Acta agriculturae Slovenica, 118/2, 1–8, Ljubljana 2022
doi:10.14720/aas.2022.118.2.2246 Original research article / izvirni znanstveni članek
Sublethal effects of some insecticides on the functional response of Ae-
nasius bambawalei Hayat, 2009 (Hymenoptera: Encyrtidae)
Zeinab RAFATIAN 1, Nooshin ZANDI-SOHANI 1, 2, Fatemeh YARAHMADI 1
Received June 17, 2021; accepted April 23, 2022.
Delo je prispelo 17. junija 2021, sprejeto 23. aprila 2022
1 Department of Plant Protection, Faculty of Agriculture, Agricultural Sciences and Natural Resources University of Khuzestan, Mollasani, Ahvaz, Iran
2 Corresponding author, e-mail: nzandisohani@yahoo.com; zandi@asnrukh.ac.ir
Sublethal effects of some insecticides on the functional re-
sponse of Aenasius bambawalei Hayat, 2009 (Hymenoptera: 
Encyrtidae)
Abstract: Aenasius bambawalei Hayat, 2009 is one of the 
most effective natural enemies of Phenacoccus solenopsis Tin-
sley, 1898. The sublethal effects of dimethoate, imidacloprid, 
and thiodicarb on the functional response of A. bambawalei 
to different densities of third instar nymphs of P. solenopsis 
were evaluated under laboratory conditions. Young females 
were exposed to the insecticides and then introduced to the 
host densities of 2, 4, 8, 16, 32, and 64 for 24 h. The results 
revealed a type III functional response in control and insec-
ticide treatments. The handling time and maximum attack 
rates of A. bambawalei females were adversely affected by in-
secticides. The longest handling time and the lowest value of 
maximum attack rate were observed in thiodicarb treatment, 
5.03 h and 4.76, respectively. Therefore, for the simultaneous 
application of biological and chemical control of P. solenopsis, 
the influence of insecticides on the functional response be-
havior of natural enemies must be evaluated.
Key words: parasitoid; biological control; chemical con-
trol; IPM
Subletalni učinki nekaterih insekticidov na funkcionalen 
odziv vrste Aenasius bambawalei Hayat, 2009 (Hymenopte-
ra: Encyrtidae)
Izvleček: Vrsta Aenasius bambawalei Hayat, 2009 je naj-
učinkovitejši naravni sovražnik škodljivca Phenacoccus sole-
nopsis Tinsley, 1898. Subletalni učinki dimetoata, imidaklopri-
da in tiodikarba na funkcionalni odziv vrste A. bambawalei na 
različne gostote nimf tretjega štadija škodljivca P. solenopsis 
so bili ovrednoteni v laboratorijskih razmerah. Mlade samice 
so bile izpostavljene insekticidom in nato prinešene gostitelju 
v gostotah 2, 4, 8, 16, 32, in 64 za 24 h. Rezultati so pokazali 
funkcionalni odziv tipa III pri kontroli in obravnavanjih z in-
sekticidi. Na čas obravnavanja in največji napad samic vrste 
A. bambawalei so negativno vplivala obravnavanja z insektici-
di. Najdaljši čas obravnavanja (5,03 h) in najmanjša vrednost 
maksimalnega napada (4,76) sta bila opažena pri obravnava-
nju s tiodikarbom. Zaradi tega moramo pri hkratnem biolo-
škem in kemijskem uravnavanju škodljivca P. solenopsis pred-
hodno ovrednostiti vpliv insekticidov na funkcionalni odziv 
naravnega sovražnika.
Ključne besede: parazitoid; biološki nadzor; kemijski 
nadzor; IPM
Acta agriculturae Slovenica, 118/2 – 20222
Z. RAFATIAN et al.
1 INTRODUCTION
Extensive application of synthetic insecticides has 
caused unsuitable effects on ecosystems such as insect 
resistance, pest outbreaks, pesticide residues in soil and 
products, and undesirable effects on non-target organ-
isms (Ambrose et al., 2010). On the other hand, in an 
integrated pest management (IPM) program, success 
mainly depends on the simultaneous use of chemical 
compounds and biological control agents and insec-
ticides are essential elements for pest population sup-
pression (Abedi et al., 2012). Thus, in such systems, the 
compatibility of insecticides with biocontrol agents 
is the main concern for IPM managers (Martinou & 
Stavrinides, 2015).
Parasitoid wasps can regulate the pest popula-
tion and prevent the pest outbreak (Hentz et al., 1998). 
One of the major interactions between parasitoids and 
pests that can influence pest suppression is functional 
response (Holling, 1959). In parasitoids, functional re-
sponse refers to the relationship between the number of 
hosts attack by a female parasitoid during a given time 
interval as a function of host density (Solomon, 1949). 
According to Holling (1959, 1966), there are three types 
of functional responses. In type I, the parasitoid has a 
constant search rate overall densities and the result is a 
linear response until parasitoid satiation (Hassell, 1978). 
In type II, the parasitoid response to the pest density is 
curvilinear and in higher densities changes to plateau. 
Type II response integrates parasitoid handling time, 
which defines as the time parasitoids spend for over-
coming and parasitizing a host. Moreover, parasitoid 
cleaning and resting behavior before starting to search 
for a new host are included. Type III shows a sigmoid 
curve that rises to a plateau when the parasitoid feels 
satiation. The sigmoid form is due to a slow increase in 
the attack rate of the parasitoid in higher densities of 
the host (Holling, 1959, Hassell, 1978).
Cotton mealybug, Phenacoccus soleopsis Tinsley 
(Hemiptera: Pseudococcidae), has been reported as a 
serious pest on cotton in the United States for the first 
time (Fuchs et al., 1991) and then from India and Pa-
kistan (Hodgson et al., 2008, Sahito et al., 2011). It was 
also described as a pest of Hibiscus rosa-sinensis L. in 
Nigeria and Iran (Akintola & Ande, 2008, Joodaki et al., 
2018). P. soleopsis is highly polyphagous and more than 
202 plant species are attacked across the world includ-
ing ornamentals, fruits, weeds, and field crops (Kumar 
et al., 2009, Fand & Suroshe, 2015). Several chemical in-
secticides are used for managing mealybug infestation; 
however, due to the wax covers the whole body and the 
cryptic habit of the pest, the efficiency of the method 
is limited (Fand & Suroshe, 2015). The pest is attacked 
by 23 species of predators and 7 species of parasitoids 
in Iran and all of the reported parasitoids belong to 
the family Encyrtidae (Mossadegh et al., 2015). Among 
them, only the solitary parasitoid, Aenasius bambawa-
lei Hayat is effective in suppressing the pest population 
and has a key role in its natural parasitism (Fand & 
Suroshe, 2015).
Pesticide exposure is one of the several factors 
which can influence the functional response of Natural 
enemies (Martinou et al., 2015). The effect of sublethal 
concentrations of insecticides on different parasitoids 
such as Diaeretiella rapae (McIntoch, 1855) (Hym.: Bra-
conidae) (Rezaei et al., 2014), Habrobraon hebetor Say, 
1836 (Hym.: Braconidae) (Abedi et al., 2012, Mahdavi 
et al., 2013, Rashidi et al., 2018), Dolichogenidea tasman-
ica (Cameron, 1912) (Hym.: Braconidae) (Paull et al., 
2014), and Eretmocerus mundus Mercet, 1931 (Sohrabi 
et al., 2014) have been reported in previous studies. 
Nevertheless, there is no available information on the 
sublethal effects of insecticides on A. bambawalei. In the 
current study, the sublethal effects of dimethoate, imi-
dacloprid, and thiodicarb on the functional response of 
the parasitoid wasp, A. bamabawalei, were investigated 
on P. solenopsis.
2 MATERIALS AND METHODS
2.1 INSECT REARING
Different life stages of P. solenopsis were collected 
from twigs of Hibiscus rosa-sinensis L. available at the 
campus of Agricultural Sciences and Natural Resources 
University of Khuzestan. Young potato, Solanum tu-
berosum L., sprouts (0.5-1.5 cm length) were used as a 
laboratory host of the mealybugs and the transfer was 
carried out using a fine brush. Then, the potato sprouts 
were kept in a container (24 × 10 × 16 cm) covered with 
fine mesh. The newly established colony was used in the 
experiments. 
To create the colony of A. bambawalei, the para-
sitized nymphs of P. solenopsis were collected from the 
same H. rosa-sinensis twigs. A separate container was 
used to keep the mummies until the adults’ emergence. 
While the adult parasitoids appeared in the contain-
ers they were moved by an aspirator to new containers 
containing 3rd instar nymphs of P. solenopsis. Both colo-
nies were maintained in the incubators at 27 ± 2 ᵒC, 65 
± 5 % R. H., and 14 l: 10 D h, and all the experiments 
were carried out in the mentioned conditions.
Acta agriculturae Slovenica, 118/2 – 2022 3
Sublethal effects of some insecticides on the functional response of Aenasius bambawalei Hayat, 2009 (Hymenoptera: Encyrtidae)
2.2 INSECTICIDES
Dimethoate, imidacloprid, and thiodicarb were 
tested in the experiments. Table1 shows more informa-
tion about insecticides.
2.3 FUNCTIONAL RESPONSE BIOASSAY
For these experiments, the sublethal concentra-
tions of 1, 0.5, and 25 ppm of dimethoate, imidacloprid, 
and thiodicarb were used, respectively. The cylindrical 
plastic containers (15 cm high and 7 cm diameter) were 
considered as exposure cages and impregnated to the 
insecticidal solution for 30 seconds. Distilled water was 
used as control. Then, they were allowed to dry for 24 h. 
After this time, 50 newly emerged mated female wasps 
(less than one day old) were released in each exposure 
cage for 24 h. Then, randomly selected females were 
transferred to the new containers consist of different 
densities of 2, 4, 8, 16, 32, and 64 third instar nymphs 
of P. solenpsis. The containers were transferred to the 
incubators with the above-mentioned conditions for 
24 h. Then the females were removed and the contain-
ers were kept in the incubator until the appearance 
of mummies. The number of parasitized nymphs was 
recorded. Ten replications were considered for this ex-
periment.
2.4 STATISTICAL ANALYSIS
Logistic regression analysis of the proportion of 
host-parasitoid (Na/N0) as a function of host density 
(N0) was used to determine the functional response 
type of A. bamabawalei as recommended by Juliano 
(2001).This was done by fitting the below polynomial 
function:
(1)
Where Na is the number of parasitized hosts, N0 is 
the initial number of hosts offered, and P0, P1, P2, and 
P3 are intercept, linear, quadratic, and cubic parameters, 
respectively. These parameters were calculated using 
the method of maximum likelihood (PROC CATMOD, 
SAS Institute, 2001). If the linear parameter (P1) is neg-
ative, the type of functional response is II, whereas a 
positive linear parameter reveals a type III functional 
response (Juliano, 2001). 
In the second step, a nonlinear least-squares re-
gression (PROC NLIN; SAS Institute Inc., 2001) was 
used to calculate the functional response parameters 
(Th and either a for type II functional response or b, 
c, and d for type III functional response) using Rog-
er’s random parasitoid equation (Rogers, 1972; Juliano, 
2001). The parameters were estimated according to the 
following equations: 
 (2)
where Na is the number of parasitized hosts, N0, 
the initial number of hosts,  is the instantaneous search-
ing efficiency (attack rate), T is the total amount of time 
available for searching (24h), and  is the handling time. 
For modeling the type III functional response, the 
searching efficiency (a) in equation (2) was substituted 
with equation (3) with a function of host density. 
 (3)
Where a, b, c, and d are constants and must be es-
timated. In cases where both d and c were not signifi-
cantly different from 0; the case observed in this study, 
led to a = bN0 which was inserted into Equation (2). 
This yielded the following formula (Hassell, 1978): 
 (4)
Since thedata from the above experiment fitted the 
type III functional response, the functional response 
parameters were obtained using (3) and (4).
The maximum attack rate (T/Th) which indicates 
the maximum number of hosts that can be parasitized 
by an individual parasitoid during 24 h, was estimated 
using calculated Th (Hassell, 2000).
DosageFormulationCompanyActive ingredientInsecticide
0.5 ppm35 % SCAria ChimiImidaclopridConfidor®
1 ppm40 % ECKimiyaGohareKhakDimethoateRoxion®
25 ppm80 % DFMoshkfam Fars ThiodicarbLarvin®
Table 1: Information about experimental insecticides
Acta agriculturae Slovenica, 118/2 – 20224
Z. RAFATIAN et al.
plained the functional response of A. bambawalei in all 
treatments (Table 3).
The maximum number of 3rd instar nymphs that 
could be parasitized by A. bambawalei (T/Th) decreased 
from 8.35 in control to 6.49, 4.88, and 4.76 in imidaclo-
prid, dimethoate, and thidicarb, respectively (Table 3). 
4 DISCUSSION
Pesticides are prevalent elements in integrated 
pest management programs and the study of their be-
havioral effects such as functional response on natural 
enemies can be helpful for the success of IPM. Accord-
ing to the results of the current study, the functional 
response of A. babmawalei in control and insecticide 
treatments was of type III. Parasitoids with type III 
functional response are density-dependent and can in-
crease their search rate on higher densities of the host. 
Although a previous overview on functional response 
indicated that type II is more common in parasitoids 
(Fernandez-arhex & Corley, 2003), several studies in-
dicate type III in parasitoid wasps such as Eretmocerus 
mundus Mercet on Bemisia tabaci Gennadius, 1889 
(Sohrabi et al., 2014), Aphidius colemani Viereck, 1912 
on Aphis gossypii Glover, 1877 (Van Steenis & El-Wha-
wass, 1995) and Praon volucre (Haliday, 1833) on Myzus 
persicae (Sulzer, 1776) (Tazerouni et al., 2016). Accord-
ing to an earlier study, type II functional response was 
3 RESULTS
The logistic regression analysis of the proportion 
of P. solenopsis parasitized by A. babmawalei indicated 
Type III functional response for this parasitoid in con-
trol and all insecticidal treatments. The linear coeffi-
cient, P1, was positive and the quadratic coefficient, P2, 
was negative in all treatments (Table 2).
Therefore, the proportion of host parasitized was 
density-dependent, which shows a type III functional 
response (Figure 1).
Roger’s random parasitoid equation was used for 
data analysis in control and other treatments. Accord-
ing to the results of nonlinear least square regression 
parameters, c and d were not significantly different 
from zero; therefore, they were removed from the mod-
el and a reduced model was used (Equation 4). Estimat-
ed b values for the control, dimethoate, imidacloprid, 
and thiodicarb were 0.00620, 0.00304, 0.00344, and 
0.00267, and estimated handling times in these treat-
ments were 2.87, 4.92, 3.70, and 5.03 h, respectively (Ta-
ble 3). Comparing the asymptotic 95 % confidence of 
b values in Table 3 indicated that imidacloprid had no 
significant effect on the value of the b of A. bambawa-
lei; however, it was significantly reduced in dimethoate 
and thiodicarb treatments. Nevertheless, handling time 
(Th) significantly increased in all insecticide treatments. 
The values of r2, coefficient of determination, revealed 
that Rogers’s random parasitoid equation properly ex-
P valueSEEstimateParametersTreatment
0.21050.3778-0.4730P0 (Constant)Control
0.36140.05780.0528P1 (Linear)
0.11890.00220-0.00344P2 (Quadratic)
0.10550.000022-0.000035P3 (Cubic)
0.00040.4598-1.6313P0 (Constant)Dimetoat
0.21600.06890.0853P1 (Linear)
0.13660.00261-0.00388P2 (Quadratic)
0.16190.0000260.000036P3 (Cubic)
0.00750.4118-1.1003P0 (Constant)Imidacloprid
0.29190.06250.0659P1 (Linear)
0.14080.00238-0.00350P2 (Quadratic)
0.14580.0000240.000034P3 (Cubic)
0.00140.4536-1.4500P0 (Constant)Thiodicarb
0.47870.06890.0488P1 (Linear)
0.34210.00262-0.00249P2 (Quadratic)
0.38940.0000260.000022P3 (Cubic)
Table 2: Maximum likelihood estimates from logisitic regression analysis of the proportion of third instar nymphs of Pheno-
coccus solenopsis parasitized by Aenasius bambawalei as a function of initial host density
Acta agriculturae Slovenica, 118/2 – 2022 5
Sublethal effects of some insecticides on the functional response of Aenasius bambawalei Hayat, 2009 (Hymenoptera: Encyrtidae)
Figure 1: Functional response of A. bambawalei to different densities of 3rd instar nymphs of P. solenopsis in different insecti-
cide treatments. From the top: dimethoate, thiodicarb, imidacloprid, and control treatments. Symbols are observed data and 
lines were predicted by the model (Equation 2)
Acta agriculturae Slovenica, 118/2 – 20226
Z. RAFATIAN et al.
recorded for A. bambawalei to different densities of P. 
solenopsis at selected temperatures which is varied from 
the results of our study (Joodaki et al., 2018). Several 
factors including difference in experimental conditions, 
parasitoid strain, host plant cultivar, host species, the 
age of parasitoid and host, physiological state of the 
host may be responsible for the change of functional 
response type in parasitoid wasp (Sagarra et al., 2001, 
Ambrose et al., 2010, Asadi et al., 2012, Pasandideh et al., 
2015, Tazerouni et al., 2016, Joodaki et al., 2018). In this 
study, the type of functional response did not change 
depending on different insecticide treatments. There is 
no available information about other studies reporting 
the effects of insecticides on the functional response of 
A. bambawalei. On the other hand, Habrobracon hebetor 
Say, 1836 showed type III functional response to dif-
ferent densities of Anagasta kuheniella Zeller, 1879 in 
control and all insecticide treatments (Mahdavi et al., 
2013). In another study, the type of functional response 
of Diaretiella rapae (McIntosh) did not change when it 
was exposed to primicarb and thiamethoxam (Rezaei et 
al., 2014). However, Sohrabi et al. (2014) reported an al-
teration in type III functional response of Eretmocerus 
mundus Mercet in control treatment as well as imida-
cloprid to type II in buprofezin treatment. Moreover, 
the sublethal concentrations of primicarb, cyperme-
thrin, and dimethoate changed the functional response 
of D. rapae from type II to type III (De-Jiu et al., 1991).
Handling time (the time needed to subdue and 
consume the prey item) and attack rate are important 
parameters used to assess the parasitoid functional 
response (Juliano, 2001). In this study, all insecticides 
had a significant negative effect on the handling time 
of parasitoids; however, the influence of thiodicarb was 
r2T/Th  Th  bTreatments
0.968.352.87 ± 0.0980
(2.6781-3.0704)
0.00620 ± 0.00103
(0.00484- 0.00825)
Control
0.964.884.92 ± 0.3197
(4.2774-5.7773)
0.00304 ± 0.000881
(0.00128-0.00480)
Dimethoate
0.866.493.70 ± 0.2602
(3.1747-4.2163)
0.00344 ± 0.00106
(0.00131-0.00556)
Imidacloprid
0.884.765.03 ± 0.3203
(4.3940-5.6765)
0.00267 ± 0.000740
(0.00119-0.00415)
Thiodicarb
Table 3: Parameters (± SE) estimated by random parasitoid 
equation indicating functional response of A. bambawalei to 
different treatments
The values in parentheses are 95 % confidence intervals; b: constant; 
Th: handling time; T/Th maximum attack rate
even higher than the other insecticides and had the 
most adverse effect on the host-finding of the para-
sitoid. The difference in handling time in insecticide 
treatments may be due to their various mode of action, 
which influence the neural system of parasitoids. The 
longer handling time in parasitoids exposed to insecti-
cides could be related to the commotion of their neu-
ral system (Rezaei et al., 2014). An increase in handling 
time under insecticide treatments has been reported in 
different parasitoids such as H. hebetor when exposed 
to spinosad (Dastgersi, 2009), and cypermethrin (Abedi 
et al., 2012). 
Among all insecticide treatments, dimethoate and 
thiodicarb had the most, and imidacloprid had the least 
negative effect on the value of maximum attack rate of 
the wasp. The parasitism rate of A. bambawalei in imida-
cloprid treatment was 1.3 times more than dimethoate 
and thiodicarb; however, in control, it was distinctly 
higher than insecticide treatments. Insecticides can 
cause a repellent effect on parasitoids or decrease their 
host finding ability due to boosting disturbance and re-
ducing the olfactometric abilities, which may result in 
a reduction in parasitism rate (Decourtye et al., 2004).
5 CONCLUSIONS
The results confirmed the negative impact of in-
secticides on the functional response of parasitoids and 
probably the success of biological control programs. 
Hence, for the simultaneous application of biological 
and chemical control in integrated pest management 
programs, the influence of insecticides on the differ-
ent behavior of natural enemies such as functional re-
sponse has to be evaluated. Such information is essen-
tial to estimate the appropriate time to release natural 
enemies in the case of using insecticides.
6 ACKNOWLEDEMENTS
The authors would like to thank Agricultural Sci-
ences and Natural Resources University of Khuzestan, 
Iran, for the financial support of this research project.
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