Age-Stage, Two-Sex Life Table Study of the Effects of Sub-Lethal
Concentrations of Novaluron on Earias vittella (Lepidoptera: Noctuidae)
Dilawar Khan1,
Bilal Rasool2*, Asim Gulzar1, Muhammad Tariq1,
Sobia Khaliq1, Ihsan ul Haq3
and Sakhawat Ali4
1Department of Entomology, Pir-Meher
Ali Shah Arid Agriculture University, Rawalpindi, Punjab, Pakistan
2Departement of Zoology, Faculty of Life Sciences,
Government College University Faisalabad, Punjab, Pakistan
3Directorate of Agricultural Planning, Quetta, Balochistan, Pakistan
4Directorate of Vegetable Seed Farm Agriculture Research
Institute, Quetta, Balochistan, Pakistan
*For correspondence:
bilalisb2001@yahoo.com
Received
02 February 2021; Accepted 15 January 2022; Published 28 February 2022
Abstract
Earias vittella (F) is an
important insect pest of cotton (Gossypium hirsutum)
and okra (Abelmoschus esculentus) in Pakistan. The current study was
carried out to explore the effects of sub-lethal concentrations of novaluron on
the life table parameters of the pest. Bioassays were performed to assess the
sub-lethal concentrations (LC20 and LC50) of the
novaluron and its effects on the demographic parameters of the E. vittella.
Age-stage, two-sex life table theory was applied to interpret the data for
population parameters of E. vitella. In the current study, the LC20 and
LC50 were calculated as 2.224 ppm and 9.837 ppm, respectively. The
results showed that in novaluron treated samples rates of all biological
parameters decreased whereas the larval, pupal period and mean generation time
were increased. The intrinsic rate of increase remained high in control as
0.166 d-1 in comparison with LC50 as 0.128 d-1.
The net reproductive rate ranged from 94.542 offsprings
per individual (control) to 61.228 offsprings per
individual (LC50). Fecundity was dropped in insects treated with
sub-lethal concentrations from 330.9 eggs per female (control) to 238.11 eggs
per female (LC50). This study revealed that the sub-lethal
concentrations of novaluron significantly decreased the biological rate of E.
vitella under laboratory conditions and suggests
that such doses should be practiced in the fields for proper integrated pest
management strategies. © 2022 Friends Science Publishers
Keywords: Eairas vittella; Sub-lethal
concentration; Novaluron; Insect growth regulator; Two-sex life table
Introduction
Earais vittella (F.) (Noctuidae: Lepidoptera), also known as spotted bollworm, is
a notorious polyphagous pest of many malvaceous crops (Aziz et al. 2012). Some of its major host
crops include Gossypium spp. (cotton), Abelmoschus
esculentus (okra), Abutilon indicum, Hibiscus cannabinus, Althaearosea (hollyhock) and Malwa
parviflora (sonchal) (Rasool et al. 2002;
Jan et al. 2015; Rahman et al. 2016). The spotted bollworm is
active throughout the year and have 6 to 8 generations during each year.
Several buds and bolls are damaged by a single larva in its life span. In
cotton, it pupates in bolls and reduces the boll growth (Aziz et al. 2011; Jan et al. 2015) commonly the buds, flowers, and fruits are attacked by
second instar larvae and results in the reduction of quality and quantity. It
may reduce the yield up to 50% in cotton and about 69% in okra (Aziz et al. 2011).
The use of
chemicals plays a key role in the management of pests in fields, resulting in a
low risk of yield loss (Popp and Hantos 2011). E. vitella infestation has been managed using different
insecticides including, pyrethroids and organophosphates (Praveen et al.
2007; Umrao et al. 2013). Irregular and
massive application of such chemicals has resulted in resistance development in
field pests (Abbas et al. 2014; Gulzar and Wright 2014; Abbas and Shad
2015; Ahmad et al. 2019). Novaluron is one of the recent insect growth
regulators (IGR) that belong to the
insecticidal group, benzoylphenyl urea. It is a chitin synthesis inhibitor that
acts through ingestion and contact. It targets the larval stage of insects
which synthesize chitin actively (Lohmeyer and Pound
2012). The residual activity of novaluron in field
conditions depends upon the environmental conditions and ranges from 10 to 30
days (Ishaaya et al. 2003). It has a very low
toxic effect on mammals, birds, earthworms (Ishaaya et
al. 2007) and adults of non-targeted beneficial insect species (Cutler et
al. 2005).
The
application of pesticides in fields does not kill all the pest populations with
immediate effects, so over time the pesticide decreases and, as a result, the
sublethal effects including behavioral and physiological changes in pests can
occur (Rehan and Freed 2015). These sublethal
concentrations of pesticides can significantly alter the adult development,
adult insect weight, larval and pupa periods and reproduction parameters of the
insect (Han et al. 2012). For a
comprehensive pesticide evaluation, only acute toxicity is not enough, but the
sublethal effects may also be included (Zhang et al. 2015). Previously, Rahmani and Bandani (2013) found that the sub-lethal doses of
thiamethoxam chemical significantly altered the different Hippodamia
variegate population parameters in adverse modus. This study was planned to
elucidate the sublethal effects of the novaluron on population parameters of E.
vittella by application of Age-stage, two-sex life
table theory. The finding of this study may be helpful to monitor the
insecticide resistance in E. vittella to
insect growth regulators (IGRs) in fields and develop improved integrated pest
management strategies.
Materials and Methods
Insect culture and insecticides
Laboratory
culture of spotted bollworm (E. vittella) was
established from the larvae collected from okra fields in the surrounding of
Rawalpindi, Taxila and Attock. The infested pods from
the fields were transferred into transparent plastic jars (20 cm length and 10
cm wide) and were kept under control conditions (27 ± 2°C, 60 ± 5% R.H.
photoperiod of 16 L: 8 D). Insect culture was maintained on okra fruits as
described by Al-Mehmmady (2000). Fresh okra fruits
were washed thoroughly by tap water and air-dried before feeding to the
neonates. The okra fruits were cut into 0.5‒1.0 cm pieces,
4‒5 larvae were
released per piece and placed in the plastic container. The food was replaced
daily till pupation. The larvae were carefully removed from the okra pods and
the excreta were cleaned. The pupae were shifted to another plastic jar (10 cm
length and 5 cm width) until adult emergence. The emerged adults were shifted
to adult cages and fed with 10% sugar solution. Nappy strips were hanged in the
adult cages as oviposition sites, these strips were replaced regularly when
eggs were observed.
Novaluron,
insect growth regulator, (Corvus®) FMC Pvt. Ltd. was used at the recommended
dose along with different concentrations against the 1st instar
larvae of spotted bollworm (E. vittella) to
investigate the larvicidal effects.
Bioassays
Bioassays were performed by using diet emersion method
and toxicity of novaluron was checked against 1st larval instar of
spotted bollworm (E. vitella).
Different concentrations of novaluron by serial dilutions (mg L-1)
of stock solution were prepared using distilled water. Fresh okra fruits were
dipped separately in each concentration for 10 sec and then dried for 10 min at
room temperature. Five okra fruits were used in one replication. Two 1st instar
larvae were released on each okra pods in all replications treated with
different concentrations. Each treatment was replicated four times. Distilled
water was used as a control treatment. All the treated larvae were kept under
controlled conditions (Temperature of 25 ± 2°C; R. H. of 65 ± 5%). Mortality
data were assessed after 72 h.
Sublethal
effects on demographic parameters of E. vittella
In life table study, 210 eggs were used, which were
collected after 24 h of deposition by females of the laboratory population.
Three treatments (control, LC20, and LC50) were prepared
for this experiment. Seventy eggs were treated with each treatment. Each egg is
an individual petri dish that was considered as one replicate (Huang and Chi
2013; Zhang et al. 2015). All the
Petri dishes were kept under controlled conditions. The egg hatching data were
recorded daily. The neonates from control, LC20 and LC50
were shifted on the okra pods treated with control, LC20 and LC50,
respectively. The larval development was observed daily and fresh okra pods
were provided after each instar. Pupae were removed and placed in new
Petri dishes until emergence. After the adult emergence, they were paired (one
male and one female) and transferred to individual plastic containers for
oviposition. The adults were checked daily for oviposition and transferred to
new containers for egg-laying. The fecundity and survival rate of the adults
have assessed until the death of the adults.
Data analysis
The LC values were calculated based on mortality data by
using R Statistical Software version 2.9.0 (R Development Core Team 2009). The data
regarding different stage development periods, survival rate and fecundity
along with oviposition periods were analyzed using Age-stage, two-sex life
table theory (Chi and Liu 1985; Chi 1988) with TWO SEX-MS Chart software (Chi
2017). Means of the biological parameters were compared by using 100,000
bootstrap techniques to achieve stable SE estimates (Huang and Chi 2013). The
curves for age-specific survival rate, fecundity, life expectancy and
reproductive values were generated bu using Sigma
Plot 14.0. The net reproductive rate was calculated as:
The intrinsic rate of increase (r) is calculated by using the iterative bisection method from:
With age
indexed from zero (Goodman 1982). The mean generation time (T) is calculated as follow:
The Gross
reproductive rate (GRR) is calculated by the formula as follow:
The
age-specific survival rate (lx)
and age-specific fecundity (mx)
were given as:
Results
Toxicity bioassays
The toxicity
of novaluron against the 1st instar of E. vittella after 72 h is given in Table
1. The LC20 and LC50 were calculated as 2.224 mg L-1
and 9.837 mg L-1, respectively.
Sub-lethal effects of novaluron on biological parameters
of E. vittella
The
developmental periods, fecundity and adult longevity of both males and females
of E. vittella treated with sub-lethal
concentrations (LC20 and LC50) of novaluron are given in Table
2. Egg duration was significantly (P ≤
0.005, df=2, F=87.61) prolonged when treated with sub-lethal concentrations
(4.26 days and 4.07 days for LC50 and LC20 respectively
of novaluron as compared with the control (3.66 days). Total larval time was also
increased by treating with sub-lethal concentrations (LC50 andLC20)
as 12.54 days and11.23 days respectively (P
≤ 0.005, df=2, F=117.24) as compared with control (11.03 days). No
significant variation was noted between LC20 (11.35 days) and LC50
(11.47 days) in terms of the pupal period but differed significantly (P ≤ 0.005, df=2, F=122.82) when
compared with the untreated larvae (Table 2). Adult male longevity was not
significantly different (p=0.104, df=2, F=11.82), while female longevity was significantly
(P ≤ 0.005, df=2, F=92.87)
different ranging from highest (12.7 days) on control to the lowest (7.62 days)
on LC50. The differences in total pre-oviposition period (TPOP)
between sub-lethal concentrations were statistically non-significant (P ≤ 0.01, df=2, F=7.45), while a
significant difference was found between the control and treated larvae. The
number of eggs per female varied significantly (P ≤ 0.005, df=2, F=648.22) between sub-lethal concentrations
(238.11 and 268.5 eggs per female in LC50 and LC20
respectively). The highest fecundity (330.9 eggs per female) was noted for
untreated larvae.
Sub-lethal effects of novaluron on population parameters
of E. vittella
Novaluron
significantly altered the population parameters of the E. vittella (Table
3). To estimate the population parameters, the bootstrap method with 100,000
replicate sample method was used. The intrinsic rate of increase was decreased
by treating with both the concentrations of novaluron (0.128 and 0.140 d-1
for LC50 and LC20, respectively)
as compared with the untreated larvae (0.166 d-1). A similar trend
was found in the finite rate of increase (λ), as the highest value for
λ was found in control larvae (1.181 d-1) which gradually
decreases with an increase in concentration from LC20 to LC50
as 1.150 and 1.137 d-1 respectively. A significant decrease was also
observed in net reproductive rate after novaluron treatment from being highest
on control larvae (94.542 offsprings per individual)
to 76.714 and 61.228 offsprings per individual for LC20
and LC50 treated larvae respectively. Moreover, the gross
reproductive rate (GRR) of LC20 treated larvae (146.45, offsprings per individual) was significantly similar to
that of LC50 and control. The highest GRR was recorded for control
larvae (183.42 offsprings per individual), while the
lowest recorded for LC50 treated larvae (136.77 offsprings
per individual) which were both statistically significant to each other. The
mean generation time was prolonged in the treated larvae compared to the
control larvae. Minimum mean generation time was taken by the control larvae
(27.255 d), followed by LC20 treated larvae (30.967 d). The maximum
days were recorded on LC50 treated larvae (31.917 d). The curves of
developmental rates of the individuals showed an overlapped nature showing the
differences in their development rates (Fig. 1). Females were emerged late in
the population than males, while their survival was longer than males. The LC20
and LC50 treatment were observed with less number of larvae as
compared with untreated. The longest time for development was noted for LC50
and LC20 treated larvae when compared with untreated larvae
(Fig. 1).
Age-specific
survival rates (lx), age-specific fecundity (fx,
female), age-specific fecundity for total population and age-specific maternity
(lxmx) are presented in Fig. 2. A significant
decline in the curve of lx was noted in LC20 and LC50
treated larvae after 32 days of the treatment. The untreated group has the
highest top peaks of fx and mx than
compared with the LC20 and LC50 treated group. A
significant variation was shown in the life expectancy (exj)
among the treated (LC20 and LC50) and untreated larvae
(Fig. 3). The maximum life expectancy of new eggs was recorded in LC50 (39.0
days), followed by LC20 (38.0 days) while the minimum life
expectancy of eggs was recorded in the untreated group (36.0 days).
Reproductive rate (vxj) is defined
as the measure of dedication to newly coming offspring in the future from age x
to stage j (Fig. 4). The contribution of males in the population to the
next generation was not well defined, therefore the curve for males was not
included. A decline was observed in the reproductive values when larvae treated
with LC50 and LC20 as compared to the untreated larvae.
Maximum vxj was recorded on the
untreated group, while the minimum was observed in LC50 treated
group.
Discussion
In the current
study, Age-stage, two-sex life table theory was utilized to calculate the
population parameters of E. vittella exposed
to the sublethal concentrations of novaluron. Age-stage, two-sex life table
study is a promising way to estimate the population parameters of the pest by
considering both the Table
1: Acute toxicity of novaluron on
the 1stinstar of E. vittella after 72 h of treatment
Chemical |
n |
Concentration mg
liter-1 (95% CL) |
Slope ± SE |
χ2
(df) |
||
|
|
LC10 |
LC20 |
LC50 |
|
|
Novaluron |
240 |
1.022
(0.534-2.156) |
2.224
(1.162-4.256) |
9.837
(5.140-18.827) |
1.304 ± 0.144 |
0.997 (5) |
LC (lethal concentration), n (number of
samples), CL (confidence level), SE (standard error), χ2 (Chi
square), df (degree of freedom)
Table
2: Life table parameters of E. vittella
treated with sub-lethal concentrations of novaluron
Treatment |
Control |
LC20 |
LC50 |
|
||||
|
n |
Mean ± SE |
n |
Mean ± SE |
n |
Mean ± SE |
||
Egg (days) |
70 |
3.66 ± 0.1b |
70 |
4.07 ± 0.094a |
70 |
4.26 ± 0.125a |
||
1st
instar (days) |
64 |
2.28 ± 0.08c |
60 |
2.33 ± 0.088b |
58 |
2.52 ± 0.094a |
||
2nd
instar (days) |
54 |
2.19 ± 0.076b |
50 |
2.20 ± 0.082b |
56 |
2.54 ± 0.096a |
||
3rd
instar (days) |
48 |
2.17 ± 0.078b |
44 |
2.36 ± 0.105a |
46 |
2.48 ± 0.106a |
||
4th
instar (days) |
46 |
2.13 ± 0.072b |
42 |
2.19 ± 0.088b |
40 |
2.53 ± 0.125a |
||
5th
instar (days) |
46 |
2.26 ± 0.094b |
40 |
2.15 ± 0.082b |
38 |
2.47 ± 0.125a |
||
Larva (days) |
46 |
11.03 ± 0.028c |
40 |
11.23 ± 0.041b |
38 |
12.54 ± 0.013a |
||
Pupa(days) |
41 |
8.74 ± 0.201b |
34 |
11.35 ± 0.15a |
31 |
11.47 ± 0.151a |
||
Male
longevity(days) |
18 |
8.52 ± 2.066a |
19 |
7.72 ± 1.56a |
16 |
7.12 ± 0.331a |
||
Female
longevity(days) |
23 |
12.7 ± 2.13a |
15 |
9.04 ± 1.21b |
14 |
7.62 ± 0.242c |
||
APOP |
23 |
1.2 ± 0.133a |
15 |
1.00 ± 0.00a |
14 |
1.00 ± 0.00a |
||
TPOP |
23 |
24.5 ± 0.619b |
15 |
28.3 ± 0.26a |
14 |
29.22 ± 0.464a |
||
Fecundity
(eggs/f) |
23 |
330.9 ± 26.41a |
15 |
268.5 ± 19.67b |
14 |
238.11 ± 14.24c |
||
LC (lethal concentration), SE (standard error), n
(number of insects exposed. Adult pre oviposition period (APOP), total pre
oviposition period (TPOP), means sharing similar letters in a row are
not different statistical at 5% probability
Table
3: Effect of sub-lethal
concentration of novaluron on the biological parameters of E. vittella
Population parameters |
Control |
LC20 |
LC50 |
|||
Mean |
SE |
Mean |
SE |
Mean |
SE |
|
Intrinsic rate
of increase (r) |
0.166a |
0.011 |
0.140b |
0.009 |
0.128c |
0.010 |
Finite rate of
increase (λ) |
1.181a |
0.013 |
1.150b |
0.010 |
1.137b |
0.011 |
Net reproductive
rate (Ro) |
94.542a |
25.23 |
76.714ab |
20.679 |
61.228b |
17.610 |
Mean generation
time (T) |
27.255c |
0.573 |
30.967b |
0.272 |
31.917a |
0.301 |
Gross
reproductive rate (GRR) |
183.42a |
8.055 |
146.45ab |
32.83 |
136.77b |
30.553 |
LC (lethal
concentration), SE (standard error), df (degree of
freedom), means sharing similar letters in a row are
not different statistical at 5% probability
sexes of the
existing population (Rahmani and Bandani
2013; Huang and Chi 2013). The intrinsic rate of increase, reproductive rate
and total oviposition period are the most important characteristics of the life
table study to predict the insect population effected by insecticides (Papachristos and Milonas 2008).
The sub-lethal
concentrations (LC20 and LC50) of novaluron for E. vittella were calculated as 2.224 and 9.837 mg L-1,
respectively in this study. Cutler et al. (2005) studied the acute toxicity of novaluron on the second
instar of L. decemlineata and calculated LC50
as 18.7 ppm and categorized it as broad-spectrum insecticides. Population
parameters of E. vittella studied in this
paper showed that the sub-lethal (LC20 and LC50)
concentrations of novaluron have decreased the intrinsic rate of increase, finite
rate of increase, reproductive value, survival rate, and net reproductive rate,
however, the larval period, pupal period and TPOP were increased by the
sub-lethal concentrations. The above results proved that the population growth
of E. vittella was significantly reduced by
the sub-lethal concentrations of novaluron. These results are according to the
sub-lethal effects of thiamethoxam on Bradysia
odoriphaga
(Zhang et al. 2015). Significantly no difference was found in the
adult pre-oviposition period (APOP) among treatments, while a significant
variation was found in the total pre-oviposition period (TPOP), which was
positively correlated with the intrinsic rate of increase of the E. vittella.
Sub-lethal concentrations significantly prolonged the larval duration, this may
have occurred because of agitations in nerve tissue development by neurotoxic
chemical contact (Desneux et al. 2007).
Similar results were found when the population of E. vittella
treated with sublethal doses of lufenuron (Hafeez et al. 2019). The
reason for the prolonged larval duration would be that the treated larvae were
more intense with the detoxification of the sub-lethal effect of novaluron
causing the increased larval period as compared to the control (Meng et al.
2018). The number of eggs per female also reduced to a significant level by the
application of sub-lethal concentrations of novaluron. This showed that the
chemical has produced some effects on the ovaries of the females in treated
groups (Seth et al. 2004; Qu et al. 2017). It has been found that
exposure of insects to insecticides results in the reduction of ovarioles size,
basal oocytes, and firmness of follicular epithelium of armyworm, which was the
main reason for reduced fecundity (Perveen and Miyata
2000). The reduction may also be due to changes in the behavioral and physiological
effects of the insecticide. The short life span of adults will result in the
short mating periods,
Fig. 1: Age-stage specific survival rate (sxj) of E. vittella
exposed to sublethal concentration of novaluron
which will
ultimately result in fewer eggs in the field and thus a decline will be found
in the field population over time. In this study, the population parameters viz., intrinsic rate of increase, gross
reproductive rate, net reproductive rate and finite rate of increase were
decreased with the LC20 and LC50 treatments. These
results are in line with the result of previous studies, in which the intrinsic
rate of increase, finite rate of increase and net reproductive rate
statistically declined in diamondback moth and cabbage aphid by the treatment
of spinosad and imidacloprid respectively (Lashkari et al. 2007; Yin et al. 2008). This
study provides a clear knowledge about the population dynamics of E. vittella
subjected to the sub-lethal effects of the insecticides. These sublethal
concentrations of novaluron can be utilized in the field to delay the
development rate and reduce the reproduction ability of the females in the pest
population. These
Fig.
2: Survival rate (lx) and fecundity of E. vittella
exposed to sublethal concentration of novaluron
concentrations
will reduce the number of insecticides used in fields, reduce the risk of
resistance development in the insect pests and reduce environmental pollution.
Conclusion
This study publicized that the novaluron with sub-lethal
concentrations significantly decreased the biological rate of E. vitella in
the laboratory conditions and advocates the implementation of such doses in the
fields for incorporation in integrated pest management strategies.
Author Contributions
DK, AG, BR and MT designed the research. DK, SK and SA
conducted the experiments. BR and DK analyzed the data. DK, BR and IH wrote the
manuscript. All the authors read and approved the manuscript.
Conflict of Interest
Authors declare that there is no
conflict of interest
Funding Source
There is no funding source for the
present research
Fig. 4: Reproductive value (Vxj)
of E. vittella exposed to sublethal
concentration of novaluron
Fig. 3: Life expectancy (exj)
of E. vittella
exposed to sublethal concentration of novaluron
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