Previous Article in Journal
Survival and Growth of Asellus aquaticus on Different Food Sources from Drinking Water Distribution Systems
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Lethal and Sub-Lethal Effects of Spirotetramat on Red Spider Mite, Tetranychus macfarlanei Baker and Pritchard (Acari: Tetranychidae)

by
Farhana Afrose Swarna
1,
Tasfia Hayder
1,
Shreema Mandal Barsa
1,
Powlomee Mondal
1,
Tetsuo Gotoh
2 and
Mohammad Shaef Ullah
1,*
1
Laboratory of Applied Entomology and Acarology, Department of Entomology, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh
2
Faculty of Economics, Ryutsu Keizai University, Ryugasaki, Ibaraki 301-8555, Japan
*
Author to whom correspondence should be addressed.
Arthropoda 2024, 2(3), 212-225; https://doi.org/10.3390/arthropoda2030016
Submission received: 20 June 2024 / Revised: 5 September 2024 / Accepted: 10 September 2024 / Published: 12 September 2024

Abstract

:
The red spider mite, Tetranychus macfarlanei, is a serious pest of many cultivated crops in Bangladesh and other East-Asian and South-East Asian countries, in the Afrotropical, Oriental, and Palearctic regions. Sublethal concentration of pesticides, such as LC15 and LC30 (the concentrations that result in 15 and 30 percent lethality, respectively) impact reproduction, behavior, development, and physiology. This study assessed the effects of different concentrations of spirotetramat, an insecticide that disrupts lipid production, on the biological traits of T. macfarlanei. The LC15, LC30, LC50, and LC90 values were 2.16, 6.57, 20.54, and 332.81 mg·L−1, respectively. Sublethal concentrations (LC15 and LC30) slightly reduced female fecundity but did not significantly affect development duration, pre-oviposition, oviposition period, or longevity compared to the untreated control group. Life table parameters differed between the treated and control groups, with significant reductions in the intrinsic rate of increase (r), the net reproductive rate (R0), and the finite rate of increase (λ) for LC15 and LC30. LC15 and LC30 had negative effects on the intrinsic rate of increase for females. This study demonstrated that lower lethal concentrations of spirotetramat compromised survivability and negatively impacted the life-table parameters of subsequent generations of T. macfarlanei. These findings highlight the importance of sublethal effects in pest control, offering valuable insights for developing more effective and sustainable integrated pest management strategies.

Graphical Abstract

1. Introduction

The red spider mite, Tetranychus macfarlanei Baker and Pritchard (Acari: Tetranychidae), is a common agricultural pest that leads to significant yield losses in many important field and greenhouse crops, affecting a variety of plants from different families, including Malvaceae, Fabaceae, Cucurbitaceae, Convolvulaceae, and Solanaceae [1,2,3,4,5]. Tetranychus macfarlanei is prevalent in some East-Asian and South-East Asian countries, the Afrotropical, Oriental, and Palearctic regions [5,6]. It uses a haplodiploid sex-determination system, where males are haploid and develop from unfertilized eggs, while females are diploid and develop from fertilized eggs. Its lifecycle includes several stages: egg, larva, protonymph, deutonymph, and adult. The time from egg to adult varies with environmental conditions, usually taking one to two weeks [4]. Understanding the biology and development of T. macfarlanei is crucial for effective pest management, especially when using acaricides such as spirotetramat.
Chemical pesticides are often used to control spider mites, but their widespread application has led to increased pesticide resistance [7]. Concentrations below the median lethal concentration (LC50) are generally considered sublethal. Sublethal concentrations do not cause immediate death but induce changes in the biology, physiology, demography, or behavior of individuals or populations that survive exposure [8]. Sublethal effects can include reduced lifespan, slower development, decreased population growth, lower fertility and fecundity, altered sex ratios, deformities, and changes in behavior, such as feeding, searching, and egg-laying [9,10]. Therefore, it is important to consider the subtle effects of toxicants when evaluating their overall impact.
New insecticides are designed to be safer for the environment and people, while effectively controlling insect and mite pests [11]. One such insecticide is spirotetramat, used worldwide to target aphids, mites, and other pests on crops [12,13]. It moves through plants in both directions after application [12] and works by stopping lipid production, which affects the pests’ reproduction [14,15]. Lipids are important for insects’ growth and movement [16]. Spirotetramat is also effective against pests that have developed resistance to other insecticides, making it a valuable tool for managing pest resistance [17,18]. This has led to new pest control methods and products. An insect growth regulator (IGR), spirotetramat impedes the development of immature stages, diminishes their reproductive capacity, and ultimately exerts insecticidal effects [14,19].
Spirotetramat can be toxic to dogs and rats, which may be relevant for humans. In studies, it affected the thyroid and thymus glands in dogs at concentrations as low as 19 mg/kg body weight per day [20]. When studying the impact of toxic substances on insects, it is important to look beyond just immediate death. Traditional tests often focus only on how many insects die from a single concentration, which does not fully reveal how pesticides affect entire insect populations [21]. Over time, insecticides can break down into lower concentrations that do not kill insects immediately but can still cause other problems, such as changes in physiology, behavior, or health [8,22,23,24,25].
Spirotetramat has been shown to have several sublethal effects on arthropods. These include (1) prolonged development and reduced survival, adult longevity, and reproduction in cabbage aphids [Brevicoryne brassicae (Linnaeus, 1758)] and Frankliniella occidentalis Pergande, 1895 [26,27], (2) decreased survival rate and fecundity in Aphis gossypii Glover, 1877 [28], and (3) reduced gross fecundity and net fecundity in Tetranychus urticae Koch [29].
Bioassays encompassing all potential pesticide effects offer crucial insights for integrated pest management (IPM) programs [30]. Life-table analyses are considered the optimal method for assessing both lethal and sublethal impacts of acaricides [31,32,33]. In insects and mites, they also help to understand population ecology and improve pest management strategies [34], calculate birth rates, survival rates, reproduction, and overall population growth potential [35] and estimate age-specific and stage-specific survival rates [36,37,38]. Thus, we used a life-table analysis to assess the lethal and sublethal effects of spirotetramat on the spider mite T. macfarlanei. Here, we examined the sublethal effects of spirotetramat on its population characteristics, including the progeny and the females in the pre-ovipositional stage. Our findings should help determine the appropriate conditions for using spirotetramat effectively as an acaricide for controlling T. macfarlanei in the field.

2. Materials and Methods

2.1. Collection and Rearing of Spider Mites

Specimens of T. macfarlanei were collected from a bean plant at Bangladesh Agricultural University field laboratory, Mymensingh, Bangladesh (24°71′91.06″ N, 90°43′0608″ E) on August 2022. Infested leaves were gathered in large numbers and placed in small plastic bags, which were sealed with rubber bands. To maintain the appropriate temperature and prevent damage to the specimens during transport, the plastic bags containing the samples were stored in a thermocol box [39]. Voucher specimens were deposited in the laboratory of Applied Entomology and Acarology at Bangladesh Agricultural University. The spider mite culture was reared on leaf discs (16 cm2) of bean, Lablab purpureus L. The leaves were positioned on water-saturated polyurethane mats within Petri dishes, maintained at 25.0 ± 1 °C, 60–80% RH, with a 16 h light and 8 h dark photoperiod, in an acclimation chamber (Biobase BJPX-A400/II, Biobase Biozone Co., Ltd., Shandong, China). Leaves were replaced approximately every 7 days or earlier if they dried out or showed mite damage [40]. The discrepancy in leaf sizes used for mass rearing and toxicity analysis was intentional and served different purposes in our research. For mass rearing, we used leaf discs with an area of 16 cm2 to provide a larger and more stable feeding surface for the mites, which supports their growth and reproduction over extended periods. In contrast, for toxicity analysis, we used smaller leaf discs with an area of 20 mm in diameter (about 3 cm2). The smaller size ensures that the pesticide application is more controlled, and the exposure conditions are more uniform, which is crucial for accurately assessing the effects of the pesticide on the mites. Using different leaf sizes allowed us to optimize the conditions for both rearing and testing, ensuring both accurate results and effective mite cultivation.

2.2. Toxicity to Adult Females

The effects of spirotetramat on the immature development of males and females were measured on bean leaves at 25 °C. Because female spider mites lay eggs, they have a more significant impact on population growth compared to males. To assess the toxicity of spirotetramat (Movento 150 OD®, Bayer CropScience Limited, Dhaka, Bangladesh) on adult females of T. macfarlanei, 15 mated females, aged three to five days, were placed on a fresh bean leaf disc (20 mm diameter). To ensure that the females were mated, we verified their mating status by examining their reproductive condition (presence of sperm in the reproductive tract) under a stereomicroscope (Olympus SZ 40, Tokyo, Japan). We determined the age of the females by observing and recording the time they completed their final molt to adulthood. This is typically achieved by rearing the mites from eggs and monitoring their developmental stages until they become adults. Once they reach the adult stage, we keep track of their age based on the duration from their final molt to the time of the experiment. This ensures that the females used in this study are within the specified age range, maintaining consistency and accuracy in the experimental results. After 24 h, dead or injured mites were removed. Spirotetramat suspensions (0, 1.2, 2.4, 4.8, 9.6, 19.2, 38.4, 76.8, and 153.6 mg/L) were then sprayed onto the discs containing the remaining females (15 female mites per lead disc). With four replications for each concentration, this resulted in 60 female mites per concentration treatment, totaling 540 females, at an application rate of 0.25 mL/cm2 using a hand sprayer. The concentrations of spirotetramat chosen for the experiment were selected to cover a range that would include both sublethal and potentially lethal concentrations and an untreated control (no application spirotetramat). The sprayed mites on leaf discs were dried in the shade. All experiments were performed under the same conditions. Mites that did not move their appendages when touched with a fine brush were recorded as “dead” [41].
After applying spirotetramat at different concentrations, various toxic effects were observed. Based on the initial toxicity observed in adult mites, the LC15, LC30, LC50, and LC90 concentrations were measured. LC15, LC30, LC50, and LC90 represent the concentrations of the substance that cause mortality in 15%, 30%, 50%, and 90% of the test population, respectively. The concentrations of spirotetramat used in the experiment were selected based on preliminary toxicity tests conducted on adult mites. These initial tests helped determine the range of concentrations that would effectively assess both the lethal and sublethal effects of the pesticide on T. macfarlanei. The chosen concentrations—0, 1.2, 2.4, 4.8, 9.6, 19.2, 38.4, 76.8, and 153.6 mg/L—were designed to cover a broad spectrum, from very low to high concentrations, ensuring a comprehensive evaluation of spirotetramat’s impact on the mites. Subsequently, LC15 and LC30 concentrations of spirotetramat were applied to adult female T. macfarlanei, along with their host plant.

2.3. Immature Development Duration of F1 Generation

Single gravid females from cultures treated with specific concentrations were collected randomly and placed on bean leaf discs (20 mm diameter). Newly laid eggs were individually transferred to fresh leaf discs, and their developmental stages were monitored every 12 h until they reached adulthood. The sex of the spider mites was determined at the teleiochrysalis stage under the stereomicroscope, and observed until they reached the adult stage.

2.4. Reproduction and Longevity of Females of F1 Generation

When a female reached the deutonymph stage, a single male from the mass culture was placed on the leaf disc for mating. The male remained on the disc throughout the study period and was replaced if it died before the female died; however, these replacement males were omitted from the analyses. The females were monitored every 12 h to determine the pre-oviposition period.
Newly emerged females from the same environmental conditions were used to study reproductive traits and longevity. Each female’s daily egg production was recorded using the stereomicroscope. These data were used to determine the oviposition period, total eggs laid per female, daily eggs laid per female, post-oviposition period, and female longevity until all mites had died.

2.5. Life Table Parameters

Raw data on development, survival, longevity, and female daily fecundity of T. macfarlanei were analyzed using the age-stage, two-sex life table method using the TWOSEX-MSChart software [42]. In the life table study, only viable, hatched eggs are considered to ensure accurate estimation of population parameters [43]. The age-stage-specific survival rate (sxj), age-specific survival rate (lx), age-stage-specific fecundity (fxj), age-specific fecundity (mx), and population parameters, including net reproductive rate (R0), intrinsic rate of increase (r), finite rate of increase (λ), and mean generation time (t), were calculated using established equations [44,45]. The age-stage life expectancy (exj), oviposition days (Od), mean fecundity of reproductive female (Fr), and age-stage reproductive value (vxj) was also calculated [46,47].

2.6. Statistical Analyses

The lethal and sub-lethal concentration (LC15, LC30, LC50, and LC90) values, along with the slopes and 95% confidence limits, were calculated by probit analysis using POLOPlus software version 2.0 (LeOra Software, Berkeley, CA, USA) [48]. Significant differences were determined by the non-overlapping 95% confidence limits.
The age-stage survival rates and fecundity of different concentrations of spirotetramat were determined using TWOSEX-MSChart software (version 2024.07.06) [42]. Variances and standard errors of population parameters were estimated via bootstrap analysis. Given that bootstrap analysis involves random resampling, a small number of replications can lead to variable means and standard errors. Therefore, a large number of bootstrap replications were used to ensure accurate and stable estimates of these parameters. To minimize this variability, we performed 100,000 bootstrap iterations. Differences among treatments were then assessed using the paired bootstrap test [49].

3. Results

3.1. Toxicity of Spirotetramat to T. macfarlanei Females of Parent Generation

Spirotetramat is highly toxic to adult females of T. macfarlanei. The concentrations required to kill 15, 30, 50, and 90 percent of test populations ranged from about 2.2 to about 332.81 mg·L−1 (Table 1).

3.2. The Development of Immatures in F1 Generation

The immature survival rate from egg to adult was lower in the LC15- and LC30-treated mites than in the control. The immature developmental period of T. macfarlanei was significantly affected by different concentrations of spirotetramat and sex (Table 2). The egg-hatching period showed differential response with the application of different concentrations of spirotetramat. A similar trend was also observed in larvae and protonymphs. The egg-to-adult development time of both males and females was significantly increased in the LC30 concentration of spirotetramat in comparison to LC15 and the control. The total development time from egg to adults of females was higher on LC30 in comparison to LC15 and the control (Table 2).

3.3. Adult Reproduction and Longevity of F1 Generation

The total pre-oviposition period, oviposition days, and female longevity of T. macfarlanei were not significantly affected by spirotetramat. The average pre-oviposition period increased with increasing spirotetramat concentration, but the periods were not significantly different (Table 3). The total pre-oviposition period showed a similar trend, being 16.07, 15.79, 16.49 days, respectively, in the control, as well as in the LC15 and LC30 dosages of spirotetramat. The oviposition days and female longevity decreased with increasing spirotetramat concentrations, but the number of days were not significantly different. The oviposition periods for the control, LC15, and LC30 groups were 11.47, 11.44, 10.34 days, and the female adult longevities were 28.80, 28.56, 29.26 days, respectively (Table 3). The number of eggs per female decreased with increasing spirotetramat concentration: the numbers in the control, LC15, and LC30 groups were 59.2, 56.1, 41.5, respectively (Table 3).

3.4. Life Table Parameters

The population parameters of T. macfarlanei reared on bean plants were affected by spirotetramat (Table 4). The net reproduction rate (R0), the intrinsic rate of natural increase (r), and the finite rate of increase (λ) of T. macfarlanei decreased with increasing spirotetramat concentrations (p < 0.001), while the gross reproduction rate (GRR) and the mean generation time (t) were not affected by spirotetramat.
The age-stage specific survivorship (sxj) curves of T. macfarlanei treated with spirotetramat were illustrated using an age-stage, two-sex life table (Figure 1). Overlapping stage-specific survivorship curves highlighted individual variation in developmental rates. The age-stage survival rate (lx) represents T. macfarlanei that emerged and survived to adulthood (Figure 1). Ignoring stage differentiation yields a simplified age-specific survival rate (lx).
Figure 2 shows the age-specific survival rate (lx), the age-specific fecundity (mx), and age-specific maternity (lxmx) for each treatment. The female T. macfarlanei began dying on days 13, 9, and 8 for the control, LC15, and LC30, respectively, with all females dead by days 45, 42, and 42 for the control, LC15, and LC30, respectively. Oviposition began on days 13, 13, and 14 for the control, LC15, and LC30, respectively. The peak mx occurred at 27, 23, and 21 days for the control, LC15, and LC30, respectively. The age-specific maternity (lxmx) followed a similar trend to the age-specific fecundity across all treatments.
To characterize the life expectancy (exj) of each age-stage group of T. macfarlanei, the expected lifespan of individuals at age x and stage j under different treatments was measured (Figure 3). For newly laid eggs reared under the control, LC15, and LC30 treatments of spirotetramats, the life expectancy was 28.3, 24.8, and 24.2 days, respectively (Figure 3). The peak life expectancy (exj) for adult females was 12 days on the control, 13 days on LC15, and 13 days under LC30 treatments (Figure 3).
Reproductive value defines an individual’s contribution to future population growth. The reproductive values (vxj) for T. macfarlanei at various ages and stages are shown in Figure 4. For newly laid eggs, the vxj were 1.2 days for the control, 1.2 days for the LC15, and 1.1 days for the LC30 treatments (Figure 4). The adult females at peak reproduction contributed significantly more to the population. The peak vxj for adult females were 25 days under the control, 17 days under the LC15, and 19 days under the LC30 treatments (Figure 4).

4. Discussion

Population analysis is an effective method for evaluating the lethal and sublethal effects of pesticides [34,50]. This study is the first to evaluate the sublethal effects of spirotetramat on the life-table parameters of T. macfarlanei. We found that sublethal concentrations of spirotetramat reduced the survival rate and fecundity of T. macfarlanei. In our study, the LC15 and LC30 concentrations of spirotetramat generally had negative effects on the life-table parameters of the spider mite, T. macfarlanei. These findings have several important implications for integrated pest management (IPM) strategies.
The sub-lethal concentrations of spirotetramat (LC15 and LC30) reduced survivorship, fecundity, and longevity, which suggests that these concentrations can effectively suppress mite populations. This can delay the development of mite resistance by reducing the selection pressure on the population. Sub-lethal concentrations can disrupt the population structure and reproductive potential of T. macfarlanei. Such disruptions can lead to a decrease in the intrinsic rate of increase (r), ultimately reducing the population growth rate. This aligns with the findings of Desneux et al. [8], who showed that sub-lethal effects can reduce pest populations over time.
Sub-lethal concentrations also reduce the effect of pesticides on the environment and help to preserve beneficial arthropods. Incorporating spirotetramat into an IPM program and rotating it with acaricides with different modes of action can prevent or delay the development of resistance in T. macfarlanei populations. Nauen et al. [51] discussed the importance of such rotation strategies in resistance management. Combining spirotetramat with biological control agents (e.g., predatory mites) can enhance the overall effectiveness of IPM programs. The compatibility of spirotetramat with hoverfly Episyrphus balteatus de Geer has been demonstrated, indicating its potential for use in integrated approaches [52]. In this study, the LC15 and LC30 concentrations of spirotetramat insecticide had progressively increasing negative effects on various life table parameters, including r and R0. Additionally, the development, fecundity, and survival rates were adversely impacted by both sub-lethal dosages. Sublethal concentrations of spirotetramat had similar adverse effects on the cabbage aphid [36]. The reproductive parameters in mites treated with LC15 and LC30 were altered compared to the control, affecting their survivability and reproduction. The lethal and sublethal effects of spirotetramat on T. urticae demonstrated that spirotetramat could effectively act as an acaricide against motile stages [29]. Untreated mites had a survival rate of 0.72, while female mites treated with spirotetramat had significantly lower survival rates: 0.40 at 2 mg/L, 0.27 at 20 mg/L, and 0.05 at 200 mg/L. Spirotetramat also reduced both gross fecundity (9% at 2 mg/L, 29% at 20 mg/L, and 93% at 200 mg/L) and net fecundity (40% at 2 mg/L, 67% at 20 mg/L, and 98% at 200 mg/L) compared to the control group. These findings suggest that spirotetramat has a strong sub-lethal effect on the survivability and fecundity of T. urticae [29]. The sublethal concentration of spirotetramat affected the survivorship and fecundity of Neoseiulus californicus McGregor [53]. The intrinsic rate of increase is a critical factor in describing the effect of pesticides on pests [22,33] because it encompasses overall effects on both survivorship and fecundity [32]. Our research demonstrated that spirotetramat decreased the intrinsic rate of increase in T. macfarlanei, similar to previous findings [32].
Other parameters, such as sxj, lx, and vxj help to clarify the conflicting effects of insecticides on population growth and the development of various insect and mite pests [36,37,38]. Since lx is a basic form of sxj, the lx curve for the acaricide-exposed group shows that spirotetramat primarily affects survival rates during the immature stages [54]. Additionally, the decrease in mx and lxmx curves in the insecticide-treated groups indicates that the reproductive success is negatively impacted by spirotetramat, a finding that is supported by previous works [54,55].
We previously evaluated the effects of bifenazate on T. truncatus Ehara [33], whereas the current research investigates spirotetramat on T. macfarlanei. While our earlier work examined how bifenazate affected T. truncatus, this study looks at a different insecticide and species, allowing us to compare the effects of two different treatments on two distinct pests. The biological impact and mechanisms of action of these acaricides are different, warranting separate studies. This research is part of a broader series aimed at understanding the effects of various acaricides on different spider mite species, with the goal of developing effective and sustainable pest management strategies. Each study provides unique insights into the specific acaricide–species interactions.

5. Conclusions

Our findings reveal that both lethal and sublethal concentrations of spirotetramat significantly impact key biological parameters, including the survival rate and fecundity. Spirotetramat effectively reduces the survival and reproductive potential of T. macfarlanei, even at lower concentrations (LC15 and LC30). These sublethal effects can disrupt population dynamics by decreasing the intrinsic rate of increase (r), thereby reducing population growth rates. This supports previous research on the role of sublethal effects in integrated pest management (IPM) and suggests that spirotetramat can be a valuable tool for managing mite populations sustainably.
This study highlights the potential for using spirotetramat at reduced concentrations to minimize environmental impact, while effectively controlling spider mites. Lower dosages reduce the overall chemical load and help preserve non-target organisms and beneficial arthropods. Incorporating spirotetramat into an IPM strategy can aid in resistance management when combined with rotation strategies involving other acaricides. Additionally, integrating spirotetramat with biological control agents could further enhance IPM effectiveness.
Future research should investigate the long-term ecological effects of sublethal spirotetramat on non-target species and ecosystems, as well as assess its impact on the development of resistance in pest populations. This will provide a comprehensive understanding of both the broader environmental effects and the potential for resistance, informing more effective pest management strategies. Field trials are essential for validating lab findings and assessing practical applications in agriculture. Exploring resistance management strategies, including rotation with other pesticides, and examining their compatibility with biological control agents will optimize IPM strategies.

Author Contributions

Conceptualization, F.A.S., P.M. and M.S.U.; investigation, F.A.S., P.M., S.M.B. and T.H.; formal analysis, M.S.U.; writing—original draft, M.S.U. and T.G.; supervision, M.S.U. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Ethical review and approval were waived for this study.

Informed Consent Statement

Informed consent was obtained from all subjects involved in this study.

Data Availability Statement

The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Jeppson, L.R.; Keifer, H.H.; Baker, E.W. Mites Injurious to Economic Plants; University of California Press: Berkeley, CA, USA, 1975; p. 614. [Google Scholar]
  2. Bolland, H.R.; Gutierrez, J.; Flechtmann, C.H. World Catalogue of the Spider Mite Family (Acari: Tetranychidae); Brill Academic Publishers: Leiden, The Netherlands, 1998; p. 392. [Google Scholar]
  3. Ullah, M.S.; Gotoh, T. Laboratory-based toxicity of some acaricides to Tetranychus macfarlanei and Tetranychus truncatus (Acari: Tetranychidae). Int. J. Acarol. 2013, 39, 244–251. [Google Scholar] [CrossRef]
  4. Ullah, M.S.; Haque, M.A.; Nachman, G.; Gotoh, T. Temperature dependent development and reproductive traits of Tetranychus macfarlanei (Acari: Tetranychidae). Exp. Appl. Acarol. 2012, 56, 327–344. [Google Scholar] [CrossRef] [PubMed]
  5. Ullah, M.S.; Hossain, M.A.; Jahan, M.; Sarker, M.A.; Hamim, I. A Field Guide of Major Insect Pests and Diseases of Different Crops in Bangladesh; Bangladesh Agricultural University Extension Centre (BAUEC): Mymensingh, Bangladesh, 2021; p. 500. [Google Scholar]
  6. Migeon, A.; Dorkeld, F. Spider Mites Web: A Comprehensive Database for the Tetranychidae. 2024. Available online: https://www1.montpellier.inra.fr/CBGP/spmweb/ (accessed on 10 June 2024).
  7. Van Leeuwen, T.; Vontas, J.; Tsagkarakou, A.; Tirry, L. Mechanisms of acaricide resistance in the two-spotted spider mite Tetranychus urticae. In Biorational Control of Arthropod Pests; Ishaaya, I., Horowitz, A.R., Eds.; Springer: Dordrecht, The Netherlands, 2009; pp. 347–393. [Google Scholar]
  8. Desneux, N.; Decourtye, A.; Delpuech, J.M. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 2007, 52, 81–106. [Google Scholar] [CrossRef] [PubMed]
  9. Lee, C.Y. Sublethal effects of insecticide on longevity, fecundity, and behaviour of insect pests: A review. Biosci. J. 2000, 11, 107–112. [Google Scholar]
  10. Singh, J.P.; Marwaha, K.K. Effects of sublethal concentrations of some insecticides on growth and development of maize stalk borer, Chilo partellus (Swinhoe) larvae. Shashpa 2000, 7, 181–186. [Google Scholar]
  11. Babcock, J.M.; Gerwick, C.B.; Huang, J.X.; Loso, M.R.; Nakamura, G.; Nolting, S.P.; Rogers, R.B.; Sparks, T.C.; Thomas, J.; Watson, G.B.; et al. Biological characterization of sulfoxaflor, a novel insecticide. Pest. Manag. Sci. 2011, 67, 328–334. [Google Scholar] [CrossRef]
  12. Brück, E.; Elbert, A.; Fischer, R.; Krueger, S.; Kühnhold, J.; Klueken, A.M.; Nauen, R.; Niebes, J.F.; Reckmann, U.; Schnorbach, H.J. Movento®, an innovative ambimobile insecticide for sucking insect pest control in agriculture: Biological profile and field performance. Crop Prot. 2009, 28, 838–844. [Google Scholar] [CrossRef]
  13. Wang, X.; Song, Y.; Sun, H.; Zhu, J. Evaluation of the demographic potential of Aphelinus albipodus (Hymenoptera: Aphelinidae) with Aphis glycines (Homoptera: Aphididae) as alternate host at various temperatures. Appl. Entomol. Zool. 2016, 51, 247–255. [Google Scholar] [CrossRef]
  14. Salazar-López, N.J.; Aldana-Madrid, M.L.; Silveira-Gramont, M.I.; Aguiar, J.L. Spirotetramat—An Alternative for the Control of Parasitic Sucking Insects and Its Fate in the Environment; IntechOpen: London, UK, 2016; ISBN 978-953-51-2258-6. [Google Scholar]
  15. Gong, Y.; Shi, X.; Desneux, N.; Gao, X. Effects of spirotetramat treatments on fecundity and carboxylesterase expression of Aphis gossypii Glover. Ecotoxicology 2016, 25, 655–663. [Google Scholar] [CrossRef]
  16. Arrese, E.L.; Canavoso, L.E.; Jouni, Z.E.; Pennington, J.E.; Tsuchida, K.; Wells, M.A. Lipid storage and mobilization in insects: Current status and future directions. Insect Biochem. Mol. Biol. 2001, 31, 7–17. [Google Scholar] [CrossRef]
  17. Ouyang, Y.; Montez, G.H.; Liu, L.; Grafton-Cardwell, E.E. Spirodiclofen and spirotetramat bioassays for monitoring resistance in citrus red mite, Panonychus citri (Acari: Tetranychidae). Pest Manag. Sci. 2012, 68, 781–787. [Google Scholar] [CrossRef] [PubMed]
  18. Döker, İ.; Kazak, C.; Ay, R. Resistance status and detoxification enzyme activity in ten populations of Panonychus citri (Acari: Tetranychidae) from Turkey. Crop Prot. 2021, 141, 105488–105497. [Google Scholar] [CrossRef]
  19. Vermeer, R.; Baur, P. Movento® product development: Custom-made formulations for an exceptional active ingredient. Bayer CropSci. J. 2008, 61, 141–157. [Google Scholar]
  20. Sverdrup, L.E.; Bjørge, C.; Eklo, O.M.; Grung, M.; Källqvist, T.; Klingen, I.; Låg, M.; Ropstad, E.; Øvrebø, S. Risk assessment of the insecticide Movento 100 SC with the active substance spirotetramat. Eur. J. Nutr. Food Saf. 2022, 14, 9–11. [Google Scholar] [CrossRef]
  21. Lashkari, M.R.; Sahragard, A.; Ghadamyari, M. Sublethal effects of imidacloprid and pymetrozine on population growth parameters of cabbage aphid, Brevicoryne brassicae on rapeseed, Brassica napus L. Insect Sci. 2007, 14, 207–212. [Google Scholar] [CrossRef]
  22. Stark, J.D.; Banks, J.E. Population-level effects of pesticides and other toxicants on arthropods. Annu. Rev. Entomol. 2003, 48, 505–519. [Google Scholar] [CrossRef]
  23. Mahmoodi, L.; Mehrkhou, F.; Guz, N.; Forouzan, M.; Atlihan, R. Sublethal effects of three insecticides on fitness parameters and population projection of Brevicoryne brassicae (Hemiptera: Aphididae). J. Econ. Entomol. 2020, 113, 2713–2722. [Google Scholar] [CrossRef]
  24. Ullah, F.; Gul, H.; Tariq, K.; Desneux, N.; Gao, X.; Song, D. Functional analysis of cytochrome P450 genes linked with acetamiprid resistance in melon aphid, Aphis gossypii. Pestic. Biochem. Physiol. 2020, 170, 104687. [Google Scholar] [CrossRef]
  25. Jie, M.; Gao, Y.; Kuang, D.; Shi, Y.; Wang, H.; Jing, W. Relationship between imidacloprid residues and control effect on cotton aphids in arid region. Environ. Geochem. Health 2021, 43, 1941–1952. [Google Scholar] [CrossRef]
  26. Liang, H.-Y.; Yang, X.-M.; Sun, L.-J.; Zhao, C.-D.; Chi, H.; Zheng, C.-Y. Sublethal effect of spirotetramat on the life table and population growth of Frankliniella occidentalis (Thysanoptera: Thripidae). Entomol. Gen. 2021, 41, 219–231. [Google Scholar] [CrossRef]
  27. Iftikhar, A.; Hafeez, F.; Aziz, M.A.; Hashim, M.; Naeem, A.; Yousaf, H.K.; Saleem, M.J.; Hussain, S.; Hafeez, M.; Ali, Q.; et al. Assessment of sublethal and transgenerational effects of spirotetramat, on population growth of cabbage aphid, Brevicoryne brassicae L. (Hemiptera: Aphididae). Front. Physiol. 2022, 13, 1014190. [Google Scholar] [CrossRef] [PubMed]
  28. Kim, S.E.; Kim, H.K.; Kim, G.H. Sublethal effects of spirotetramat, cyantraniliprole, and pymetrozine on Aphis gossypii (Hemiptera: Aphididae). Insects 2024, 15, 247. [Google Scholar] [CrossRef] [PubMed]
  29. Marcic, D.; Petronijevic, S.; Drobnjakovic, T.; Prijovic, M.; Peric, P.; Milenkovic, S. The effects of spirotetramat on life history traits and population growth of Tetranychus urticae (Acari: Tetranychidae). Exp. Appl. Acarol. 2012, 56, 113–122. [Google Scholar] [CrossRef] [PubMed]
  30. Beers, E.H.; Schmidt, R.A. Impacts of orchard pesticides on Galendromus occidentalis: Lethal and sublethal effects. Crop Prot. 2014, 56, 16–24. [Google Scholar] [CrossRef]
  31. Kim, M.; Sim, C.; Shin, D.; Suh, E.; Cho, K. Residual and sublethal effects of fenpyroximate and pyridaben on the instantaneous rate of increase of Tetranychus urticae. Crop Prot. 2006, 25, 542–548. [Google Scholar] [CrossRef]
  32. Li, Y.Y.; Fan, X.; Zhang, G.H.; Liu, Y.Q.; Chen, H.Q.; Liu, H.; Wang, J.J. Sublethal effects of Bifenazate on life history and population parameters of Tetranychus urticae (Acari: Tetranychidae). Syst. Appl. Acarol. 2017, 22, 148–158. [Google Scholar] [CrossRef]
  33. Rimy, S.J.; Das, G.; Gotoh, T.; Ullah, M.S. Lethal and sublethal effects of bifenazate on the biological parameters of Tetranychus truncatus Ehara (Acari: Tetranychidae). Syst. Appl. Acarol. 2021, 26, 2118–2132. [Google Scholar] [CrossRef]
  34. Chi, H.; Kavousi, A.; Gharekhani, G.; Atlihan, R.; Özgökçe, M.S.; Güncan, A.; Gökçe, A.; Smith, C.L.; Benelli, G.; Guedes, R.N.C.; et al. Advances in theory, data analysis, and application of the age-stage, two-sex life table for demographic research, biological control, and pest management. Entomol. Gen. 2023, 43, 705–732. [Google Scholar] [CrossRef]
  35. Southwood, T.R.E.; Henderson, P.A. Ecological Methods, 3rd ed.; Blackwell: Oxford, UK, 2000; p. 592. [Google Scholar]
  36. Iftikhar, A.; Hafeez, F.; Hafeez, M.; Farooq, M.; Asif Aziz, M.; Sohaib, M.; Naeem, A.; Lu, Y. Sublethal effects of a juvenile hormone analog, Pyriproxyfen on demographic parameters of non-target predator, Hippodamia convergens Guerin-Meneville (Coleoptera: Coccinellidae). Ecotoxicology 2020, 29, 1017–1028. [Google Scholar] [CrossRef]
  37. He, Y.; Zhao, J.; Zheng, Y.; Weng, Q.; Biondi, A.; Desneux, N.; Wu, K. Assessment of potential sublethal effects of various insecticides on key biological traits of the tobacco whitefly, Bemisia tabaci. Int. J. Biol. Sci. 2013, 9, 246–255. [Google Scholar] [CrossRef]
  38. Hafeez, M.; Li, X.; Yousaf, H.K.; Khan, M.M.; Imran, M.; Zhang, Z.; Shah, S.; Wang, L. Sublethal effects of bistrifluron on key biological traits, macronutrients contents and vitellogenin (SeVg) expression in Spodoptera exigua (Hübner). Pestic. Biochem. Physiol. 2021, 174, 104802. [Google Scholar] [CrossRef]
  39. Hoy, M.A. Agricultural Acarology: Introduction to Integrated Mite Management; CRC Press: Boca Raton, FL, USA, 2011; p. 430. [Google Scholar]
  40. Nishi, A.N.; Chowdhury, S.; Mondal, P.; Akram, M.W.; Ullah, M.S. Efficacy of entomopathogen Cordyceps tenuipes (Peck) Kepler, B. Shrestha et Spatafora against spider mite Tetranychus piercei McGregor (Acari: Tetranychidae). Int. J. Acarol. 2023, 49, 239–246. [Google Scholar] [CrossRef]
  41. Ullah, M.S.; Kobayashi, Y.; Gotoh, T. Development and reproductive capacity of the miyake spider mite Eotetranychus kankitus (Acari: Tetranychidae) at different temperatures. Insects 2022, 13, 910. [Google Scholar] [CrossRef]
  42. Chi, H. TWOSEX-MSChart: A Computer Program for the Age, Two Sex Life Table Analysis; National Chung Hsing University: Taichung, Taiwan, 2024. [Google Scholar]
  43. Mou, D.F.; Lee, C.C.; Smith, C.L.; Chi, H. Using viable eggs to accurately determine the demo graphic and predation potential of Harmonia dimidiata (Coleoptera: Coccinellidae). J. Appl. Entomol. 2015, 139, 579–591. [Google Scholar] [CrossRef]
  44. Chi, H.; Liu, H. Two new methods for the study of insect population ecology. Bull. Inst. Zool. Acad. Sin. 1985, 24, 225–240. [Google Scholar]
  45. Tuan, S.J.; Yeh, C.C.; Atlihan, R.; Chi, H. Linking life table and predation rate for biological control: A comparative study of Eocanthecona furcellata (Hemiptera: Pentatomidae) fed on Spodoptera litura (Lepidoptera: Noctuidae) and Plutella xylostella (Lepidoptera: Plutellidae). J. Econ. Entomol. 2016, 109, 13–24. [Google Scholar] [CrossRef]
  46. Chi, H. Life table analysis incorporating both sexes and variable development rates among individuals. Environ. Entomol. 1988, 17, 26–34. [Google Scholar] [CrossRef]
  47. Chen, G.M.; Chi, H.; Wang, R.C.; Wang, Y.P.; Xu, Y.Y.; Li, X.D.; Yin, P.; Zheng, F.Q. Demography and uncertainty of population growth of Conogethes punctiferalis (Lepidoptera: Crambidae) reared on five host plants with discussion on some life history statistics. J. Econ. Entomol. 2018, 111, 2143–2152. [Google Scholar] [CrossRef]
  48. Robertson, J.L.; Savin, N.E.; Savin, N.E.; Preisler, H.K. Bioassays with Arthropods, 2nd ed.; CRC Press: Boca Raton, FL, USA, 2007; p. 224. [Google Scholar]
  49. Efron, B.; Tibshirani, R.J. An Introduction to the Bootstrap; Chapman & Hall: New York, NY, USA, 1993; p. 456. [Google Scholar]
  50. Daniels, R.E.; Allan, J.D. Life table evaluation of chronic exposure to a pesticide. Can. J. Fish. Aquat. Sci. 1981, 38, 485–494. [Google Scholar] [CrossRef]
  51. Nauen, R. Insecticide mode of action: Return of the ryanodine receptor. Pest Manag. Sci. 2006, 62, 690–692. [Google Scholar] [CrossRef]
  52. Moens, J.; De Clercq, P.; Tirry, L. Side effects of pesticides on the larvae of the hoverfly Episyrphus balteatus in the laboratory. Phytoparasitica 2011, 39, 1–9. [Google Scholar] [CrossRef]
  53. Mollaloo, M.G.; Kheradmand, K.; Sadeghi, R.; Talebi, A.A. Demographic analysis of sublethal effects of spiromesifen on Neoseiulus californicus (Acari: Phytoseiidae). Acarologia 2017, 57, 571–580. [Google Scholar] [CrossRef]
  54. Liang, P.Z.; Ma, K.S.; Chen, X.W.; Tang, C.Y.; Xia, J.; Chi, H.; Gao, X.W. Toxicity and sublethal effects of flupyradifurone, a novel butenolide insecticide, on the development and fecundity of Aphis gossypii (Hemiptera: Aphididae). J. Econ. Entomol. 2019, 112, 852–858. [Google Scholar] [CrossRef]
  55. Tang, Q.; Xiang, M.; Hu, H.; An, C.; Gao, X. Evaluation of sublethal effects of sulfoxaflor on the green peach aphid (Hemiptera: Aphididae) using life table parameters. J. Econ. Entomol. 2015, 108, 2720–2728. [Google Scholar] [CrossRef]
Figure 1. Age-stage specific survival rates (sxj) of Tetranychus macfarlanei on different treatments of spirotetramat reared on bean plants at 25 °C under a 16L:8D photoperiod. The sxj curves at different spirotetramat dosages indicate the probability of newly emerged T. macfarlanei surviving to age x and stage j. L denotes larva, PN denotes protonymph, and DN denotes deutonymph.
Figure 1. Age-stage specific survival rates (sxj) of Tetranychus macfarlanei on different treatments of spirotetramat reared on bean plants at 25 °C under a 16L:8D photoperiod. The sxj curves at different spirotetramat dosages indicate the probability of newly emerged T. macfarlanei surviving to age x and stage j. L denotes larva, PN denotes protonymph, and DN denotes deutonymph.
Arthropoda 02 00016 g001
Figure 2. Age-specific survivability (lx), age-stage specific fecundity (fx5), age-specific fecundity (mx) and age-specific maternity (lxmx) of Tetranychus macfarlanei on different treatments of spirotetramat reared on bean plants at 25 °C under a 16L:8D photoperiod.
Figure 2. Age-specific survivability (lx), age-stage specific fecundity (fx5), age-specific fecundity (mx) and age-specific maternity (lxmx) of Tetranychus macfarlanei on different treatments of spirotetramat reared on bean plants at 25 °C under a 16L:8D photoperiod.
Arthropoda 02 00016 g002
Figure 3. Age-stage life expectancy (exj) of Tetranychus macfarlanei on different treatments of spirotetramat reared on bean plants at 25 °C under a 16L:8D photoperiod. L denotes larva, PN denotes protonymph, and DN denotes deutonymph.
Figure 3. Age-stage life expectancy (exj) of Tetranychus macfarlanei on different treatments of spirotetramat reared on bean plants at 25 °C under a 16L:8D photoperiod. L denotes larva, PN denotes protonymph, and DN denotes deutonymph.
Arthropoda 02 00016 g003
Figure 4. Age-stage fecundity (vxj) of Tetranychus macfarlanei on different treatments of spirotetramat reared on bean plants at 25 °C under a 16L:8D photoperiod. L denotes larva, PN denotes protonymph, and DN denotes deutonymph.
Figure 4. Age-stage fecundity (vxj) of Tetranychus macfarlanei on different treatments of spirotetramat reared on bean plants at 25 °C under a 16L:8D photoperiod. L denotes larva, PN denotes protonymph, and DN denotes deutonymph.
Arthropoda 02 00016 g004
Table 1. Toxicity of spirotetramat to Tetranychus macfarlanei adult.
Table 1. Toxicity of spirotetramat to Tetranychus macfarlanei adult.
ParametersValues
Slope1.060 ± 0.103
n480
χ21.116
Df6
LC15 (95% CL)2.160 (1.226–3.265)
LC30 (95% CL)6.572 (4.546–8.866)
LC50 (95% CL)20.541 (15.596–27.504)
LC90 (95% CL)332.811 (193.320–718.028)
Note: LC values are expressed in mg·L−1 (AI) of spirotetramat.
Table 2. Development duration in days (mean ± S.E.) from egg to adult of Tetranychus macfarlanei reared on different treatments of spirotetramat on bean plants at 25 °C under a 16L:8D photoperiod.
Table 2. Development duration in days (mean ± S.E.) from egg to adult of Tetranychus macfarlanei reared on different treatments of spirotetramat on bean plants at 25 °C under a 16L:8D photoperiod.
TreatmentSexN aEggLarvaProtonymphDeutonymphEgg to AdultSurvival (%)
Control406.35 ± 0.11 b2.73 ± 0.09 b2.25 ± 0.08 a2.92 ± 0.08 a14.25 ± 0.12 bc98.8
396.44 ± 0.14 ab3.03 ± 0.13 ab2.36 ± 0.11 a2.62 ± 0.10 bc14.44 ± 0.13 ab
LC15346.24 ± 0.19 b2.74 ± 0.11 b2.18 ± 0.09 b2.85 ± 0.09 ab14.00 ± 0.21 c80.0
306.93 ± 0.24 a3.10 ± 0.18 ab2.47 ± 0.11 a2.37 ± 0.18 c14.87 ± 0.20 a
LC30356.37 ± 0.10 b2.80 ±0.11 b2.31 ± 0.08 a2.91 ± 0.10 a14.40 ± 0.13 bc82.5
316.65 ± 0.19 ab3.26 ± 0.16 a2.39 ± 0.10 a2.45 ± 0.12 c14.74 ± 0.20 ab
a Number of individuals tested. The letters “a, b, c, ab, bc” are used to denote statistical significance based on paired bootstrap match method. Mean values followed by the same letter are not significantly different from each other.
Table 3. Average pre-oviposition period (APOP), total pre-oviposition period (TPOP), oviposition days, female longevity in days (mean ± S.E.), and eggs per female (number ± S.E.) of Tetranychus macfarlanei reared on different treatments of spirotetramat on bean plants at 25 °C under a 16L:8D photoperiod.
Table 3. Average pre-oviposition period (APOP), total pre-oviposition period (TPOP), oviposition days, female longevity in days (mean ± S.E.), and eggs per female (number ± S.E.) of Tetranychus macfarlanei reared on different treatments of spirotetramat on bean plants at 25 °C under a 16L:8D photoperiod.
TreatmentN aAPOPTPOPOviposition DaysFemale LongevityEggs Per Female
Control401.82 ± 0.13 a16.07 ± 0.15 a11.47 ± 1.00 a28.80 ± 1.05 a59.20 ± 6.17 a
LC15541.79 ± 0.13 a15.79 ± 0.24 a11.44 ± 1.04 a28.56 ± 1.09 a56.12 ± 6.60 ab
LC30522.09 ± 0.25 a16.49 ± 0.29 a10.34 ± 1.10 a29.26 ± 1.27 a41.46 ± 4.96 b
a Number of individuals tested. The letters “a, b, ab” are used to denote statistical significance based on paired bootstrap match method. Mean values followed by the same letter are not significantly different from each other.
Table 4. Demographic parameters (mean ± S.E.) of Tetranychus macfarlanei reared on different treatments of spirotetramat on bean plants at 25 °C under a 16L:8D photoperiod: net reproductive rate (R0), intrinsic rate of increase (r, day−1), mean generation time (t, day), finite rate of increase (λ), and gross reproduction rate (GRR).
Table 4. Demographic parameters (mean ± S.E.) of Tetranychus macfarlanei reared on different treatments of spirotetramat on bean plants at 25 °C under a 16L:8D photoperiod: net reproductive rate (R0), intrinsic rate of increase (r, day−1), mean generation time (t, day), finite rate of increase (λ), and gross reproduction rate (GRR).
TreatmentR0rtλGRR
Control29.60 ± 4.52 a0.1500 ± 0.0063 a22.59 ± 0.43 a1.1618 ± 0.0073 a55.60 ± 9.47 a
LC1523.85 ± 4.15 ab0.1412 ± 0.0075 ab22.46 ± 0.44 a1.1516 ± 0.0086 ab56.24 ± 10.98 a
LC3018.14 ± 3.143 b0.1276 ± 0.0076 b22.72 ± 0.38 a1.1361 ± 0.0086 b44.88 ± 5.99 a
The letters “a, b, ab” are used to denote statistical significance based on paired bootstrap match method. Mean values followed by the same letter are not significantly different from each other.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Swarna, F.A.; Hayder, T.; Barsa, S.M.; Mondal, P.; Gotoh, T.; Ullah, M.S. Lethal and Sub-Lethal Effects of Spirotetramat on Red Spider Mite, Tetranychus macfarlanei Baker and Pritchard (Acari: Tetranychidae). Arthropoda 2024, 2, 212-225. https://doi.org/10.3390/arthropoda2030016

AMA Style

Swarna FA, Hayder T, Barsa SM, Mondal P, Gotoh T, Ullah MS. Lethal and Sub-Lethal Effects of Spirotetramat on Red Spider Mite, Tetranychus macfarlanei Baker and Pritchard (Acari: Tetranychidae). Arthropoda. 2024; 2(3):212-225. https://doi.org/10.3390/arthropoda2030016

Chicago/Turabian Style

Swarna, Farhana Afrose, Tasfia Hayder, Shreema Mandal Barsa, Powlomee Mondal, Tetsuo Gotoh, and Mohammad Shaef Ullah. 2024. "Lethal and Sub-Lethal Effects of Spirotetramat on Red Spider Mite, Tetranychus macfarlanei Baker and Pritchard (Acari: Tetranychidae)" Arthropoda 2, no. 3: 212-225. https://doi.org/10.3390/arthropoda2030016

Article Metrics

Back to TopTop