Exp Appl Acarol
https://doi.org/10.1007/s10493-018-0226-2
Sublethal effects of spirodiclofen, abamectin
and pyridaben on life‑history traits and life‑table
parameters of two‑spotted spider mite, Tetranychus
urticae (Acari: Tetranychidae)
Moosa Saber1
· Zeinab Ahmadi2 · Gholamreza Mahdavinia3
Received: 16 October 2017 / Accepted: 14 February 2018
© Springer International Publishing AG, part of Springer Nature 2018
Abstract Two-spotted spider mite, Tetranychus urticae Koch, is one of the economically
most important pests on a wide range of crops in greenhouses and orchards worldwide.
Control of T. urticae has been largely based on the use of acaricides. Sublethal effects of
spirodiclofen, pyridaben and abamectin were studied on life-table parameters of T. urticae
females treated with the acaricides. LC25 values of spirodiclofen, abamectin and pyridaben
(3.84, 0.04 and 136.96 µg a.i./ml, respectively) were used for sublethal studies. All acaricides showed significant effects on T. urticae biological parameters including developmental time, survival rate, and fecundity. The females treated with spirodiclofen, abamectin
and pyridaben at LC25 exhibited significantly reduced net reproductive rate (R0), finite rate
of increase (λ) and intrinsic rate of increase (r). The intrinsic rate of increase in spirodiclofen, abamectin and pyridaben treated groups and control were 0.0138, 0.0273, 0.039
and 0.2481 female offspring per female per day, respectively. The results indicated that
sublethal concentrations of tested pesticides strongly affected the life characteristics of spider mite and consequently may influence mite population growth in future generations.
Keywords Tetranychus urticae · Sublethal effects · Life-table parameters ·
Spirodiclofen · Abamectin · Pyridaben
Introduction
Two-spotted spider mite (TSM), is one of the most important pest on many plant species in worldwide. Using of acaricides has been the main approach to controlling TSM,
although biological control has proven successful in some protected crops. Continuous
* Moosa Saber
saber@tabrizu.ac.ir; moosaber@gmail.com
1
Department of Plant Protection, Faculty of Agriculture, University of Tabriz, Tabriz, Iran
2
Department of Plant Protection, Faculty of Agriculture, University of Maragheh, Maragheh, Iran
3
Department of Chemistry, Faculty of Basic Science, University of Maragheh, Maragheh, Iran
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Exp Appl Acarol
use of pesticides may lead to high-level resistance in pests populations and destroy populations of natural enemies of the pest (Ruberson et al. 1998; Ambikadevi and Samarjit
1997; Isman 2000; Shi et al. 2005). Considerable research works have been devoted to
finding other strategies for suppression of T. urticae population. In recent decades, with
the increasing knowledge on detrimental effects of chemical pesticides on human, environment, and non-target organisms, the use of lower amounts of toxic compounds have
received relatively great attention. There are several studies indicating sublethal effect
of pesticides on life-history traits and life-table parameters of tetranychid mites (Marcic
2007; Marcic et al. 2010, Landeros et al. 2002; Li et al. 2017).
Searching for new acaricides with novel mode of actions is necessary due to rapid
development of pest resistance to several chemical compounds with different modes of
action. Nervous system of mites has long been the target for most chemicals used for
their control, but at the recent years many compounds acting on respiration and growth
and development of the pest have been introduced (Dekeyser 2005; Marcic 2012; Van
Leeuwen et al. 2015).
Spirodiclofen, a tetronic acid derivative, has recently been introduced as a compound
that inhibits lipid biosynthesis. It was commercialized as an acaricide highly effective
against all relevant phytophagous mite species. This compound effectively controls the
population of mites resistant to other acaricides (Nauen et al. 2000; Elbert et al. 2002;
Dekeyser 2005; Marcic 2007). Pyridaben belongs to the pyridazinone class of acaricides.
Its mode of action is inhibition of mitochondrial electron transport at complex I (METI).
Pyridaben provides long-lasting and good efficacy against all developmental stages of the
spider mites (Stumpf and Nauen 2001; Marcic 2012). Abamectin is a mixture of avermectins containing more than 80% avermectin B1a and less than 20% avermectin B1b.
The avermectins are insecticidal, acaricidal and anti-helminthin compounds derived from
various laboratory broths fermented by the soil bacterium Streptomyces avermitilis (Hayes
and Laws 1991). Abamectin is a natural fermentation product of this bacterium. This compound, acting as a modulator of glutamate-gated chloride channels in the nervous system,
causes mites paralyze.
There are two major types of toxicological studies, the acute toxicological study looking at mortality occurred in short time and the chronic exposure study that monitoring
the effects of repeated exposures to pesticides over longer time periods (Stark and Banks
2003; Martinez-Villar et al. 2005). Toxicity of pesticides are often evaluated at the laboratory by testing on pests by estimating values that measure median lethal dose (LD50) or
median lethal concentration (LC50) (Robertson and Worner 1990; Stark et al. 1997; Kim
et al. 2004) because these assessment are fast, easy and inexpensive. One approach attaining popularity in ecotoxicology is the use of demographic parameters as endpoints of toxicological bioassays (Daniels and Allan 1981; Stark and Banken 1999). Acaricides may
affect life-history traits (longevity, fecundity, fertility, developmental time, sex ratio etc.)
and population growth rates of mites that survived exposure to pesticides (Stark and Rangus 1994; Stark and Banks 2003; Teodoro et al. 2005). The acute toxicity tests has mostly
been utilized for toxicity studies while sublethal effects include any negative effect other
than mortality, such as reduced feeding; lower fecundity or egg viability; reduced longevity
or increased developmental time; and altered sex ratios (Beers and Schmidt 2014; Biondi
et al. 2013) and are important for understanding the total effects of pesticides (Parsaeyan
et al. 2017; Delpuech et al. 1998). Bioassays that address all potential effects of pesticides
provide needed information to use in IPM programs (Beers and Schmidt 2014). It is suggested that life-table analysis is the best method to evaluate the lethal and sublethal effects
of an acaricide (Kim et al. 2006; Li et al. 2017).
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Exp Appl Acarol
The aim of this study was to evaluate the sublethal effects of low lethal concentration
(LC25) of three commonly used acaricides against two-spotted spider mite and consequently to determine the potential of these pesticides to include in management of T. urticae populations at low lethal rates (applied at rates under recommended dose). The objectives were to expose T. urticae females to low lethal concentrations and estimate life-table
parameters. The results of this study could be seen as a starting point for further greenhouse and/or field research in order to improve the management of spider mites.
Materials and methods
Mite rearing
Tetranychus urticae was collected from infected leaves of bean, Phaseolus vulgaris L., at
the agricultural research greenhouse of the University of Maragheh, Iran. The mites have
not been exposed to any chemical pesticides prior to the experiments during the preceding
2 years. Tetranychus urticae were reared on P. vulgaris in a growth chamber at 25 ± 1 °C,
60 ± 10% RH, and L16:D8 h photoperiod for at least three generations before using them
for experiments. Bioassays were performed under the same conditions.
Acaricides
The acaricides used in the study were: Spirodiclofen (Envidor® 24 SC, Bayer CropScience,
Germany), abamectin (Vermectin® 1.8 EC, Golsam, Iran) and pyridaben (Sunmite® 20%
w/w, Iprochem, China). These acaricides were chosen because they are recommended for
controlling the TSM in Iran and many other countries and belong to different classes of
chemicals with different modes of action on T. urticae.
Toxicity bioassays
Pre-ovipositing females (< 1 day old) were used in bioassay tests. Leaf discs (2 cm diameter) were dipped in each of specified concentrations of either acaricide for 30 s and allowed
to air dry for 1 h at laboratory conditions. Then 15 young adult females of TSM were introduced on each leaf disc. Leaf discs were placed on moist cotton in a plastic Petri dish (6 cm
diameter) with a ventilation hole (1 cm diameter) in the center of the lid covered by net.
After 24 h exposure, the number of dead and survived females was recorded. Each bioassay consisted of five concentrations. The bioassays were replicated five times. Control leaf
discs were dipped in distilled water only. The concentrations used for the bioassay were
selected based on preliminary tests (dose setting). The concentration range were 2.4, 3.63,
5.49, 8.32, 12.59 and 19.2 µg a.i./ml for spirodiclofen, 0.02, 0.03, 0.04, 0.07, 0.11, 0.17 and
0.27 µg a.i./ml for abamectin, and 100, 144.88, 209.4, 304.6, 437.4 and 600 µg a.i./ml for
pyridaben. Data were subjected to probit analysis (Finney 1971). Concentration–mortality
curves were estimated by probit analysis (SAS Institute 2002).
Life‑table bioassays
Sublethal effects of the acaricides were evaluated on life-table parameters of offspring from T.
urticae females treated with the acaricides. The experimental procedures and acaricides were
13
Exp Appl Acarol
the same as those used for concentration–mortality bioassays described above. According to
the methods of Li et al. (2017), Mohammadi et al. (2016) and Yin et al. (2013), 100 pairs of
unmated female and male individuals of T. urticae (< 1 day old) were placed on each leaf
arena treated by LC25 concentration of spirodiclofen, abamectin or pyridaben acaricides that
were 3.84, 0.04 and 136.96 µg a.i./ml, respectively. After 24 h exposure, the surviving pairs
of mites from each treatment (control and acaricide treatments) were transferred to new clean
leaf discs free of acaricide residue for oviposition. Eggs laid were counted daily and collected
per female for each replication and treatment. The number of hatched eggs was recorded.
Females and males were monitored for survival daily, until all mites died naturally. Daily
monitoring of the number of eggs laid per female for each replication and treatment and the
number of offspring individuals, developmental time of subsequent stages reaching the adult
stage provided the basic elements for both the construction of life tables and the calculation of
life-table parameters. Leaf discs treated with distilled water only served as the control.
Data analysis
Data were analyzed by the age-stage, two-sex life-table theory (Chi 2015). TWOSEX-MS
Chart software was used to analyze the data (Chi 2015). Age-stage survival rate (sxj, where x
indicates age and j stage), age-stage specific fecundity (fxj), age-specific survival rate (lxj), agespecific fecundity (mx), age-stage life expectancy (exj), age-stage specific reproductive value
(vxj), adult pre-ovipostional period (APOP, the time from emergence of the adult female to
its initial oviposition), total pre-ovipostional period (TPOP, the time from female birth to the
initial oviposition), and the population parameters (rm, intrinsic rate of increase; λ, finite rate
of increase; R0, net reproductive rate; GRR, gross reproductive rate; T, mean generation time)
were estimated accordingly. Means, standard errors of developmental time, longevity and variances of the life-table parameters were calculated with the bootstrap (m = 100,000) method
(Efron and Tibshirani 1993; Huang and Chi 2012). Differences among treatments were compared using the paired bootstrap test (Chi 2015).
The intrinsic rate of increase (rm) was estimated using the iterative bisection method from
the Euler–Lotka equation:
∞
∑
e−r(x+1) lx mx = 1,
(1)
x=0
with the age indexed from zero (Goodman 1982). Gross reproductive rate was calculated
as:
GRR = 𝛴mx .
(2)
Net reproductive rate represents the mean number of offspring that an individual can produce during its lifetime and was calculated as:
R0 =
∞
∑
lx mx
(3)
x=0
Mean generation time defined as the period that a population needs to increase to R0-fold
of its size was calculated as:
T=
13
lnR0
.
r
(4)
Exp Appl Acarol
The finite rate of increase was calculated as
𝜆 = er .
(5)
is
the
probability
that
a
newborn
nymph
will
survive
to
age
x
and
is
The value of lxj
calculated by pooling all of the surviving individuals of different stages. It is calculated as:
lxj =
∞
∑
sxj ,
(6)
j=1
where ∞ is the last stage of the study cohort. mx was calculated using the following
equation:
∑∞
s f
j=1 xj xj
mxj = ∑∞
s
j=1 xj
.
(7)
The age-stage life expectancy (exj) was calculated according to Chi and Su (2006) and
defined as the time that an individual of age x and stage j is expected to live. The life
expectancy for individuals in different age-stage-sex units can be calculated as:
exy =
n m
∑
∑
s� ij.
(8)
i=x j=y
The age-stage-specific reproductive value (vxj) of T. urticae female was calculated for an
individual of age x and stage j to the future population:
[m
]
n
∑
er(i+1) ∑ −r(k+1)
s� (k, y, 1)f (k, y, 1) .
×
e
v(i,j,1) =
(9)
s(i, j, 1) k=i
y=1
Results
Toxicity bioassay tests results of spirodiclofen, abamectin and pyridaben are shown in
Table 1. Based on LC50 values and fiducial limits it was concluded that abamectin was the
most toxic acaricide against T. urticae followed by spirodiclofen and pyridaben. Pyridaben
had the lowest toxicity against the pest compared to the others.
Sublethal effect study showed that the mean total pre-adult developmental times of
females of F1 generations and male were significantly affected when exposed to LC25
values of spirodiclofen, abamectin and pyridaben compared to control female and male,
Table 1 Mean lethal concentration (µg a.i./ml) of spirodiclofen, abamectin and pyridaben for 25, 50 and
90% of pre-ovipositing females of Tetranychus urticae (95% fiducial limits in parentheses)
Treatment
Slope ± SE χ2 (df 5) LC25
LC50
LC90
Spirodiclofen 1.80 ± 0.28 40.67
3.84 (2.61–4.90)
9.07 (7.38–11.60)
46.46 (29.19–108.16)
Abamectin
Pyridaben
0.04 (0.03–0.05)
136.96 (96.63–
170.40)
0.092 (0.076–0.11)
283.57 (237.71–
342.49)
0.38 (0.28–0.63)
1130 (783.83–2164)
2.05 ± 0.23 73.76
2.13 ± 0.32 43.05
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Exp Appl Acarol
respectively (Table 2). Adult longevity of female and male adults exposed to LC25 values
of spirodiclofen, abamectin and pyridaben were shorter in comparison with control. The
total longevity of female and male treated with abamectin, spirodiclophen and pyridaben
also was reduced significantly (Table 2). The finding of this study revealed that the sublethal concentration of spirodiclofen, abamectin and pyridaben may influence the durability
of pre-adult stages, longevity and biological parameters of T. urticae.
Results showed that exposure of females to spirodiclofen, abamectin and pyridaben
reduced the net reproductive rate (R0) and intrinsic rate of increase (r) compared to control. Similarly, the finite rate of increase (λ) and gross reproduction rate (GRR) for the
control were significantly higher than those of for spirodiclofen, abamectinand pyridaben.
Also mean generation time (T) of control was significantly shorter than of abamectin and
pyridaben treatments (Table 3).
The age-stage-specific survival rate (sxj) of T. urticae represents the probability that
a newly born individual will survive to each age-stage unit age x and stage j. The agestage, two-sex life table is able to describe the stage differentiation, the beginning and
finish of subsequent stages can be observed in the survival curve for each stage. There
were no significant differences in the survival rate at the egg stage of treated T. urticae
with LC25 of acaricides (Fig. 1). The highest sxj for the curve of nymph stage was 1.00,
0.90, 0.90 and 0.92 for control¸ abamectin, spirodiclofen and pyridaben, respectively.
The curves in Fig. 1 show that nymphal period sxj of control (7 days) is significantly
shorter than the treatments and the longest nymphal period observed in abamectin and
spirodiclofen (11 days). Female adult stage began at age 7, 8 and 8 days for abamectin, spirodiclofen and pyridaben, respectively, and continued until days 18, 16 and 16,
respectively, while for the control the first female adult stage began at age 6 days and
the last female died at age 22 days. The survivorship rate of different stages of the pest
Table 2 Life-history traits [mean ± SE developmental time (days)] of offspring of Tetranychus urticae
females treated with spirodiclofen, abamectin or pyridaben
Sex
Female
Male
Stage
Egg
Nymph
Adult
Total pre-adult
APOP
TPOP
Longevity
Fecundity
Egg
Nymph
Adult
Total pre-adult
Longevity
Control
Spirodiclofen
Abamectin
Pyridaben
2.87 ± 0.17b
4.58 ± 0.13a
4.52 ± 0.24a
4.68 ± 0.14a
4.67 ± 0.19b
10.53 ± 0.52a
7.53 ± 0.26c
0.2 ± 0.05b
7.7 ± 0.135b
17.65 ± 0.29a
21.47 ± 0.85a
2.78 ± 0.28c
4.44 ± 0.18ba
12.56 ± 0.84a
7.22 ± 0.36c
19.78 ± 0.91a
5.75 ± 0.11a
4.25 ± 0.24c
10.33 ± 0.2a
0.23 ± 0.08b
10.57 ± 0.18a
14.58 ± 0.26b
2.46 ± 0.24b
4.83 ± 0.11a
5.58 ± 0.29a
5.33 ± 0.4b
10.42 ± 0.29a
15.75 ± 0.51b
5.0 ± 0.31ab
4.1 ± 0.28c
9.52 ± 0.42b
0.63 ± 0.1a
10.15 ± 0.31a
13.62 ± 0.56c
3.33 ± 0.29b
3.6 ± 0.21b
4.47 ± 0.17ba
5.93 ± 0.56b
8.07 ± 0.21b
14 ± 0.59c
5.2 ± 0.58ab
4.72 ± 0.27bc
9.88 ± 0.19a
0.68 ± 0.09a
10.4 ± 0.18a
14.6 ± 0.22b
3.2 ± 0.33b
4.07 ± 0.25b
4.86 ± 0.33a
6.36 ± 0.6b
8.93 ± 0.54b
15.29 ± 0.5b
APOP Adult pre-oviposition period and TPOP total pre-oviposition period
Treatments were estimated with the bootstrap technique using 100,000 replications; SEs were estimated
using 100,000 bootstraps and compared by paired bootstrap test (comparison of 95% CL). Means within a
row followed by different letters are significantly different between treatments by using the paired bootstrap
test (P < 0.05)
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Exp Appl Acarol
Table 3 Mean (±SE) life-table parameters of offspring of Tetranychus urticae females treated with spirodiclofen, abamectin or pyridaben
Treatment
rm
λ
R0
T
GRR
12.9 ± 1.1a
10.29 ± 0.09b
13.39 ± 1.1a
Control
0.2481 ± 0.01a
1.28 ± 0.01a
Spirodiclofen
Abamectin
Pyridaben
0.0138 ± 0.01b
0.0273 ± 0.01b
0.0390 ± 0.01b
1.01 ± 0.01b
1.02 ± 0.01b
1.04 ± 0.01b
1.2 ± 0.16c
1.4 ± 0.20bc
1.6 ± 0.23b
11.95 ± 0.63ba
12.28 ± 0.46a
12.03 ± 0.21a
1.55 ± 0.19d
3.84 ± 0.674b
2.1 ± 0.28c
rm Intrinsic rate of increase, λ finite rate of increase, R0 net reproductive rate, T mean generation time and
GRR gross reproduction rate
Means within a column followed by different letters are significantly different between treatments by using
the paired bootstrap test (P < 0.05)
Fig. 1 Age-stage-specific survival rate (Sxj) of offspring of Tetranychus urticae females treated with LC25
of abamectin, spirodiclofen andpyridaben
followed exposure to the acaricides is shown in Fig. 1. Adults and nymphal of T. urticae
emerged sooner and survived for a longer time in control (Fig. 1). Figure 1 shows the
survival curve and differentiated stages, which is an important feature of mites. Overlapping between stages were shown the different growth rate among individuals. By
ignoring individual differences and assuming the same developmental period for them
provide incomplete survival and reproduction curve.
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Exp Appl Acarol
The age-specific survival rate (lx) remained as high as 1.0 until age 5, 6, 5d and
7 days in abamectin, spirodiclofen, pyridaben and control treatments, respectively. The
lowest survival rate of all age stages was observed in T. urticae treated with abamectin.
The highest offspring production for abamectin (0.48) occurred at age 11 days, for spirodiclofen (0.45) at age 13 days, for pyridaben (0.57) at age 11 days and for control at
age 8 days with 2.8 offspring (Fig. 2).
The parameters lx and fecundity (mx) are also plotted in Fig. 2 and 3. The lowest peaks of mx and the lowest fecundity of all age stages were observed in T. urticae treated with spirodiclofen. The maternity (lxmx) of spirodiclofen-treated mites were
lowest of all (Fig. 4). The maximum values of lxmx were 1.0, 1.33 and 1.0 for mites
treated by LC25 concentration of spirodiclofen, abamectin and pyridaben, respectively,
which occurred on day 8.
The age-stage life expectancy (exj) represents the length of time that an individual of
age x and stage j is expected to survive. The age-stage-specific life expectancy (exj) of
T. urticae in different treatments is shown in Fig. 5. Overall, the life expectancy of T.
urticae individuals treated with abamectin was shorter than in all age and stage groups
(Fig. 5).
The vxj value defines the contribution of an individual at age x and stage j to the
future population. The age-reproductive values (vxj) of T. urticae in different pesticides are plotted in Fig. 6. The peak of the reproductive values of females treated with
abamectin was at age 9 days, spirodiclofen at age 8, pyridaben at age 9, and for control
it was at age 8 days (Fig. 6). When females emerged, the vxj increased to a high value
of 1.41, 1.28, 1.56 and 7.83 in abamectin, spirodiclofen, pyridaben and control, respectively. The reproductive values for T. urticae treated with LC25 of pesticides were significantly lower than for the control.
Fig. 2 Age-specific survival rate (lx) of offspring of Tetranychus urticae females treated by LC25 of
abamectin, spirodiclofen and pyridaben compared with control
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Exp Appl Acarol
Fig. 3 Age-specific fecundity (mx) of offspring of Tetranychus urticae females treated with LC25 of
abamectin, spirodiclofen and pyridaben compared with control
Fig. 4 Age specific maternity (lxmx) of offspring of Tetranychus urticae females treated with LC25 of
abamectin, spirodiclofen and pyridaben compared with control
Discussion
Demographic toxicology or life-table analysis is the best method for evaluation and combining lethal and sublethal effects of pesticides (Daniels and Allan 1981; Day and Kaushik
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Exp Appl Acarol
Fig. 5 Age-specific life expectancy (ex) of offspring of Tetranychus urticae females treated with LC25 of
abamectin, spirodiclofen and pyridaben compared with control
Fig. 6 Age-reproductive value (vx) of offspring of Tetranychus urticae females treated with LC25 of
abamectin, spirodiclofen and pyridaben compared with control
1987; Kim et al. 2004). LC25 Concentration of these acaricides influenced the life-table
parameters of two-spotted spider mite. Our study here is the first comprehensive research
on the sublethal effects of spirodiclofen, abamectin and pyridaben on life-table parameters of progeny generation of T. urticae. The results demonstrated that LC25 of acaricides
could reduce the survival rate, oviposition period, fecundity and longevity of the female
of T. urticae. Several studies have been done on the effect of pesticides on T. urticae.
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Exp Appl Acarol
For example, Marcic (2007) reported that sublethal concentration/dose of spirodiclofen
reduced the survival rate and other life-table parameters of T. urticae. Stark et al. (1997)
revealed that reproductive potential of T. urticae can be greatly influenced by their susceptibility to acaricides. This described and compared the effects of LC25 concentrations of
tested pesticides by using the age-stage, two-sex life table the demographic characteristics
of T. urticae.
The present study showed that spirodiclofen, abamectin and pyridaben had sublethal
negative affect on life-table parameters of adult T. urticae. The concentrations (LC25) of
either acaricide applied to females were enough to affect fecundity and longevity. However abamectin and spirodiclofen have had a greater impact on longevity and fecundity (Table 2). Similar effects on life-table parameters were recorded by Marcic (2007)
and Martinez-Villar et al. (2005), who treated T. urticae adult females with several spirodiclofen concentrations. Their results showed that higher concentrations caused greater
reduction in rm. Our results revealed that the population growth rate of T. urticae was
affected by LC25 of tested pesticides as result of negative effects on immature developmental time, reproduction period, fecundity and, finally in the population parameters (i.e., rm,
λ, R0, and T). Our findings are in agreement with many studies on the effects of pesticides
on development, survival, and reproduction of T. urticae (Kim and Seo 2001; Kim and Yoo
2001; Marcic 2003; Ashley et al. 2006; Hardman et al. 2007). Compared with the control,
the reproductive values in mites treated with LC25 were changed, which may cause restriction in reproduction and survivorship. In accordance with Alinejad et al. (2014), the sublethal dose of fenazaquin affected survivorship and fecundity of T. urticae.
Intrinsic rate of increase (rm) is the best factor to describe the effect of pesticides on
pests (Hamedi et al. 2010; Stark and Banks 2003), because it demonstrates the overall
effects on both survivorship and fecundity (Li et al. 2017). The results of this study showed
that rm in T. urticae was reduced by acaricides compared with the control indicating the
adverse effect of the chemicals on this parameter. Li et al. (2017) also reported that the rm
values of progeny generation of the treated mites with bifenazate decreased significantly.
The net reproductive rate (R0) of T. urticae treated with spirodiclofen is significantly lowered compared to that of the others (Table 3). The mean generation time (T) of the T. urticae treated with acaricides was also influenced significantly by the acaricide.
Moreover, Tuan et al. (2016) and Alinejad et al. (2014) illustrated that because of the
variable developmental rates occurring among T. urticae individuals, the survival rate
curve showed significant stage overlap. This agrees with our results. In our experimental
conditions, the mites treated with abamectin were reduced the age-specific survival rate (lx)
values (Fig. 2). Furthermore, lxmx (age-specific maternity) values were reduced by pyridaben and spirodiclofen, in agreement with results of Marcic (2007). His results indicated
that the tested acaricides would significantly reduce mite growth. Lower age-specific reproductive value and life expectancy was observed in treated mites by acaricides. Mohammadi
et al. (2016) reported that life expectancy of Tetranychus turkestani Ugarov and Nikolskii
was affected differently in individuals of the same age, stages and sexes. Similar results
were observed in this research: for example, exj of female adults was about 10–12 days,
whereas the value was between 9 and 12 days for males in different treatments.
Finally, studies of sublethal effects on life-table parameters of pests allow us to have the
most complete delineation of the population-level responses to pesticides. Quantification
of the importance of pesticide impact on life cycle timing at the population level of target
pest species will assist the researchers to manage the pest population properly. The fact
that pesticides in lower doses may have significant effects on population levels and might
affect population dynamics of T. urticae (Stark and Banks 2003). According to our results,
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Exp Appl Acarol
the lower lethal concentration (LC25) of the tested acaricides showed negative effects on
survivorship and life-table parameters of the subsequent generation of T. urticae. Despite
the negative effects of LC25 values of spirodiclofen, abamectin and pyridaben on life-table
parameters of T. urticae at laboratory study, more detailed evaluations are needed on total
effects of these acaricides on the mite and its biological control agents under greenhouse
and field conditions.
References
Alinejad M, Kheradmand K, Fathipour Y (2014) Sublethal effects of fenazaquin on life table parameters of
the predatory mite Amblyseiuss wirskii (Acari: Phytoseiidae). Exp Appl Acarol 64:361–373
Ambikadevi D, Samarjit R (1997) Chemical control of red spider mite, Tetranychus cinnabarinus (Boisduval) on okra. J Trop Agric Sci 35:38–40
Ashley JL, Herbert DA, Lewis EE, Brewster CC, Huckaba R (2006) Toxicity of three acaricides to Tetranychusurticae (Tetranychidae: Acari) and Oriusinsidiosus (Anthocoridae: Hemiptera. J Econ Entomol
99(1):54–59
Beers EH, Schmidt RA (2014) Impacts of orchard pesticides on Galendromusoccidentalis: lethal and sublethal effects. Crop Prot 56:16–24
Biondi A, Zappala L, Stark JD, Desneux N (2013) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS ONE 8(9):1–11
Chi H (2015) Computer program for the age-stage, two-sex life table analysis. National Chung Hsing University, Taichung
Chi H, Su HY (2006) Age-stage, two-sex life tables of Aphidius gifuensis (Ashmead) (Hymenoptera: Braconidae) and its host Myzus persicae (Sulzer) (Homoptera: Aphididae) with mathematical proof of the
relationship between female fecundity and the net reproductive rate. Environ Entomol 35:10–21
Daniels RE, Allan JD (1981) Life table evaluation of chronic exposure to a pesticide. Can J Fish Aquat Sci
38:485–494
Day K, Kaushik NK (1987) An assessment of the chronic toxicity of the synthetic pyrethroid, fenvalerate, to
Daphniagaleatamendotae, using life tables. Environ Pollut 44:12–26
Dekeyser MA (2005) Acaricide mode of action. Pest Manag Sci 61:103–110
Delpuech JM, Gareau E, Terrier O, Fouillet P (1998) Sublethal effects of the insecticide chlorpyrifos on sex
pheromonal communication of Trichogramma brassicae. Chemosphere 36:1775–1785
Efron B, Tibshirani RJ (1993) An introduction to the bootstrap. Chapman and Hall, New York, p 465
Elbert A, Bruck E, Sone S, Toledo A (2002) Worldwide use of the new acaricide Envidor® in perennial
crops. Pflanzenschutz- Nachrichten Bayer 55:287–304
Finney DJ (1971) Probit analysis, 3rd edn. Cambridge University Press, London, p 383
Goodman D (1982) Optimal life histories, optimal notation, and the value of reproductive value. Am Nat
119:803–823
Hamedi N, Fathipour Y, Saber M (2010) Sublethal effects of fenpyroximate on life table parameters of the
predatory mite Phytoseiu splumifer. Biol Control 55:271–278
Hardman JM, Franklin JL, Beaulieu F, Bostanian NJ (2007) Effects of acaricides, pyrethroids and predator
distributions on populations of Tetranychus urticae in apple orchards. Exp Appl Acarol 43:235–253
Hayes WJ, Laws ER (1991) Handbook of pesticide toxicology. In handbook of pesticide toxicology. Academic Press, New York
Huang YB, Chi H (2012) Assessing the application of the Jackknife and Bootstrap techniques to the estimation of the variability of the net reproductive rate and gross reproductive rate: a case study in Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae). J Agric For 61:37–45
Isman MB (2000) Plant essential oils for pest and disease management. Crop Prot 19:603–608
Kim SS, Seo SG (2001) Relative toxicity of some acaricides to the predatory mite, Amblyseiu swomersleyi
and the twospotted spider mite, Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae). Appl Entomol Zool 36(4):509–514
Kim SS, Yoo SS (2001) Comparative toxicity of some acaricides to the predatory mite, Phytoseiulus persimilis and the twospotted spider mite, Tetranychus urticae. Biol Control 47:563–573
Kim M, Shin D, Suh E, Cho K (2004) An assessment of the chronic toxicity of fenpyroximate and pyridaben toTetranychus urticae using a demographic bioassay. Appl Entomol Zool 39(3):401–409
Kim M, Sim C, Shin D, Suh E, Cho K (2006) Residual and sublethal effects of fenpyroximate and pyridaben
on the instantaneous rate of increase of Tetranychus urticae. Crop Prot 25(6):542–548
13
Exp Appl Acarol
Landeros J, Mora N, Badii M, Cerda PA, Flores AE (2002) Effect of sublethal concentrations of avermectin
on population parameters of Tetranychus urticaeon strawberry. Southwest Entomol 27:283–289
Li YY, Fan X, Zhang GH, Liu YQ, Chen HQ, Liu H, Wang JJ (2017) Sublethal effects of bifenazate on life
history and population parameters of Tetranychus urticae (Acari: Tetranychidae). Syst Appl Acarol
22:148–158
Marcic D (2003) The effects of clofentezin on life-table parameters in two-spotted spider mite Tetranychus
urticae. Exp Appl Acarol 30:249–263
Marcic D (2007) Sublethal effects of spirodiclofen on life history and life-table parameters of two-spotted
spider mite (Tetreanychus urticae). Exp Appl Acarol 42:211–229
Marcic D (2012) Acaricides in modern management of plant feeding mites. J Pest Sci 85:395–408
Marcic D, Ogurlic I, Mutavdzic S, Peric P (2010) The effects of spiromesifen on life history traits and population growth of two-spotted spider mite (Acari: Tetranychidae). Exp Appl Acarol 50:255–267
Martinez-Villar E, Francisco Saenz-De-Caezon FJ, Moreno-Grijalba F, Vicente M, Perez-Moreno I (2005)
Effects of azadirachtin on the two-spotted mite, Tetranychus urticae (Acari: Tetranychidae). Exp Appl
Acarol 35:215–222
Mohammadi S, Ziaee M, Seraj A (2016) Sublethal effects of Biomite® on the population growth and life
table parameters of Tetranychus turkestani Ugarov and Nikolskii on three cucumber cultivars. Syst
Appl Acarol 21(2):218–226
Nauen R, Stumpf N, Elbert A (2000) Efficacy of BAJ 2740. A new acaricidal tetronic acid derivative,
against Tetranychid spider mite species resistant to conventional acaricides. In: Proceedings of the
Brighton crop protection conference—pest and diseases, pp 453–458
Parsaeyan E, Safavi SA, Saber M, Poorjavad N (2017) Effects of emamectin benzoate and cypermethrin on
the demography of Trichogramma brassicae Bezdenko. Crop Prot 3:1–6
Robertson JL, Worner SP (1990) Population toxicology: Suggestions for laboratory bioassays to predict pesticide efficacy. J Econ Entomol 83:8–12
Ruberson JR, Nemato H, Hirose Y (1998) Pesticides and conservation of natural enemies in pest management. In: Barbosa P (ed) Conservation biological control. Academic Press, New York, p 396
SAS Institute (2002) SAS/STAT User’s Guide: Statistics, version 6.12. SAS Institute, Cary, NC, USA
Shi WB, Jiang Y, Feng MG (2005) Compatibility of ten acaricides with Beauveria bassianaand enhancement of fungal infection to Tetranychus cinnabarinus (Acari: Tetranychidae) eggs by sublethal application rates of pyridaben. Appl Entomol Zool 40(4):659–666
Stark JD, Banken JA (1999) Importance of population structure at the time of toxicant exposure. Ecotoxicol
Environ Saf 42(3):282–287
Stark JD, Banks JE (2003) Population-level effects of pesticides and other toxicants on arthropods. Annu
Rev Entomol 48:505–519
Stark JD, Rangus T (1994) Lethal and sublethal effects of the neem insecticide, Margosan-O, on pea aphid.
J Pest Sci 41:155–160
Stark JD, Tanigoshi L, Bounfour M, Antonelli A (1997) Reproductive potential: its influence on the susceptibility of a species to pesticides. Ecotoxicol Environ Saf 37:273–279
Stumpf N, Nauen R (2001) Cross-resistance, inheritance, and biochemistry of mitochondrial electron
transport inhibitor-acaricide resistance in Tetranychusurticae (Acari: Tetranychidae). J Econ Entomol
94:1577–1583
Teodoro AV, Fadini MAM, Lemos WP, Guedes RNC, Pallini A (2005) Lethal and sub-lethal selectivity
of fenbutatin oxide and sulfur to the predator Iphiseiodes zuluagai (Acari: Phytoseiidae) and its prey,
Oligonychus ilicis (Acari: Tetranychidae), in Brazilian coffee plantations. Exp Appl Acarol 36:61–70
Tuan SJ, Lin YH, Yang CM, Atlihan R, Saska P, Chi H (2016) Survival and reproductive strategies in twospotted spider mites: demographic analysis of arrhenotokous parthenogenesis of Tetranychus urticae
(Acari: Tetranychidae). J Econ Entomol 109(2):502–509
Van Leeuwen T, Tirry L, Yamamoto A, Nauen R, Dermauw W (2015) The economic importance of acaricides in the control of phytophagous mites and an update on recent acaricide mode of action research.
Pest Biochem Physiol 121:12–21
Yin WD et al (2013) Age-stage two-sex life tables of Panonychus ulmi (Acari: Tetranychidae), on different
apple varieties. J Econ Entomol 106(5):2118–2125
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