are two major factors involved in the cowpea resistance to
C. maculatus in storage.
Understanding how C. maculatus performs biologically on the grains
received from various fertilizer treatments can aid in its effective con­
trol. For instance, owing to the rapid population increase of C. maculatus
on the grains treated with urea and tested biofertilizers, farmers should
avoid using only these fertilizers. However, the application of TSP fer­
tilizer along with biofertilizers, especially B. japonicum, can be recom­
mended to enhance the resistance of stored cowpeas to this pest.
CRediT authorship contribution statement
Fatemeh Hamzavi: Investigation, Formal analysis, Methodology,
Writing–review & editing. Bahram Naseri: Conceptualization, Formal
analysis, Methodology, Writing–review & editing, Supervision. Mehdi
Hassanpour: Investigation, Writing–review & editing. Jabraeil
Razmjou: Investigation, Writing–review & editing. Ali Golizadeh:
Investigation, Writing–review & editing.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgment
We acknowledge the University of Mohaghegh Ardabili, Ardabil,
Iran, for collaboration by support for the experiment.
References
AACC, 2000. Approved Methods of the American Association of Cereal Chemists, tenth
ed. The American Association of Cereal Chemists, St Paul, MN.
Adam, J.I., Baidoo, P.K., 2008. Susceptibility of some five cowpea varieties to attack by
Callosobruchus maculatus F. (Coleoptera: Bruchidae). J. Ghana Sci. Assoc. 10 (2),
85–92.
Agrawal, A.A., Petschenka, G., Bingham, R.A., Weber, M.G., Rasmann, S., 2012. Toxic
cardenolides: chemical ecology and coevolution of specialized plant-herbivore
interactions. New Phytol. 194, 28–45.
Arong, G.A., Usua, E.J., 2006. Comparative development of cowpea bruchid
(Callosobruchus maculatus (F.) (Coleoptera: Bruchidae) on pods and seeds of some
cowpea cultivars (Vigna unguiculata). Global J. Appl. Pure Sci. 12, 35–40.
Badenhuizen, N.P., 1963. Formation and distribution of amylose and amylopectin in the
starch granule. Nature, Land. 197, 464467.
Badii, B.K., Adrakwah, C., Obeng-Ofori, D., Ulrichs, C., 2013. Efficacy of diatomaceous
earth formulations against Callosobruchus maculatus (F.) (Coleoptera: Bruchidae) in
Kersting’s groundnut (Macrotyloma geocarpum Harms): influence of dosage rate and
relative humidity. J. Pest. Sci. 87, 285–294.
Bernfeld, P., 1955. Amylase, α and β. Methods Enzymol. 1, 149–158.
Bhattacharjee, R., Dey, U., 2014. Biofertilizer, a way towards organic agriculture: a
review. AJMR (Am. J. Ment. Retard.) 8 (24), 2332–2342. https://doi.org/10.5897/
AJMR2013.6374.
Bidar, F., Razmjou, J., Golizadeh, A., Fathi, S.A.A., Ebadollahi, A., Naseri, B., 2021. Effect
of different legume seeds on life table parameters of cowpea weevil, Callosobruchus
maculatus (F.) (Coleoptera: Chrysomelidae). J. Stored Prod. Res. 90, 101755 https://
doi.org/10.1016/j.jspr.2020.101755.
Boughdad, A., Gillon, Y., Gagnepain, C., 1986. Influence des tannins condences du
tégument de fèves (Vicia faba) sur le développement larvaire de Callosobruchus
maculatus. Entomol. Exp. Appl. 42, 125–132. https://doi.org/10.1111/j.1570-
7458.1986.tb01012.x.
Bradford, M.M., 1976. A rapid and sensitive method for the quantitation of microgram
quantities of protein utilizing the principle of protein dye binding. Anal. Biochem.
72, 248–254. https://doi.org/10.1016/0003-2697(76)90527-3.
Broadhurst, R.B., Jones, W.T., 1978. Analysis of condensed tannins using acidified
vanillin. J. Sci. Food Agric. 29, 788–794. https://doi.org/10.1002/jsfa.2740290908.
Carey, J.R., 1993. Applied Demography for Biologists with Special Emphasis on Insects.
Oxford University Press, Inc., New York.
Castro, M.J.P., Baldin, E.L.L., Cruz, P.L., de Souza, C.M., da Silva, P.H.S., 2013.
Characterization of cowpea genotype resistance to Callosobruchus maculatus. Pesq.
Agropec. Bras, Brasília 48 (9), 1201–1209. https://doi.org/10.1590/S0100-
204X2013000900003.
7
Journal of Stored Products Research 97 (2022) 101978
Chi, H., 1988. Life-table analysis incorporating both sexes and variable development
rates among individuals. Environ. Entomol. 17, 26–34. https://doi.org/10.1093/ee/
17.1.26.
Chi, H., 2020. TWOSEX–MSChart: a Computer Program for the Age Stage, Two-Sex Life
Table Analysis. National Chung Hsing University, Taichung, Taiwan. http://140.
120.197.173/Ecology/Download/Twosex-MSChart.zip. (Accessed 1 August 2020).
Chi, H., Liu, H., 1985. Two new methods for the study of insect population ecology. Bull.
Inst. Zool. Acad. Sin. (Taipei) 24, 225–240.
Credland, P.F., Wright, A.W., 1989. Factors affecting female fecundity in the cowpea
seed beetle, Callosobruchus maculatus (Coleoptera: Bruchidae). J. Stored Prod. Res.
25, 125–136.
Danielsson, C.E., 1949. Seed globulins of the Gramineae and Leguminosae. Biochem. J.
44, 387–400.
Deepika, K.L., Singh, P.S., Singh, S.K., Saxena, R.P.N., 2020. Biochemical basis of
resistance against pulse beetle, Callosobrucus chinensis (L.) in stored chickpea
genotype. J. Exp. Zool. India 23 (2), 1175–1180.
Fox, C.W., 1993. Multiple mating, lifetime fecundity and female mortality of the bruchid
beetle, Callosobruchus maculatus (Coleoptera: Bruchidae). Funct. Ecol. 7, 203–208.
https://doi.org/10.2307/2389888.
Fox, C.W., Czesak, M.E., 2000. Evolutionary ecology of progeny size in arthropods. Annu.
Rev. Entomol. 45, 341–369.
Furk, B.C., Hines, C.M., 1993. Aspects of insecticide resistance in the melon and cotton
aphid, Aphis gossypii (Hemiptera: Aphididae). Ann. Appl. Biol. 123, 9–17.
Gao, S.J., Chen, S.S., Li, M.Q., 1989. Effects of phosphorus nutrition on photosynthesis
and photorespiration in tobacco leaves. Acta Phytopathol. Sin. 15, 281–287.
Hagstrum, D.W., Phillips, T.H., Cuperus, G., 2012. Stored product protection. In:
Mason, L.J., McDonough, Biology, M. (Eds.), Behavior, and Ecology of Stored Grain
and Legume Insects. Kansas State University Agricultural Experiment Station and
Cooperative Extension Service.
Hertlein, M.B., Thompson, G.D., Subramanyam, B., 2011. Spinosad: a new natural
product for stored grain protection. J. Stored Prod. Res. 47 (3), 131–146.
Hill, D.S., 1990. Pests of Stored Products and Their Control. CRC press, Boca Raton,
p. 274.
Hugentobler, U., Renwick, J.A., 1995. Effects of plant nutrition on the balance of insect
relevant cardenolides and glucosinolates in Erysimum cheiranthoides. Oecologia 102,
95–101.
Imbuhila, B.S., 2020. Influence of Cowpea Plant and Seed Characteristics and Packaging
Material in Storage on Cowpea Weevil (Callosobruchus Maculatus) Infestation. Master
of Science Thesis. Jomo Kenyatta University of Agriculture and Technology.
Isman, M.B., 2008. Botanical insecticides: for richer, for poorer. Pest Manag. Sci. 64,
8–11.
Jat, R.S., Ahlawat, I.P.S., 2006. Direct and residual effect of vermicompost, biofertilizers
and phosphorus on soil nutrient dynamics and productivity of chickpea-fodder maize
sequence. J. Sustain. Agric. 28 (1), 85–112. https://doi.org/10.1300/J064v28n01_
05.
Kakde, A.M., Patel, K.G., Tayade, S., 2014. Role of life table in insect pest management-A
review. IOSR-JAVS. 7, 40–43.
Kellenbarger, S., Silveira, V., Mcciuady, R.M., Owens, H.S., Chapmanj, L., 1951.
Inheritance of starch content and amylose content of starch in peas (Pisum sativum).
Agron. J. 43, 337–340.
Khashaveh, A., Ziaee, M., Safaralizadeh, M.H., 2011. Control of pulse beetle,
Callosobruchus maculatus (F.) (Coleoptera: Bruchidae) using spinosad dust in storage
conditions. J. Stored Prod. Res. 51 (1), 77–81. https://doi.org/10.2478/v10045-
011-0014-z.
Kitch, L.W., Shade, R.E., Murdock, L.L., 1991. Resistance to the cowpea weevil
(Callosobruchus maculatus) larva in pods of cowpea (Vigna unguiculata). Entomol.
Exp. Appl. 60, 183–192.
Kooistra, E., 1962. On the differences between smooth and three types of wrinkled peas.
Eubhytica 11, 357–373.
Krisp, O.E., Witul, A., Willems, P.E.L., Dicke, M., 1998. Intrinsic rate of population
increase of the spider mite Tetranychus urticae on the ornamental crop gerbera:
intraspecific variation in host plant and herbivore. Entomol. Exp. Appl. 89, 159–168.
Majd-Marani, S., Naseri, B., Nouri-Ganbalani, G., Borzoui, E., 2018. Maize hybrids
affected nutritional physiology of the Khapra beetle, Trogoderma granarium Everts
(Coleoptera: Dermestidae). J. Stored Prod. Res. 77 https://doi.org/10.1016/j.
jspr.2018.02.005.
Makkar, H.P.S., 2003. Measurement of Total Phenolics and Tannins Using Folin-
Ciocalteu Method. Quantification of Tannins in Tree and Shrub Foliage, vols. 49–51.
Springer, Dordrecht. https://doi.org/10.1007/978-94-017-0273-7_3.
Megali, L., Glauser, G., Rasmann, S., 2014. Fertilization with beneficial microorganisms
decreases tomato defenses against insect pests. Agron. Sustain. Dev. 34, 649–656.
https://doi.org/10.1007/s13593-013-0187-0.
Mohamed, H.I., Abd-El Hameed, A.G., 2014. Molecular and biochemical markers of some
Vicia faba L. genotypes in response to storage insect pests infestation. J. Plant
Interact. 9 (1), 618–626. https://doi.org/10.1080/17429145.2013.879678.
Naseri, B., Hamzavi, F., 2021. Effects of chemical- and bio-fertilizers on cowpea
resistance to cowpea weevil. Callosobruchus maculatus (F.) (Coleoptera:
Chrysomelidae. J. Stored Prod. Res. 92, 101785 https://doi.org/10.1016/j.
jspr.2021.101785.
Naseri, B., Hamzavi, F., Ebadollahi, A., Sheikh, F., 2022. Physicochemical traits of Vicia
faba L. seed cultivars affect oviposition preference and demographic parameters of
Callosobruchus maculatus (F.) (Coleoptera: Chrysomelidae). J. Stored Prod. Res. 95,
101924 https://doi.org/10.1016/j.jspr.2021.101924.
Naseri, B., Majd-Marani, S., 2022. Different cereal grains affect demographic traits and
digestive enzyme activity of Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae).
J. Stored Prod. Res. 95 https://doi.org/10.1016/j.jspr.2021.101898.
F. Hamzavi et al.
Pathak, S., Namdeo, K.N., Chakrawarti, V.K., Tiwari, R.K., Pathak, S., 2003. Effect of
biofertilizers, diammonium phosphate and zinc sulphate on growth and yield of
chickpea (Cicer arietinum L.). Crop Res 26, 42–46.
Phillips, R.D., McWatters, K.H., Chinnan, M.S., Hung, Y.C., Beuchat, L.R., Sefa-Dedeh, S.,
Sakyi-Dawson, E., Ngoddy, P., Nnanyelugo, D., Enwere, J., Komey, N.S., Liu, K.,
Mensa-Wilmot, Y., Nnanna, I.A., Okeke, C., Prinyawiwatkul, W., Saalia, F.K., 2003.
Utilization of cowpeas for human food. Field Crop. Res. 82, 193–213.
Podoler, H., Applebaum, S.W., 1971. Host specificity in the Bruchidae-VII. The effect of
carbohydrate composition on varietal resistance of garden peas to Callosobruchus
chinensis L. J. Stored Prod. Res. 7, 97–105.
Reuveni, R., Reuveni, M., 1998. Foliar-fertilizer therapy - a concept in integrated pest
management. Crop Protect. 17 (2), 111–118. https://doi.org/10.1016/S0261-2194
(97)00108-7.
Sarwar, M., 2012. Assessment of resistance to the attack of bean beetle Callosobruchus
maculatus (Fabricius) in chickpea genotypes on the basis of various parameters
during storage. Songklanakarin J. Sci. Technol. 34, 287–291.
Sattari Nasab, R., Pahlavan Yali, M., Bozorg-Amirkalaee, M., 2018. Effects of humic acid
and plant growth-promoting rhizobacteria (PGPR) on induced resistance of canola to
Brevicoryne brassicae L. Bull. Entomol. Res. 109, 479–489. https://doi.org/10.1017/
S0007485318000779.
View publication stats
Journal of Stored Products Research 97 (2022) 101978
Seyed Sharifi, R., Khavazi, K., 2011. Effects of seed priming with plant growth promoting
rhizobacteria (PGPR) on yield and yield attributes of maize (Zea mays L.) hybrids.
J. Food Agric. Environ. 9, 496–500.
Somani, L.L., Bhandari, S.C., Vyas, K.K., Saxena, S.N., 1994. Biofertilizers. 85-112.
Scientific Publishers, Jodhpur India.
Stapopoulos, D.C., 1987. Influence of the Leguminosae secondary substances on the
ecology and biology of Bruchidae. Entomol. Hell. 5, 61–67. https://doi.org/
10.12681/eh.13949.
Torres, E.B., Nobrega, R.S.A., Fernandes-Jonior, P.I., Silva, L.B., Carvalho, G.S.,
Marinho, R.C.N., Pavan, B.E., 2016. The damage caused by Callosobruchus maculatus
on cowpea grains is dependent on the plant genotype. J. Sci. Food Agric. 96 (12),
4276–4280. https://doi.org/10.1002/jsfa.7639.
Turaki, J.M., 2012. Simulating infestations and losses in storage from egg and adult
Callosobruchus maculatus (Coleoptera: Bruchidae) sources in cowpea (Vigna
unguiculata L. Walp.). IRJAS 2, 333–340.
Venugopal, K.J., Janarthanan, S., Ignacimuthu, S., 2000. Resistance of legume seeds to
the bruchid, Callosobruchus maculates: metabolites relationship. Indian J. Exp. Biol.
38 (5), 471–476.
Yakubu, A., Bern, C.J., Coats, J.R., Bailey, T.B., 2011. Hermetic on-farm storage for
maize weevil control in East Africa. Afr. J. Agric. Res. 6, 3311–3319.