ECOLOGY AND POPULATION BIOLOGY

Assessing Compatibility of the Predatory Mite Typhlodromus

bagdasarjani (Acari: Phytoseiidae) and Resistant Eggplant
Cultivar in a Tritrophic System
MOSTAFA KHANAMANI, YAGHOUB FATHIPOUR,1 AND HAMIDREZA HAJIQANBAR
Department of Entomology, Faculty of Agriculture, Tarbiat Modares University, P. O. Box 14115-336, Tehran, Iran.

Ann. Entomol. Soc. Am. 108(4): 501–512 (2015); DOI: 10.1093/aesa/sav032

ABSTRACT The fitness and population dynamics of predators depend on the quality of host plants
consumed by their prey. In this study, age-stage, two-sex life table parameters and predation rate of
Typhlodromus bagdasarjani Wainstein & Arutunjan were determined on two-spotted spider mite reared
on susceptible (‘Isfahan’) and resistant (‘Neishabour’) eggplant cultivars under laboratory conditions at
25 6 1 C, 60 6 5% relative humidity, and a photoperiod of 16:8 (L:D) h. The means, variances, and stan-
dard errors of the life table and predation parameters were estimated using the bootstrap resampling
procedure. The value of the intrinsic rate of increase (r) of this predator on the susceptible eggplant culti-
var (0.1538 d1) was significantly higher than that on the resistant one (0.1175 d1). The value of the net
reproductive rate (R0) on the susceptible and resistant eggplant cultivars was 7.55 and 8.21 offspring,
respectively. In addition, the mean generation time (T) was 12.97 and 17.75 d, respectively. The age-
stage-specific predation rate (cxj) of all stages of the predator on the resistant eggplant cultivar was higher
than that on the susceptible one. In addition, the value of net predation rate (C0) on the susceptible and
resistant eggplant cultivars was 193.05 and 221.44 preys per predator, respectively. In addition, the value
of finite predation rate (x) on the resistant cultivar (7.005 preys per predator per day) was significantly
higher than that on the susceptible one (6.361 preys per predator per day). In conclusion, due to higher
finite predation rate on the resistant eggplant cultivar, the performance of the predator on this cultivar
was more than that on the susceptible one.

KEY WORDS eggplant, two-sex life table, consumption rate, finite predation rate, Typhlodromus
bagdasarjani

Integrated pest management (IPM) is a systemic
approach in which interacting components (mainly
control measures) act together to maximize the advan-
tages (mainly producing a profitable crop yield) and
minimize the disadvantages (mainly causing risk to
human and environment) of pest control programs
(Fathipour and Sedaratian 2013). IPM has also been
defined as a pest population management system that
uses all suitable techniques in a compatible manner to
reduce pest populations and maintain them at levels
below those causing economic injury (Kogan 1998).
A fundamental component of an IPM program for any
crop is an understanding of the compatibility of control
tactics that we will integrate to control a target pest.
Eggplant, Solanum melongena L. (Solanaceae), is
grown in both fields and greenhouses worldwide and is
one of the main vegetables in Iran (Khanamani et al.
2012). This crop is attacked by various pests including
spider mites, especially the two-spotted spider mite,
Tetranychus urticae Koch. Due to biological character-
istics, its control by using common methods with
1
Corresponding author, e-mail: fathi@modares.ac.ir.
C The Authors 2015. Published by Oxford University Press on behalf of Entomological Society of America.
V
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emphasis on chemicals has not been successful. Inte-
grated management with focus on combination of
biological control agents and resistant plants can
be one of the efficient strategies to manage this pest
(Khanamani et al. 2014). Predatory mites of the family
Phytoseiidae are economically important predators of
phytophagous mites and insects in greenhouse crops.
Because of high ability of phytoseiid predatory mites in
control of two-spotted spider mite, several species of
them have been produced commercially worldwide,
and used for two-spotted spider mite control. Typhlo-
dromus bagdasarjani Wainstein & Arutunjan is an
effective predator of phytophagous mites and is an
indigenous widespread species of the Middle East with
high efficiency (Ganjisaffar et al. 2011a, Moghadasi
et al. 2014).
Biological control and host plant resistance are often
combined in integrated pest management programs
and are classically considered to be compatible. How-
ever, the interactions among plants, herbivores, and
natural enemies are tightly entwined. Plant chemistry
can have profound bottom-up effects on the interac-
tions between herbivores and their natural enemies.
Therefore, differences in the quality of host plants may
in turn affect the top-down force strength, either in a
positive or a negative way (Hunter 2003, Soufbaf et al.
502 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA
2012, Khanamani et al. 2014). Numerous studies
suggested negative associations between plant chemis-
try and biological control agent fitness (e.g., Gunasena
et al. 1990, Reitz and Trumble 1997, Ode et al. 2004).
Hence, the study of interactions between host plant
cultivars and biocontrol agents is important in inte-
grated pest management programs (Fathipour and
Sedaratian 2013).
The life table parameters are powerful tools for
analyzing and understanding the impact of an external
factor like host plant quality (e.g., Wermelinger et al.
1991, Golizadeh et al. 2009), temperature (e.g., Tani-
goshi et al. 1975, Kheradmand et al. 2007), and
pesticide sublethal doses (e.g., Jones and Parrella 1984;
Hamedi et al. 2010, 2011, Alinejad et al. 2014) on
growth, survival rate, reproduction, and increased rate
of a biocontrol agent population. Female age-specific
life table of T. bagdasarjani has been constructed on
two-spotted spider mite reared on susceptible and re-
sistant eggplant cultivars (Khanamani et al. 2014). In
the female age-specific life table, only female individ-
uals are taken into consideration and any variable de-
velopmental rate among individuals is ignored.
However, there are many differences between male
and female in longevity, survival rate, predation rate,
and pesticide susceptibility. The two-sex life table is ca-
pable of precise calculation of the age and stage struc-
ture of a two-sex population (Chi 1988), and it provides
the actual control efficiency of the entire population,
i.e., both sexes are included. Thus, use of two-sex life
table can be extremely helpful in biological control
decisions.
The use of standard parameters for describing and
comparing predation potential of predators is important
in biological control programs. Intrinsic rate of increase
(r) is an appropriate index for describing and compar-
ing growth potential of populations. The predation
potential of predators cannot be properly described
using intrinsic rate of increase alone (Chi et al. 2011).
To accurately evaluate the effect of predation in a pred-
ator–prey system, we need not only to assess the
growth potential of the predator but also its predation
potential. Chi et al. (2011) pointed out that the finite
predation rate can be the standard parameter by
linking the finite rate of increase (k), stable age-stage
distribution (axj), and age-stage-specific predation rate
(cxj). The finite predation rate takes both the intrinsic
rate of increase of predator and the age-stage specific
predation rate into consideration and then can be used
to describe and compare the predation potentials of
natural enemies used in biological control programs.
The finite predation rate can be used for comparison of
predation capacity among different predators under
the same condition or predation of a predator under
different conditions (Yu et al. 2013).
For implementation of integrated management pro-
grams against two-spotted spider mite in eggplant
fields, it is necessary to evaluate compatibility of inte-
grated components (biological agent and host plant
resistance). Therefore, the aim of this study was to
compare age-stage two-sex life table parameters and
predation rate of the predatory mite, T. bagdasarjani,
Vol. 108, no. 4
on the resistant (‘Neishabour’) and susceptible (‘Isfa-
han’; as control) eggplant cultivars.
Materials and Methods
Plant Cultivation. Our previous study comparing
seven eggplant cultivars indicated that Neishabour was
the least suitable for development and reproduction of
two-spotted spider mite, whereas Isfahan was the most
suitable cultivar (Khanamani et al. 2013). Seeds of the
susceptible (Isfahan) and resistant (Neishabour) egg-
plant cultivars were obtained from Seed and Plant
Improvement Institute, Karaj, Iran. The seeds were
sown in 20-cm plastic pots filled with fertilized field
soil and maintained in the greenhouse condition. Dur-
ing the experiments, no pesticides or additional fertil-
izers were used.
Stock Cultures of Mites. To provide the stock
cultures, the individuals of T. bagdasarjani were origi-
nally collected from leaves of a mulberry tree located
in campus of Faculty of Agriculture, Tarbiat Modares
University, Tehran, Iran, and the individuals of two-
spotted spider mite were obtained from the Iranian
Research Institute of Plant Protection, Tehran, Iran.
The two-spotted spider mite colony was maintained on
planted beans (Phaseolus vulgaris variety Khomein) in
a greenhouse at 27 6 5 C, with natural humidity and
photoperiod. Then, offspring of this colony were reared
on eggplant cultivars (susceptible and resistant) for two
generations before conducting the experiments. Also,
the individuals of T. bagdasarjani were transferred onto
detached bean leaves infested with the different stages
of two-spotted spider mite as prey maintained in
a growth chamber at 25 6 1 C, 65 6 5% relative
humidity (RH), and a photoperiod of 16:8 (L:D) h.
Before beginning the experiments, the offspring of the
predator were reared for one generation on two-
spotted spider mite fed on the susceptible and resistant
eggplant cultivars, separately. To provide colonies on
these cultivars, the leaf discs taken from leaves of each
cultivar were used. Each leaf disc was placed with the
upper surface facing down on a cotton layer in a Petri
dish (6 cm in diameter), in which a 5-mm-diameter
hole was drilled. The leaf margin was surrounded by a
cotton strip to prevent the escape of mites. The pre-
pared Petri dishes were kept in larger dishes (8 cm in
diameter). Water was added daily to the larger dishes
to keep the leaves fresh.
Experimental Setup. All experiments were carried
out under laboratory conditions at 25 6 1 C, 60 6 5%
RH, and a photoperiod of 16:8 (L:D) h. To obtain the
same-aged eggs of T. bagdasarjani, 30 pairs of both
sexes of the predator were transferred from the condi-
tioned colonies onto a leaf disc of each cultivar. After
24 h, the deposited eggs were transferred individually
to the experimental units up to 80 replicates per treat-
ment. The experimental units were similar to those
used for predator culture, but in a smaller scale. The
3-cm-diameter Petri dishes were placed in larger ones
(6 cm in diameter) containing water. These experimen-
tal units were checked daily using a stereomicroscope,
and the development and survivorship of the different
July 2015 KHANAMANI ET AL.: Typhlodromus bagdasarjani AND RESISTANT EGGPLANT 503

immature stages were monitored. After emergence of age x and according Chi and Yang (2003) and Yu et al.
adults, females were coupled with males obtained in (2005) was calculated as follows:
the same experiment or taken from the colony on the
same cultivar. The couples were kept together up to Pb
the end of the study. The daily observations continued j¼1 sxj cxj
until the death of the last individual.
kx ¼ Pb (1)
Estimating Age-Stage, Two-Sex Life Table j¼1 sxj
Parameters. The life history data of all individuals
were analyzed according to the age-stage, two-sex life where b is the number of life stages. In addition, the
table theory (Chi 1988). The age-stage-specific survival age-specific net predation rate (qx) was calculated as
rate (sxj) (where x ¼ age in days and j ¼ stage); the age- follows:
stage-specific fecundity (fxj) or f(x, female) (daily
number of eggs produced per female of age x); the qx ¼ lx kx (2)
age-specific survival rate (lx) (includes both male and
female); the age-specific fecundity (mx) (daily number According to Chi and Yang (2003), the net predation
of eggs produced per individual, i.e., this number is rate (C0) gives the mean number of prey consumed by
divided by all individuals (males and females) of age x); an average individual predator during its entire life
and the population growth parameters (the intrinsic span, and is calculated as:
rate of increase (r); finite rate of increase (k); gross
reproductive rate (GRR); net reproductive rate (R0),
and mean generation time (T)) are calculated accord-
P
1 P
b
C0 ¼ sxj cxj (3)
ingly (Safuraie-Parizi et al. 2014, Goodarzi et al. 2015). x¼0 j¼1
Data analysis and population parameters were calcu-
lated by using the TWOSEX-MSChart program According to these, the total number of prey consumed
(Chi 2013b). The means and standard errors of the by a cohort of size N is calculated as NC0 .
population parameters were estimated by using the The transformation rate from prey population to
bootstrap procedure (Huang and Chi 2013). In addi- predator offspring (Qp) is the mean number of preys
tion, the life table bootstrap-values of T. bagdasarjani that a predator needs to consume to produce an off-
on the susceptible and resistant eggplant cultivars were spring (Chi et al. 2011), and is calculated as:
compared with t-tests using the TWOSEX-MSChart
program.
Prey Consumption. Two-spotted spider mite C0
Qp ¼ (4)
immature individuals (except eggs) were used as a food R0
source in this experiment because T. bagdasarjani pref-
erentially feeds on the nymphal stage of its prey. To The stable predation rate (w) is the total predation
evaluate prey consumption of different immature capacity of a stable population whose total size is one
stages of T. bagdasarjani on two-spotted spider mite (Chi et al. 2011), and is calculated as follows:
reared on the susceptible and resistant eggplant culti-
vars, 15 prey nymphs were added daily to the experi-
P
1 P
b
mental units (Ganjisaffar et al. 2011b). These w¼ axj cxj (5)
experimental units were checked once a day, and the x¼0 j¼1
number of prey consumed by predators was counted
using a stereomicroscope. After recording prey con- where axj is the proportion of individuals belonging to
sumption, the same number of new prey was added age x and stage j in a stable age-stage distribution.
onto each disc. After the emergence of adult predators, Because the predator population itself will increase
the males and females were paired and 40 prey at the finite rate k, the total number of prey
nymphs were added daily to the experimental units for consumed will increase as kw. The finite predation rate
feeding of each pair (Ganjisaffar et al. 2011b). (kw ¼ x) describes the predation potential of a preda-
The number of consumed preys was recorded until tor population by combining its growth rate (k),
the death of both mites. Prey consumption of age-stage consumption rate (cxj), and stable age-stage
adult predators was related to the male and female structure (axj) (Chi et al. 2011), and is calculated as
together and share of each individual was considered to follows:
be 50/50.
Predation Rate Analysis. The daily consumption P
1 P
b
of all individuals, including males, females, and those x ¼ kw ¼ k axj cxj (6)
dying before the adult stage, was used to calculate the x¼0 j¼1
age-stage specific consumption rate (cxj). This is the
mean number of two-spotted spider mite consumed by Considering this, the intrinsic predation rate is
individual T. bagdasarjani age x and stage j. The age- calculated as lnðxÞ. In other words, the predation
specific predation rate (kx) is the mean number of two- capacity will increase exponentially
spotted spider mite consumed by T. bagdasarjani at (x ¼ eðintrinsic predation rateÞ ).
504 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA
Predation rate data were analyzed using the
computer program CONSUME-MSChart (Chi 2013a).
The means, variances, and standard errors of predation
parameters were estimated using the bootstrap resam-
pling method. In addition, the predation bootstrap-
values of T. bagdasarjani on the susceptible and
resistant eggplant cultivars were compared with t-tests
using the CONSUME-MSChart program. In addition,
the Excel software was used to draw figures.
Regression and Correlation Analysis. Relation-
ship between age and consumption rate of T. bagdasar-
jani throughout its life span on the susceptible and
resistant eggplant cultivars was determined with regres-
sion analysis using SPSS 16 software. In addition, cor-
relation between total prey consumption of adult
females and their total fecundity was examined using
SPSS 16 software.
Results
Two-Sex Life Table Parameters. According to
the age-stage, two-sex life table theory, the population
parameters were calculated based on data of the entire
cohort (Table 1). The value of the intrinsic rate of
increase (r) of T. bagdasarjani on the susceptible egg-
plant cultivar (0.1538 d1) was significantly higher than
that on the resistant one (0.1175 d1). The value of the
finite rate of increase (k) was 1.1665 and 1.1248 d1 on
the susceptible and resistant eggplant cultivars, respec-
tively. The value of the net reproductive rate (R0) of
this predator on the susceptible and resistant eggplant
cultivars was 7.55 and 8.21 offspring, respectively. Also,
the value of the gross reproductive rate (GRR) on the
susceptible and resistant eggplant cultivars was 9.57
and 13.24 offspring, respectively. In addition, the mean
generation time (T) on the susceptible and resistant
eggplant cultivars was 12.97 and 17.75 d, respectively.
Mortality and Fecundity Curves. The age-stage-
specific survival rate (sxj) of T. bagdasarjani shows the
probability that a newborn will survive to age x and
develop to stage j (Fig. 1). The probability that a new-
born egg survived to the adult stage was 0.5 and 0.31
for males and 0.38 and 0.41 for females on Isfahan and
Neishabour, respectively. In addition, stage mortality of
T. bagdasarjani on the susceptible and resistant egg-
plant cultivars is presented in Table 2. According to
these results, immature mortality of T. bagdasarjani on
the resistant eggplant cultivar was higher than that on
the susceptible one.
The age-specific survivorship (lx), age-specific
fecundity (mx), and age-stage-specific fecundity (fxj) of
T. bagdasarjani fed on two-spotted spider mite reared
on the susceptible and resistant eggplant cultivars are
shown in Fig. 2. It showed that T. bagdasarjani could
successfully survive and reproduce on the susceptible
and resistant eggplant cultivars. The age-specific survi-
vorship (lx) shows the probability that a newborn indi-
vidual will survive to age x and is calculated by pooling
all individuals of both sexes. The curve of lx is a simpli-
fied version of the curves in Fig. 1. Age-specific
fecundity (mx) is the mean number of offspring pro-
duced by individual at age x. But age-stage-specific
Vol. 108, no. 4
Table 1. The mean (6SE) two-sex life table parameters of T.
bagdasarjani on two-spotted spider mite reared on the susceptible
(Isfahan) and resistant (Neishabour) eggplant cultivars
Parameters Susceptible (Isfahan) Resistant (Neishabour) t-value
R0 (offspring) 7.55 6 1.74a 8.21 6 1.69a 1.813
GRR (offspring) 9.57 6 2.26a 13.24 6 2.53a 7.309
r (d1) 0.1538 6 0.0194a 0.1175 6 0.0132b 10.280
k (d1) 1.1665 6 0.0225a 1.1248 6 0.0148b 9.383
T (d) 12.97 6 0.45b 17.75 6 0.46a 47.160
The means followed by the same letter in each row are not signifi-
cantly different (t-test, P < 0.05).
fecundity (fxj) indicated the mean number of offspring
produced by individuals of the age x and stage j.
Because only females produce offspring, there is only
the single curve f(x, female). In other words,
f(x, female) is daily number of offspring produced per
females age x. Therefore, the value of fxj is greater than
mx in most of the time. According to these curves, the
start of oviposition of the first female on the susceptible
and resistant eggplant cultivars occurred at the age of 5
and 7 d, respectively.
Age-Stage-Specific Predation Rate. Age-
stage-specific predation rate (cxj) of T. bagdasarjani on
the susceptible and resistant eggplant cultivars is shown
in Fig. 3. Age-stage-specific predation rate is the mean
number of two-spotted spider mite consumed by indi-
vidual T. bagdasarjani at age x and stage j. For the non-
predatory stages (e.g., egg and larva), their predation
rate (cxEgg and cxLarva) are zero. In addition, total age-
stage-specific predation rate is shown in Fig. 4, and
defined as the total number of two-spotted spider mite
consumed by all individuals of T. bagdasarjani at age
x and stage j. According to the obtained results, the
larvae of this predator did not feed during the experi-
ment on the both susceptible and resistant eggplant
cultivars. Predator consumption rates on the both
susceptible and resistant eggplant cultivars increased
with increasing age, and the highest daily consumption
rate was related to adult female of the predator. But
in general, the daily feeding of all stages of the
predator on the resistant cultivar was more than the
susceptible one.
Age-Specific Predation Rate and Age-Specific
Net Predation Rate. Age-specific predation rate (kx)
and age-specific net predation rate (qx) of T. bagdasar-
jani on the susceptible and resistant eggplant cultivars
are shown in Fig. 5. The age-specific predation rate is
the mean number of two-spotted spider mite con-
sumed by T. bagdasarjani at age x. By considering the
survivorship, the age-specific net predation rate
(qx ¼ lxkx) can be defined as the weighted number of
prey consumed by a predator at age x.
Net Predation Rate and Transformation
Rate. Net predation rate (C0) and transformation rate
from prey population to predator offspring (Qp) of
T. bagdasarjani on the susceptible and resistant egg-
plant cultivars are shown in Table 3. Net predation rate
gives the mean number of prey consumed by an aver-
age individual predator during its entire life span.
July 2015 KHANAMANI ET AL.: Typhlodromus bagdasarjani AND RESISTANT EGGPLANT 505

Fig. 1. Age-stage survival rate (sxj) of T. bagdasarjani on two-spotted spider mite reared on susceptible (Isfahan) and
resistant (Neishabour) eggplant cultivars.

Table 2. Stage mortality (%) of T. bagdasarjani on two-spotted

was higher than that on the susceptible one (25.56
spider mite reared on susceptible (Isfahan) and resistant (Neisha- preys).
bour) eggplant cultivars Stable, Intrinsic, and Finite Predation
Rates. Stable predation rate (w) and finite predation
Cultivars Egg Larva–nymph Female Male rate ðxÞ of T. bagdasarjani on the susceptible and
resistant eggplant cultivars are shown in Table 3. The
Isfahan (susceptible) 0 11.9 38.1 50.0
Neishabour (resistant) 6.2 22.4 40.8 30.6
stable predation rate on the susceptible and resistant
eggplant cultivars was 5.454 and 6.227 preys per preda-
tor, respectively. In addition, the value of finite preda-
tion rate ðxÞ on the resistant cultivar (7.005 preys
The net predation rate (C0) of the predator on the per predator per day) was significantly higher than that
susceptible and resistant eggplant cultivars was 193.05 on the susceptible one (6.361 preys per predator per
and 221.44 preys, respectively. The transformation rate day). These results indicated that if the predator popu-
is defined as the mean number of preys that a predator lation is stable and the predator number is one, the
needs to consume to produce an offspring. The trans- predation capacity on the susceptible and resistant egg-
formation rate from prey population to predator plant cultivars will be 6.361 and 7.005 preys per day,
offspring on the resistant eggplant cultivar (27.92 preys) respectively. In addition, the intrinsic predation rate on
506 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 108, no. 4

Fig. 2. Age-specific survivorship (lx), age-specific fecundity (mx), and age-stage-specific fecundity (fxj) of T. bagdasarjani
on two-spotted spider mite reared on susceptible (Isfahan) and resistant (Neishabour) eggplant cultivars.

the susceptible and resistant eggplant cultivars was Discussion

1.850 and 1.946 preys per predator per day,
respectively.
Regression and Correlation. Consumption rate
data of T. bagdasarjani throughout its life span on both
the susceptible and resistant eggplant cultivars are fit-
ted to the cubic regression model (Fig. 6). The regres-
sion models explained 94.6% and 98.6% of variation on
the susceptible and resistant cultivars, respectively.
In addition, the obtained results from the correlation
analysis showed a positive relationship (at the 0.01 level)
between total prey consumption of adult females of
T. bagdasarjani and their total fecundity on both the sus-
ceptible and resistant eggplant cultivars. However, the
correlation coefficient (r) on the susceptible cultivar
(0.788) was higher than that on the resistant one (0.583).
The population dynamics of predators depends on
the quality of host plants consumed by herbivores. The
secondary metabolites in plant tissues can directly
affect the growth and development of herbivores (Sol-
eimannejad et al. 2010, Soufbaf et al. 2010, Karimi
et al. 2012), and they can indirectly affect performance
of their natural enemies. The negative impact of host
plant chemistry on natural enemy fitness includes
reducing survivorship, clutch size, body size, and
fecundity (Ode 2006). Therefore, herbivores on differ-
ent host plants often differ in their susceptibility to nat-
ural enemies (Lill et al. 2002, Zvereva and Rank 2003).
Thus, it is necessary to study interactions among differ-
ent host plant cultivars and biological control agents
before implementation of a biological control program.
July 2015 KHANAMANI ET AL.: Typhlodromus bagdasarjani AND RESISTANT EGGPLANT 507

Fig. 3. Age-stage predation rate (cxj) of T. bagdasarjani on two-spotted spider mite reared on the susceptible (Isfahan)
and resistant (Neishabour) eggplant cultivars.

The obtained results in current study indicated that
different eggplant cultivars (susceptible and resistant)
can affect performance of T. bagdasarjani, either in
a positive or negative way. The results revealed adverse
effects of two-spotted spider mite reared on the resist-
ant eggplant cultivar on the predatory mite T. bagdasar-
jani survivorship and population growth rate compared
with those reared on the susceptible cultivar. In addi-
tion, reproductive performance and immature survival
rate of T. bagdasarjani was lower on the resistant egg-
plant cultivar than those on the susceptible one. The
observed differences could be due to differing morpho-
logical and chemical composition of the herbivores’
host plants (susceptible and resistant eggplant
cultivars). If secondary plant compounds are responsi-
ble for the differences between eggplant cultivars in
suitability for two-spotted spider mite, these com-
pounds are also toxic for T. bagdasarjani in which the
concentrated compounds in the nymph of two-spotted
spider mite affected this predator.
The intrinsic rate of increase (r) of arthropod popula-
tions depends on species-specific life table parameters
such as age-specific survivorship, time to first reproduc-
tion, daily fecundity, and sex ratio (Carey 1993). The age
of first reproduction plays an important role in the
intrinsic rate of increase. If fecundity remains constant,
a shorter preoviposition period will result in a higher
intrinsic rate of increase. In our study, T. bagdasarjani
508 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA
Fig. 4. Total age-stage predation rate of T. bagdasarjani on two-spotted spider mite reared on the susceptible (Isfahan)
and resistant (Neishabour) eggplant cultivars.
fed on two-spotted spider mite reared on the susceptible
eggplant cultivar had shorter total preoviposition period
and higher daily fecundity, so the obtained intrinsic rate
of increase (r) on the susceptible eggplant cultivar was
higher than that estimated on the resistant one.
Our results indicated a difference between the same
life table parameters of T. bagdasarjani estimated by
two-sex (this study) and female-based (Khanamani
et al. 2014) methods. These differences are due to the
fact that the age-stage, two-sex life table includes the
male populations but the female age-specific life table
deals only with female populations. In other words,
female age-specific life table neglects the male popula-
tion as well as the variable developmental rate among
individuals; therefore, the stage overlapping, stage mor-
tality, and male survival rate could not be calculated.
In spite of these differences between female and
two-sex methods, the intrinsic rate of increase (r) of
Vol. 108, no. 4
T. bagdasarjani on the resistant eggplant cultivar
(Neishabour) was significantly lower than that on the
susceptible one (Isfahan) in both procedures.
Although the intrinsic rate of increase (r) has indeed
been used as a key demographic parameter to describe
the population growth potential under environmental
conditions, a high intrinsic rate of increase does not
necessarily represent an efficient predator (Yu et al.
2013), because a predator population with higher
intrinsic rate may have a lower net predation rate. To
measure the efficiency of a natural enemy, we must
consider not only its intrinsic rate of increase but also
its predation rate. Despite the lower intrinsic rate of
increase of T. bagdasarjani on the resistant eggplant
cultivar, its daily prey consumption was higher than
that on the susceptible one. In addition, the net preda-
tion rate of the predator on the resistant eggplant culti-
var was higher than that on the susceptible one.
July 2015 KHANAMANI ET AL.: Typhlodromus bagdasarjani AND RESISTANT EGGPLANT 509

Fig. 5. Age-specific survivorship (lx), age-specific predation rates (kx), and age-specific net predation rates (qx) of
T. bagdasarjani on two-spotted spider mite reared on the susceptible (Isfahan) and resistant (Neishabour) eggplant cultivars.

Table 3. Predation rates of T. bagdasarjani on two-spotted spider mite reared on the susceptible (Isfahan) and resistant (Neishabour)
eggplant cultivars

Parameters Predation rate (preys/predator)

Susceptible (Isfahan) Resistant (Neishabour)

Net predation rate (C0) 193.05 6 15.16a 221.44 6 20.75a

Transformation rate (Qp) 25.56 6 5.87a 27.92 6 5.53a
Stable predation rate (w) 5.454 6 0.181b 6.227 6 0.260a
Finite predation rate (x) 6.361 6 0.262b 7.005 6 0.321a
Total cohort predation (NC0) 8107.89 10850.51
The means followed by the same letter in each row are not significantly different (t-test, P < 0.05).
510 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 108, no. 4

Fig. 6. Regression curves of consumption rate of T. bagdasarjani throughout its life span on the susceptible (Isfahan) and
resistant (Neishabour) eggplant cultivars.
July 2015 KHANAMANI ET AL.: Typhlodromus bagdasarjani AND RESISTANT EGGPLANT
There are some possible reasons for higher prey
consumption rate on the resistant cultivar than suscep-
tible one as 1) smaller size of prey (two-spotted spider
mite) on the resistant cultivar than susceptible one;
therefore, the predator needs to consume more preys
for its development (Cogni et al. 2002); 2) increasing
movement of two-spotted spider mite nymphs on the
resistant cultivar, thereby increasing exposure to the
predator (Kaitaniemi 2004, Kaplan and Thaler 2010).
The morphological characteristics (such as trichomes)
of the resistant cultivar are possible factors, which could
have prevented the spider mites from feeding on the
leaf surface and hence had promoted their movement.
The transformation rate from prey population to
predator offspring (Qp) provides a demographic estima-
tion of the relationship between the reproduction rate
and the predation rate of a predator. The transforma-
tion rate on the resistant eggplant cultivar was higher
than that on the susceptible one. The higher transfor-
mation rate from prey population to predator offspring
on the resistant eggplant cultivar could be due to the
smaller size of the prey (two-spotted spider mite) on
the resistant cultivar compared with the susceptible
one, or deficiency and lack of some essential nutrients
for egg production in the consumed preys. In addition,
the positive correlation between total prey consumption
of adult females of T. bagdasarjani and their fecundity
on both the susceptible and resistant eggplant cultivars
implies that females are more reproductive with more
feeding. However, the lower correlation coefficient (r)
on the resistant cultivar indicated that the females
which rear on this cultivar to have the equal fecundity
compared with those reared on the susceptible one,
should feed more.
Without the knowledge of both life table and preda-
tion rate of a biological control agent, it is impossible to
correctly describe its performance. To precisely evaluate
the effect of predation in a biological control program,
we need not only to assess the growth potential of a
predator but also evaluate its predation potential. The
finite predation rate (x) takes the finite rate, age-stage
structure, and the age-stage predation rate of a predator
population into consideration, and then can be used as
a standard parameter to describe and compare the pre-
dation potential of natural enemies used in biological
control programs (Chi et al. 2011). In the current study,
the results indicated that the finite predation rate on
the resistant eggplant cultivars (7.005 preys per predator
per day) was higher than that on the susceptible one
(6.361 preys per predator per day). In other words, the
predation capacity of a stable population (with equal
density) of T. bagdasarjani on the resistant eggplant cul-
tivar was higher than that on the susceptible one.
Although the growth rate was lower on the resistant cul-
tivar, due to more consumption rate, the predator had a
higher finite predation rate on this cultivar.
The age-stage, two-sex life table describes the preda-
tion rate precisely because male individuals of
T. bagdasarjani contribute significantly to the predation
on two-spotted spider mite. However, the traditional
female age-specific life table ignores the male individu-
als and their contribution to predation and do not
511
enable the proper description of stage differentiation.
An accurate description of the survival, development,
and predation capacity of a predator can be achieved
with the age-stage, two-sex life table (Yu et al. 2013).
In conclusion, understanding the role of host plant
chemistry in multitrophic interactions is a key to our
ability to assess the strength of top-down forces on her-
bivore populations. Our results revealed that the sus-
ceptible and resistant eggplant cultivars can affect
performance of T. bagdasarjani. Due to higher finite
predation rate of T. bagdasarjani on the resistant egg-
plant cultivar, the performance of the predator on this
cultivar is more than the susceptible one. In addition,
the resistant eggplant cultivar alone can reduce popula-
tion density of two-spotted spider mite versus suscepti-
ble one (Khanamani et al. 2013); thus integration of the
resistant eggplant cultivar and predatory mite would be
more efficient.
Acknowledgments
The financial and technical support of this research by the
Department of Entomology, Tarbiat Modares University, is
greatly appreciated. We are also grateful to Prof. Hsin Chi for
his assistance in data analysis.
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Received 7 December 2014; accepted 30 March 2015.