Compatibility of chlorantraniliprole with the generalist predator Coccinella septempunctata L. (Coleoptera: Coccinellidae) based toxicity, life-cycle development and population parameters in laboratory microcosms

Chemosphere 225 (2019) 182e190

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Compatibility of chlorantraniliprole with the generalist predator Coccinella septempunctata L. (Coleoptera: Coccinellidae) based toxicity, life-cycle development and population parameters in laboratory microcosms Falin He a, Shiang Sun a, Haili Tan a, Xiao Sun a, Dianlong Shang a, Chentao Yao a, Chao Qin b, Shoumin Ji b, Xiangdong Li c, Jiwang Zhang d, Xingyin Jiang a, b, * a Key Laboratory of Pesticide Toxicology and Application Technique, College of Plant Protection, Shandong Agricultural University, Tai'an, Shandong, 271018, China b Research Center of Pesticide Environmental Toxicology, Shandong Agricultural University, Tai'an, Shandong, 271018, China c Shandong Provincial Key Laboratory of Agricultural Microbiology, College of Plant Protection, Shandong Agricultural University, Tai'an, Shandong, 271018, China d State Key Laboratory of Crop Biology, College of Agronomy, Shandong Agricultural University, Tai'an, Shandong, 271018, China

h i g h l i g h t s

g r a p h i c a l a b s t r a c t


Chlorantraniliprole exhibited relatively low contact toxicity to 2nd instar larvae of Coccinella septempunctata.
Chlorantraniliprole was harmless and/or slightly harmful to C. septempunctata larvae and presented a low toxicity risk.
Chlorantraniliprole significantly affected the survival, development, and predation ability of C. septempunctata.
Chlorantraniliprole strongly affected the fecundity, fertility, and population parameters of C. septempunctata.

a r t i c l e i n f o

a b s t r a c t

Article history: Received 9 January 2019 Received in revised form 4 March 2019 Accepted 5 March 2019 Available online 6 March 2019

Coccinella septempunctata is a common insect predator that provides biological control of many destructive arthropod pests. An assessment of the toxicity of pesticides to predators is a necessary component of Integrated Pest Management (IPM) strategies. In order to evaluate the risks of field insecticide application, we studied the influence of chlorantraniliprole on C. septempunctata larvae using different exposure doses. Chlorantraniliprole exhibited low contact toxicity against 2nd instar larvae of C. septempunctata with the LR50 was 482.7063 g a.i. ha1 by after a 72-h exposure. In a long-term test, the LR50 of chlorantraniliprole for C. septempunctata decreased from 88.97 to 58.22 g a.i. ha1, while the hazard quotient (HQ) values were below the threshold value of 2 during the entire observation period. This indicated a low toxicity risk from insecticide exposure. The total effect (E) suggested that chlorantraniliprole could be classified as harmless/slightly harmful to C. septempunctata below/at 200% of the MRFR (the manufacturer maximum recommended field rate) of 120 g a.i. ha1. We also determined no

Handling Editor: Willie Peijnenburg Keywords: Chlorantraniliprole Coccinella septempunctata

* Corresponding author. College of Plant Protection, Shandong Agricultural University, Tai'an, Shandong, 271018, China. E-mail address: [email protected] (X. Jiang). https://doi.org/10.1016/j.chemosphere.2019.03.025 0045-6535/© 2019 Elsevier Ltd. All rights reserved.

F. He et al. / Chemosphere 225 (2019) 182e190 Toxicity Survival Development Population parameters

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observed effect application rates (NOERs) of chlorantraniliprole on survival (7.5 g a.i. ha1), developmental time (15 g a.i. ha1) and fecundity (30 g a.i. ha1). Chlorantraniliprole significantly reduced the pupation rate, adult emergence, egg hatchability, and predation success. Population parameters, including R0, r, l, and T were significantly affected when C. septempunctata were treated with chlorantraniliprole at higher label rates. These results demonstrated that the use of chlorantraniliprole may reduce C. septempunctata population levels and the level of biological control provided by this species. © 2019 Elsevier Ltd. All rights reserved.

1. Introduction The seven-spotted lady beetle, Coccinella septempunctata L. (Coleoptera: Coccinellidae), is a generalist predator and a natural enemy of aphids in China (Yu et al., 2014a). It is common in many agricultural ecosystems and has a worldwide distribution (Singh et al., 2004). Both the larval and adult stages of C. septempunctata can provide effective control of aphid populations (Jiang et al., 2018a). Coccinella septempunctata also consumes many other agricultural insect pests (e.g., Aphidoidea, Coccoidea, Tetranychidae, Psylloidea, and mites) (Hodek and Michaud, 2008; Lu et al., 2012; Yu et al., 2014b). C. septempunctata is a useful biological control agent with a voracious appetite and it can rapidly respond to aphid populations in Integrated Pest Management programs (IPM) € lkl et al., 2007). (Bianchi and Werf, 2004; Landis et al., 2004; Vo C. septempunctata has been mass-reared and released for the control of arthropod pests (Simelane et al., 2008a,b). It is an ideal species for studying the potential negative impacts of new pesticides on non-target organisms. These data can then be submitted, along with other required data, in applications for registration of € lkl et al., 2007; Jiang et al., 2018a). new insecticides (Vo Agrochemicals can reduce direct and indirect crop losses or damage caused by herbivores (Santos et al., 2015). Traditional control strategies for pests in greenhouses and outdoor agriculture mainly depend on chemical insecticides (Schneider et al., 2009; Fogel et al., 2016). Broad-spectrum insecticides are highly toxic to target pests and are typically toxic to non-target organisms such as predators and parasitoids (Fogel et al., 2013; Martinou et al., 2014; Rimoldi et al., 2017), which are important regulators of insect pest populations (Juen et al., 2012; Lu et al., 2012). The overuse of insecticides can reduce biological control effectiveness, increase pesticide resistance, and lead to the recovery of pest populations (Barbosa et al., 2017). Therefore, the compatibility of pesticides and beneficial arthropods is an important research topic (He et al., 2012; Yu et al., 2014a). Some selective insecticides are relatively more compatible with the biological control components of IPM systems (Galvan et al., 2005a). Effective alternatives to pest management strategies based solely on pesticides are needed (Galvan et al., 2005b). Diamide insecticides, such as chlorantraniliprole, have a unique mode of action and this is the fourth most commonly used insecticide class in the world (Cui et al., 2016; Liu et al., 2018). These compounds act on the insect ryanodine receptor (RyR) and lead to Ca2þ depletion, feeding cessation, lethargy, muscle paralysis and eventually death (Troczka et al., 2012; Selby et al., 2013). Due to higher toxicity, greater selectivity and wider insecticidal range, diamides are replacing major uses of other high-risk insecticides such as neonicotinoids (Isaacs et al., 2012). In China, chlorantraniliprole is registered to control most lepidopteran pests and other pests such as whiteflies, thrips, tephritid fruit flies, beetles, and psyllids (Sattelle et al., 2008; Teixeira and Andaloro, 2013; Cui et al., 2016). However, insecticide use can have a negative effect on beneficial nontarget organisms such as ladybird beetles

(Coccinellidae) and reduce agroecosystem biodiversity (Fogel et al., 2016). The harmful effects of insecticides on beneficial arthropods are n et al., 2015; Fernandes et al., 2016) but well known (Garzo chlorantraniliprole appears to be relatively less toxic to predators and parasitoids (Brugger et al., 2010; Gontijo et al., 2015). However, adverse effects were observed after Hippodamia convergens and Coleomegilla maculata were exposed to this insecticide (Moscardini et al., 2015; Nawaz et al., 2017). Differences in pesticide sensitivity of different life stages of natural enemies have also been demonstrated (Yu et al., 2014a; He et al., 2018). Often, the larval stages of predators are more susceptible to insecticides than the adult stage n et al., 2015; Santos et al., 2017). (Garzo Effects of agrochemicals on beneficial arthropods include shortterm toxicity, physiological, biochemical, and behavioral processes (Steel et al., 2011; He et al., 2012; Fogel et al., 2013). In addition, the long-term sublethal effects of insecticides on natural enemies should receive more attention before field use (Yu et al., 2014b). Sublethal effects can adversely affect life parameters such as survival, growth, developmental, fecundity, longevity, weight, feeding, mobility, behavior, and so on (Galvan et al., 2005a; Rahmani and Bandani, 2013). Exposure can occur from direct contact with spray residues or by feeding on plant material or prey contaminated with pesticides (Cloyd and Bethke, 2011; He et al., 2012). The end result is often a decrease of biocontrol effectiveness in agroecosystems (He et al., 2018). Determining the toxicity of pesticides to predators is required for effective IPM strategies (Desneux et al., 2007; Jiang et al., 2018a). Age related life table analyses have been used to describe population dynamics and evaluate the sublethal effects of insecticides on both pests and natural enemies (Chi and Getz, 1988; Rahmani and Bandani, 2013; Zheng et al., 2017). Demographic parameters can be used to study the comprehensive effects of insecticides on both pests and natural enemies. Despite the potential of C. septempunctata as a biological-control agent of arthropod insect pests, no studies have examined its susceptibility to chlorantraniliprole at label rates. The present study evaluated the direct toxicity and ecotoxicological risks of chlorantraniliprole to C. septempunctata under laboratory conditions. We also determined the sublethal effects of different rates of chlorantraniliprole on the growth and development, survival, longevity, fecundity and fertility, and population parameters of C. septempunctata using an age-stage, two-sex life table. These results provide information on the compatibility and optimum application rates of chlorantraniliprole in IPM systems.

2. Materials and methods 2.1. Insect colonies Coccinella septempunctata adults were collected in May 2016 from wheat fields (Triticum aestivum L.) managed without pesticide applications in Ningyang City (35.76 N, 116.80E), Shandong Province, China. Adults were transferred to mesh-covered cages

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(50 cm L  30 cm W  30 cm H) and the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), reared on pesticide free fava bean plants (Vicia faba L., Fabaceae) were constantly provided as food. Rearing was at 23 ± 1  C, 50e70% RH and a 16:8 h (L:D) photoperiod in a climate-controlled room. When egg clusters were found, the eggs were collected and moved to new Petri dishes to hatch. Neonates were maintained individually in glass Petri dishes, and reared on aphids until they reached the desired developmental stages (second-instar larvae) for bioassay. The pupae collected and moved to fresh Petri dishes until adult emergence. Eggs, larvae and pupae were kept in another climate-controlled incubator at 25 ± 1  C, 70% RH and a 16:8 h (L:D) photoperiod. 2.2. Insecticides Chlorantraniliprole (technical grade, 98% purity) was obtained from Shandong Weifang Runfeng Chemical Industry Co., Ltd., China. The maximum recommended field rate (MRFR) of chlorantraniliprole is 60 g a.i. ha1 registered at the pesticide information network of the People's Republic of China (http://www.icama.org. cn/fwb/index.jhtml) (accessed 1 January 2018). We assume that the 60 g a.i. ha1 of active ingredient is applied with 450 L of water per hectare. 2.3. Bioassays Toxicity of the insecticide doses to 2nd instar C. septempunctata larvae (<24 h old) was conducted, using a residual contact assay. Newly molted larvae were exposed to the insecticide through direct contact with spray droplets via a Potter spray tower (Burkard Scientific Co., Uxbridge, UK) to simulate the spray application in field. Based on a preliminary 72 h acute toxicity experiment, the concentrations used for the assays were prepared by diluting the stock solution (chlorantraniliprole was dissolved with HPLC-grade acetone) with distilled water plus 0.1% polysorbate 80 as an emulsifier before each experiment. For each treatment the test larvae were transferred to individual Petri dishes (10 cm diam.) lined with 9-cm filter paper and anesthetized with CO2 for 5 s. They were then sprayed with 2 mL of test solutions in a Potter tower, adjusted to a 68.6 kPa pressure, resulting in 1.8 ± 0.1 mg/cm2 deposition of pesticide. These parameters are consistent with the criteria established by the Pesticides and Beneficial Organisms Working Group of the International Organization for Biological Control of Noxious Animals and Plants/ West Palearctic Regional Section (IOBC/WPRS) for pesticide toxicity studies on natural enemies (Hassan et al., 1994). After the spray treatment, the larvae were individually transferred to clean Petri dishes (10 cm diam.) lined with 9-cm moistened filter paper. The dishes were subsequently covered and sealed with PVC film to prevent larvae from escaping and maintained in a climatecontrolled room (25 ± 1  C temperature, 70% RH, and a 16:8 h (L:D) photoperiod). Aphids were provided ad libitum and refreshed daily. Mortality of the predator larvae was recorded at daily intervals during the observation period after treatment. Individuals that did not respond to a mild touch using a paint brush were considered dead. For each treatment, four replicates (120 2nd instar larvae) were used. The experimental design included a blank control treatment, sprayed with distilled water plus 0.1% polysorbate 80. The bioassay used a completely randomized design with seven treatments (different rates of chlorantraniliprole) and four replicates.

chlorantraniliprole doses at 200%, 100%, 50%, 25%, 12.5% of the maximum recommended field rate (MRFR) were used to evaluate long-term toxicity on 2nd instar larvae. At the beginning of the trial, newly molted 2nd instar larvae (<24 h) were randomly collected and transferred to Petri dishes (10 cm diam.). The toxicity test protocol was similar to that described in 2.3. Treated larvae were transferred to new Petri dishes, which were subsequently covered and sealed with PVC film to prevent larvae from escaping and kept in the same conditions (as in 2.3). For each treatment, 200 larvae were tested per replicate and there were four replicates for each treatment performed over time using a completely randomized study design. Mortality and development time of the larval and pupal stages were recorded. The larvae and pupae were checked daily until they reached the pupal stage and adult emergence, respectively. Larvae that did not successfully pupate and pupae from which adults did not emerge were considered dead. Adult beetles (<24 h old) were weighed on an electronic analytical balance (Sartorius, BT125D), and the females were identified and counted to determine the sex ratio (number of females to total adults). To determine the female pre-oviposition and oviposition period, longevities, and adult fecundity, newly emerged adults (<24 h) were paired at a 1:1 ratio in Petri dishes, provided with soybean aphids and kept in a climatecontrolled room with rearing conditions as described in Section 2.1. New eggs were recorded daily and the filter paper on which the eggs were laid was replaced with a new paper. More than 200 eggs (<24 h old) were randomly gathered in each treatment to evaluate fertility. The number of hatched larvae was checked and recorded daily for 7 d. Eggs that did not produce larvae during this period were regarded as dead. To determine the predation ability of larvae and adults of C. septempunctata, the A. glycines was abundantly provided and we recorded the number of the prey consumed. 2.5. Demographic growth parameters Demographic growth parameters were based on survival and development time of each stage, female fecundity of individuals tested of C. septempunctata from 2nd larvae treated with chlorantraniliprole. Life-table parameters were assessed for each treatment. Life tables were constructed using data for all individuals tested (including males, females and individuals that died in the immature stage) (Chi, 1988). 2.6. Risk assessment The HQ is a risk assessment method that can be used to determine the toxicological risk of pesticide products to non-target organisms (Jiang et al., 2018b). The HQ was estimated using following formula:

HQ ¼ the field recommended label rates of chlorantraniliprole =the LR50 of chlorantraniliprole to C: septempunctata larvae (1) when the HQ value is  2 the chemical represents a potential hazard to the predator, whereas a value < 2 indicates a lesser toxicity risk (Candolfi et al., 2001). The total effect (E) was estimated using the formula proposed by Overmeer and Zon (1982):

Eð%Þ ¼ 100  ð100  Mc Þ  ER

(2)

2.4. Long-term toxicity To simulate the degradation of pesticides under field conditions,

where: Mc¼the corrected mortality calculated according to the formula of Abbott (1925); and ER ¼ the mean weekly number of

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eggs laid by treated females/the mean weekly number of eggs laid in the control treatment. Based on the total effect, the pesticides were classified according to the standards for laboratory ecotoxicology tests proposed by IOBC/WPRS (Hassan et al., 1994). Different treatments were classified into the following toxicity categories: (I) harmless (E < 30%); (II) slightly harmful (30%  E  79%); (III) moderately harmful (80%  E  99%); and (IV) highly harmful (E > 99%) (Hassan et al., 1994). 2.7. Statistical analysis The data obtained from the toxicity tests were corrected using Abbott's formula (1925) before analysis. The LR50 was determined by probit analysis with SPSS software (version 23.0, SPSS Inc., Chicago, IL, USA). The NOER values were estimated by means of a one-way analysis of variance (ANOVA). Means were compared by Tukey's least significant difference (LSD) tests (P < 0.05) (Zar, 1996). The developmental time and survival rates across the different instars were analyzed using a repeated-measure ANOVA to examine differences among the treatments. 3. Results 3.1. Acute toxicity On the basis of the log-probit regression analysis, the 72-h LR50 values of chlorantraniliprole to 2nd instar larvae were estimated at 482.7063 g a.i. ha1, with a 95% confidence interval of 438.21e535.74 g a.i. ha1. The data fitted the linear model with the regression equation of y ¼ 1.7332x  0.3486 (c2 ¼ 6.426, P ¼ 0.5262, R2 ¼ 0.9831). Detailed results are shown in Table S1. 3.2. Effect of chlorantraniliprole on survival of C. septempunctata Effects of chlorantraniliprole on the survival rate of 2nd instar larvae of C. septempunctata are shown in Fig. 1. The larval period normally lasts about 18 d followed by pupation. The survival rate decreased during the initial 3 d after insecticide exposure. Significant differences in percentage survival occurred between the insecticide treatment and the control treatment at 3rd day following treatment (ANOVA, P < 0.05; 18-day NOER > 120 g a.i. ha1). With a longer observational period, the survival rates of the first-generation larval stages in the 7.5, 15, 30, 60, 120 g a.i. ha1 treatments were 72.89%, 65.47%, 53.14%, 45.92%, and 35.63%, respectively (Fig. 1). The estimated LR50 for the first-generation larvae of C. septempunctata was 71.95 at the 3rd day after chlorantraniliprole treatment in the long-term laboratory microcosm test (Fig. 2). The LR50 of the first-generation C. septempunctata larvae was 58.22 g a.i. ha1 on the 12th day after chlorantraniliprole treatment. After chlorantraniliprole treatment the HQ values for the larvae remained below the safety threshold value of 2 throughout the observation period (Fig. 2). 3.3. Effect of chlorantraniliprole on the development time of C. septempunctata Chlorantraniliprole treatment effected the development time of C. septempunctata (Table S2). The total developmental time in the control group was 68.61 ± 0.33 d and in the highest treatment it was 53.04 ± 0.45 d. Chlorantraniliprole shortened the entire developmental period of C. septempunctata. The NOER for the entire period was 15 g a.i. ha1 (P < 0.05). After treatment with chlorantraniliprole at 60 and 120 g a.i. ha1, the durations of three larval stages (2nd, 3rd, and 4th instar) of C. septempunctata were

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significantly shortened. A statistically significant difference could be proved for the duration of pupae after chlorantraniliprole treatments (P < 0.05, NOER ¼ 30 g a.i. ha1). The development time of adults was significantly reduced when 2nd instar larvae were exposed to chlorantraniliprole (P < 0.05, NOER ¼ 7.5 g a.i. ha1). At the highest dose (120 g a.i. ha1) chlorantraniliprole significantly shortened the adult pre-oviposition period (APOP). However, the 15 g a.i. ha1 treatment did not significantly lengthen the APOP. The total pre-oviposition period (TPOP) was significantly shortened by the 60 and 120 g a.i. ha1 treatments (P < 0.05, NOER ¼ 60 g a.i. ha1). 3.4. Effect of chlorantraniliprole on pupation and adult emergence of C. septempunctata There were significantly negative linear relationships between chlorantraniliprole dose and the pupation rate (R2 ¼ 0.9699, F ¼ 8.6945, df ¼ 5, 23, P < 0.001) and adult emergence (R2 ¼ 0.9877, F ¼ 11.3671, df ¼ 5, 23, P < 0.001) (Fig. 3). At the highest dose, the pupation rate of C. septempunctata decreased to 78.22%. Chlorantraniliprole significantly reduced the successful pupation of C. septempunctata (P < 0.05; NOER ¼ 7.5 g a.i. ha1) (Fig. 3A). At the highest chlorantraniliprole dose, adult emergence was 81.06%. Adult emergence after chlorantraniliprole treatment at 15, 30, 60, and 120 g a.i. ha1 was significantly lower than in the control (P < 0.05; NOER ¼ 15 g a.i. ha1) (Fig. 3B). 3.5. Effects of chlorantraniliprole on cumulative mortality, fecundity, and fertility of C. septempunctata and its total effect (E) A doseeresponse relationship throughout the whole generation was seen between the cumulative mortality and doses of chlorantraniliprole (F5,23 ¼ 78.65, P < 0.0001) (Table 1). Cumulative lethality was 67.37 ± 1.51% at the 200% MRFR (120 g a.i. ha1) dose of chlorantraniliprole. Significant differences in cumulative mortality occurred in the groups treated at dosages >7.5 g a.i. ha1 of chlorantraniliprole (P < 0.05; NOER ¼ 7.5 g a.i. ha1). A mean weekly number of 211.42 ± 7.39 eggs were laid by control female C. septempunctata (Table 1). Mean fecundity per female in the treatment groups at doses above 30 g a.i. ha1 was significantly reduced (P < 0.05; NOER ¼ 30 g a.i. ha1). Treatment effects of chlorantraniliprole on fertility (egg hatchability) of C. septempunctata are shown in Fig. 4. In the 30, 60, and 120 g a.i. ha1 treatments, the egg hatching percentage was significantly less than in the controls (P < 0.05; NOER ¼ 30 g a.i. ha1). The total treatment effect (E) is shown in Table 1. Chlorantraniliprole at 7.5 g a.i. ha1 (12.5% MRFR) appeared to be harmless (IOBC class I) and this is the level of safety. Doses >7.5 g a.i. ha1 (15, 30, 60, and 120 g a.i. ha1 for 25%, 50%, 100%, and 200% MRFR) are classified as slightly harmful (IOBC class II). 3.6. Effect of chlorantraniliprole on the proportion of female, fresh mass of adults, and deformed offspring of C. septempunctata Treatment-related effects of chlorantraniliprole on the proportion of females, fresh mass of adults and deformed offspring of C. septempunctata are shown in Table 1. A NOER of 120 g a.i. ha1 was calculated for the proportion of female C. septempunctata (P < 0.05; NOER  120 g a.i. ha1). At the highest treatment level (120 g a.i. ha1), the fresh mass of C. septempunctata was 28.22 ± 0.19 mg, which was significantly less than the control (P < 0.05; NOER ¼ 120 g a.i. ha1). The NOER for deformed offspring was 60 g a.i. ha1 (P < 0.05; NOER ¼ 60 g a.i. ha1).

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Fig. 1. Effect of chlorantraniliprole (g a.i. ha1) on survival rate of C. septempunctata larvae during a 18-day observation period in long-term toxicity test. Data are represented as means ± SE, (ANOVA, Tukey's LSD, P < 0.05).

Fig. 2. Estimated LR50 and HQ values of chlorantraniliprole for the first-generation larvae of C. septempunctata in the long-term microcosm test. Error bars represent 95% confidence intervals (95% CI). Hazard quotient (HQ) ¼ the recommended field rate (g a.i. ha1)/LR50 (g a.i. ha1) for C. septempunctata. The maximum recommended field rates (MRFR) of chlorantraniliprole (registered in China) against arthropod insect pests is 60 g a.i. ha1.

3.7. Effect of chlorantraniliprole on the predation ability of C. septempunctata The effects of chlorantraniliprole on the predation ability of larval and adult C. septempunctata are shown in Fig. 5. The average number of prey consumed by C. septempunctata control larvae was 148.36 ± 5.32 aphids in 96 h. At the higher doses of 60 and 120 g a.i. ha1, chlorantraniliprole significantly reduced the predation ability with 139.53 ± 9.74 and 126.99 ± 7.32 aphids, respectively (P < 0.05; NOER ¼ 60 g a.i. ha1). The mean number of preys consumed per control adult averaged 564.54 ± 18.36 aphids in 96 h. However,

chlorantraniliprole treatment reduced the predation ability of adults at concentrations above 60 g a.i. ha1 (P < 0.05; NOER ¼ 60 g a.i. ha1). 3.8. Effect of chlorantraniliprole on demographic parameters of C. septempunctata The C. septempunctata population parameters assessed were development time, survival, fecundity, and fertility. Chlorantraniliprole applied to 2nd instar C. septempunctata larvae significantly reduced the net reproduction rate (R0) compared to the

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Fig. 3. Effect of chlorantraniliprole on the pupation rate and adult emergence of C. septempunctata. Data are mean values ± SE. Different lowercase letters indicate significant differences among the treatments (ANOVA, Tukey's LSD, P < 0.05).

Table 1 Influence of chlorantraniliprole on the cumulative mortality of pre-adult period, sex ratio, fresh mass, fecundity, deformed eggs, total effect, and IOBC toxicity categories of insecticide applied on 2nd instar C. septempunctata larvae. Means in the same column followed by different lowercase letters indicate significant differences between treatment and control based on ANOVA and Tukey's LSD test (P < 0.05). Treatment

Concentration used (g proportion of a.i. ha1) female (%)

Fresh mass of adults (mg)

Deformed eggs (%)

Cumulative mortality (%)

Fecundity (eggs/ week/female)

Total effect (E)

IOBC toxicity categoeya

1.37 ± 0.32 c 1.42 ± 0.59 bc 1.38 ± 0.55 bc 1.85 ± 0.27 abc 2.93 ± 0.26 ab 3.39 ± 0.78 a F ¼ 6.52 df ¼ 5, 23 P ¼ 0.0013

11.27 ± 0.96 f 29.44 ± 1.43 e 38.23 ± 2.09 d 46.63 ± 1.37 c

211.42 ± 7.39 a 211.78 ± 5.21 a 202.04 ± 5.87 ab 186.77 ± 6.95 bc

29.32 40.97 52.85

I II II

57.41 ± 1.74 b 67.37 ± 1.51 a F ¼ 78.65 df ¼ 5, 23 P < 0.0001

180.82 ± 5.18 c 166.06 ± 4.32 d F ¼ 69.42 df ¼ 5, 23 P ¼ 0.0009

63.58 74.37 -

II II -

Control Chlorantraniliprole 12.5% MRFR 25% MRFR 50% MRFR

50.94 ± 0.63 a 50.36 ± 0.63 ab 50.40 ± 0.85 ab 50.05 ± 0.36 ab

29.83 ± 0.22 ab 30.17 ± 0.32 a 29.75 ± 0.21 ab 28.44 ± 0.16 bc

100% MRFR 200% MRFR

50.08 ± 0.91 ab 48.21 ± 1.22 b F ¼ 1.56 df ¼ 5, 23 P ¼ 0.2207

28.54 ± 0.27 bc 28.22 ± 0.19 c F ¼ 3.02 df ¼ 5, 23 P ¼ 0.0372

a The IOBC toxicity categories for laboratory experiments are in accordance with the total effects caused by insecticides: (I) harmless (E < 30%); (II) slightly harmful (30%  E  79%); (III) moderately harmful (80%  E  99%); and (IV) highly harmful (E > 99%).

highest dose (120 g a.i. ha1). Higher doses (15, 30, 60, and 120 g a.i. ha1) significantly lowered the mean generation time (T) compared to the control.

4. Discussion

Fig. 4. Impact of chlorantraniliprole on the fecundity and fertility of C. septempunctata. Data are mean values ± SE. Significant differences are indicated by different lowercase letters (ANOVA, Tukey's LSD, P < 0.05).

control (P < 0.05) (Table 2). The intrinsic rate of increase (r) was significantly decreased in the 30, 60, and 120 g a.i. ha1 treatments. The finite rate of increase (l) was significantly reduced at the

Our 72-h acute toxicity assay yielded an LR50 of 482.7063 g a.i. ha1 for 2nd instar C. septempunctata larvae exposed to chlorantraniliprole. However, in the long-term experiment, the chlorantraniliprole rate causing 50% mortality among C. septempunctata larvae at 72 h was considerably lower (71.95 g a.i. ha1). The difference between the 72 h LR50 values may be caused by the different fitness levels of the individuals used or different actual contact dosages experienced by individual ladybird (Jiang et al., 2018a). Other studies have documented differences between results of acute toxicity tests and long-term microcosm tests (Yu et al., 2014a; Jiang et al., 2018b). In the long-term test, the LR50 for first generation C. septempunctata larvae decreased to 58.22 g a.i. ha1 (at 12e18 d), due to the effects of cumulative mortality caused by the chlorantraniliprole. The LR50 values of the neonicotinoid insecticides, nitenpyram, clothianidin and imidacloprid gradually decreased during the larval period of C. septempunctata (Yu et al., 2014a; Jiang et al., 2018a). Yu et al. (2014b) had similar results after application of the insect growth regulator hexaflumuron. Our low HQ values (<2) indicated that chlorantraniliprole is relatively safe for C. septempunctata by residual contact

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Fig. 5. Influence of chlorantraniliprole on the predation ability of larvae and adults of C. septempunctata. Data are mean values ± SE. Different lowercase letters indicate significant differences among the treatments (ANOVA, Tukey's LSD, P < 0.05).

Table 2 Estimates of life table parameters of C. septempunctata when 2nd instar larvae were treated with chlorantraniliprole. Means followed by different letters in the same lowercase in the same row are significantly different based on ANOVA using Tukey's LSD test (P < 0.05). Treatment

Control Chlorantraniliprole

Concentration used (g a.i. ha1)

12.5% MRFR 25% MRFR 50% MRFR 100% MRFR 200% MRFR

Life table paprameters Net reproduction rate (R0) (female female1)

Intrinsic rate of increase (r) (female female1d1)

Finite rate of increase (l) (female female1d1)

Mean generation time (T) (d)

448.47 ± 23.85 a 377.11 ± 19.67 b 323.49 ± 37.21 b 219.53 ± 25.14 c 213.56 ± 31.16 c 118.14 ± 20.85 d

0.1224 ± 0.0028 a 0.1213 ± 0.0029 a 0.1185 ± 0.0039 ab 0.1099 ± 0.0013 b 0.0904 ± 0.0031 c 0.0892 ± 0.0017 c

1.1383 ± 0.0103 a 1.1377 ± 0.0080 a 1.1382 ± 0.0097 a 1.1205 ± 0.0021 ab 1.1088 ± 0.0044 ab 1.0684 ± 0.0264 b

71.38 ± 3.46 a 68.16 ± 2.14 ab 66.15 ± 4.71 b 63.74 ± 3.28 bc 61.19 ± 2.93 cd 57.86 ± 3.76 d

Standard errors were estimated using 200,000 bootstraps and compared with paired bootstrap tests based on the 5% significance level.

experiments. Conversely, the neonicotinoid insecticides at the recommended field rates can be highly toxic to predators. Jiang et al. (2018a) found a HQ value > 2 for clothianidin tested on C. septempunctata larvae. This is consistent with Yao et al. (2015), who reported a HQ value of 7.52 for Serangium japonicum (Coccinellidae) adults after a 24 h thiamethoxam exposure. This suggests a high toxicity risk of thiamethoxam to predators. Nevertheless, the HQ values for larval stage C. septempunctata were all less than the threshold value of 2, demonstrating that predators have relatively low risk to nitenpyram exposure (Jiang et al., 2018b). The toxicity level of an insecticide in a bioassay is dependent on the chemical group and the test insect species (Rugno et al., 2016; He et al., 2018). In addition, chemical pesticides are generally more toxic to immature stages than to adults (Rugno et al., 2016; Ono et al., 2017). The exposure routes of pesticides to predatory insects are largely by food contact (Angeli et al., 2000) and direct contact with residual deposits (Hassan et al., 2010). In our assay, exposure of C. septempunctata by direct contact (spray droplets) was used. Although we did not determine different exposure routes, our toxicity results indicated that chlorantraniliprole may pose some risks to C. septempunctata. In addition to acute toxicity (short-term effects), long-term toxicity effects including growth and development, survival and reproduction could also occur. These effects could lead to a reduction in offspring, lower population levels, and overall reduced effectiveness of these natural enemies in agricultural ecosystems (Fogel et al., 2016; He et al., 2018). In this study, the survival rate was lower in individuals treated with chlorantraniliprole, which is consistent with the effects of imidacloprid (Yu et al., 2014b), clothianidin (Jiang et al., 2018a), nitenpyram (Jiang et al., 2018b), and hexaflumuron (Yu et al., 2014b) on C. septempunctata. The application of chlorantraniliprole on target

crops should be timed to avoid the occurrence of large numbers of coccinellid larvae. Also, pesticides should be used, when possible, at rates below the maximum recommended label rate. Chlorantraniliprole at the 25% label rate of 15 g a.i. ha1 prolonged the larval development of C. septempunctata. These results are consistent with previous studies showing the effects of imidacloprid on natural enemies (He et al., 2012; Yu et al., 2014a; Xiao et al., 2016). Among treated larvae, metabolic energy is diverted to detoxification rather than being used for growth and development (Simelane et al., 2008a,b) and feeding behavior is also affected (Desneux et al., 2007). Chlorantraniliprole can also reduce the predation ability of larval and adult C. septempunctata. The foraging time and predation rate of other predators can be decreased after exposure to chlorantraniliprole, thiamethoxam and thiacloprid (Martinou et al., 2014; Yao et al., 2015). However, we found that the larval development time was significantly increased after exposure to chlorantraniliprole at 100% and 200% the label rate (60 and 120 g a.i. ha1). Additional factors that may prolong the larval stage remain to be determined. Side effects of chemicals on predators and parasitoids can be evaluated by several environmentally relevant endpoints (Desneux et al., 2007; Weltje et al., 2017), which can be used to demonstrate the safe margins of pesticides on non-target organisms for risk assessment (Kyong et al., 2012; Sancho et al., 2018). Chlorantraniliprole significantly decreased the pupation proportion at 12.5% MRFR (NOER ¼ 7.5 g a.i. ha1), adult emergence at 25% MRFR (MRFR ¼ 15 g a.i. ha1) and egg hatchability at 50% MRFR (MRFR ¼ 30 g a.i. ha1) of C. septempunctata. This is consistent with Yu et al. (2014b), who demonstrated that the pupation of C. septempunctata significantly decreased following application of hexaflumuron at the NOER of 3.04 g a.i. ha1. Wang et al. (2014)

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reported that nitenpyram, applied at the label rate, significantly reduced the adult emergence rate of Harmonia axyridis. However, Jiang et al. (2018b) reported that nitenpyram did not affect the pupation, adult emergence or egg hatchability of C. septempunctata. This agrees with Yu et al. (2014a), who also reported that imidacloprid, at sublethal doses, did not affect the pupation or adult emergence of C. septempunctata (NOER > 13.66 g a.i. ha1). The variability in these findings may result from testing insecticides with different modes of action and using different predator species (He et al., 2018). The total effect (E) can be used to assess the toxic effects of different treatments/doses of a pesticide (Wang et al., 2014). We found that chlorantraniliprole can be classified as harmless (IOBC class I) to C. septempunctata at the 12.5% label rate of 7.5 g a.i. ha1. Even at 200% (120 g a.i. ha1) the label rate, chlorantraniliprole was shown to be only slightly harmful (IOBC class II). These results suggest that chlorantraniliprole is suitable for use in IPM systems. However, chlorantraniliprole at/above the 50% label rate of 30 g a.i. ha1 dramatically reduced the fecundity and fertility of C. septempunctata when 2nd instar larvae were treated (NOER ¼ g a.i. ha1). The fecundity of H. axyridis was also significantly decreased after the 2nd instar larvae were treated with sublethal doses of chlorantraniliprole (Nawaz et al., 2017). These results are consistent with studies showing that neonicotinoid insecticides including thiamethoxam (Rahmani and Bandani, 2013), clothianidin (Jiang et al., 2018a), acetamiprid (Fogel et al., 2013), and imidacloprid (Fernandes et al., 2016) can lower the fecundity and fertility of coccinellid predators. Nevertheless, Fernandes et al. (2016) demonstrated that chlorantraniliprole did not affect the fecundity and fertility of three beneficial insects (Cycloneda sanguinea, Orius insidiosus, and Chauliognathus flavipes) when adults were exposed to an LC20 dose of the insecticide. However, chlorantraniliprole may cause a decline in reproduction of C. septempunctata at higher label rates. Population parameters, including the net reproductive rate (R0), intrinsic rate of increase (r), finite rate of increase (l), and mean generation time (T) can provide useful information about insect population dynamics (Liu et al., 2017; Zheng et al., 2017). Although apparently only slightly harmful to larvae, chlorantraniliprole at 100 and 200% MRFR (60 and 120 g a.i. ha1) reduced the R0, r, l, and T of C. septempunctata. The reduction of demographic parameters is directly related to the reduction of fecundity, fertility and longevity (He et al., 2018; Jiang et al., 2018a). Overuse of chlorantraniliprole in agricultural systems can disturb population growth and the biological control provided by C. septempunctata. Our results demonstrated that chlorantraniliprole at 100% and 200% of the label rate (60 and 120 g a.i. ha1) may adversely affect C. septempunctata population levels and reduce its effectiveness as a biological control agent. More studies should be performed to assess the compatibility of chlorantraniliprole with the predator C. septempunctata under semi-field and field conditions. 5. Conclusions We found that chlorantraniliprole applied at a field label rate (<120 g a.i. ha1) is harmless and/or slightly toxic to C. septempunctata larvae (IOBC class I and II). Acute toxicity tests suggest that chlorantraniliprole is compatible with C. septempunctata (HQ < 2). However, there were serious effects on subsequent growth and development, which led to reduced rates of survival, pupation, adult emergence, fecundity, and egg hatch and increased the proportions of offspring deformities. The duration of larval stages, pupae, adult, APOP, and TPOP, and the entire generation of C. septempunctata were significantly affected when 2nd instar larvae were exposed to chlorantraniliprole at higher field

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label rates. Excessive use of chlorantraniliprole may also reduce population parameters such as r, R0, l, and T. These results demonstrate that the use of chlorantraniliprole at higher field label rates may reduce predator populations and decrease the level of biological control provided by C. septempunctata. Conflicts of interest We declare no competing interests in conducting this manuscript. Acknowledgments This study was supported by the National Key R & D Program of China (2018YFD0200604), Modern Agricultural Industrial Technology System Program of Shandong (SDAIT-02-10), Shandong “Double First-Class” Awards Program (SYL2017-XTTD11), and Funds of Shandong “Double Tops” Program (SYL2017-YSTD02). We thank Dr. Hsin Chi (National Chung Hsing University, Taiwan, Republic of China) for their technical guidance and statistical assistance with the two-sex life table theory. We thank LetPub (www. letpub.com) for linguistic assistance during manuscript preparation. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.chemosphere.2019.03.025. References Abbott, W.S., 1925. A method of computing the effectiveness of an insecticide. J. Econ. Entomol. 18, 265e267. Angeli, G., Forti, D., Maines, R., 2000. Side-effects of eleven insect growth regulators on the predatory bug Orius laevigatus Fieber (Heteroptera: anthocoridae). Bulletin Oilb/srop 85e92. Barbosa, P., Oliveira, M.D., Barros, E.M., Michaud, J.P., Torres, J.B., 2017. Differential impacts of six insecticides on a mealybug and its coccinellid predator. Ecotoxicol. Environ. Saf. 147, 963e971. Bianchi, F.J.J.A., Werf, W.V.D., 2004. Model evaluation of the function of prey in noncrop habitats for biological control by ladybeetles in agricultural landscapes. Ecol. Model. 171, 177e193. Brugger, K.E., Cole, P.G., Newman, I.C., Parker, N., Scholz, B., Suvagia, P., Graham, P., Walker, G., Hammond, T.G., 2010. Selectivity of chlorantraniliprole to parasitoid wasps. Pest Manag. Sci. 66, 1075e1081. Candolfi, M., Barrett, K., Campbell, P., Forster, R., Grandy, N., Huet, M., Lewis, G., Oomen, P., Schmuck, R., Vogt, H., 2001. Guidance Document on Regulatory Testing and Risk Assessment Procedures for Plant Protection Products with Non-target Arthropods, from the ESCORT 2 Workshop SETAC. Pensacola. Chi, H., 1988. Life-table analysis incorporating both sexes and variable development rates among individuals. Environ. Entomol. 17, 26e34. Chi, H., Getz, W.M., 1988. Mass rearing and harvesting based on an age-stage, twosex life table: a potato tuberworm (Lepidoptera: Gelechiidae) case study. Environ. Entomol. 17, 18e25. Cloyd, R.A., Bethke, J.A., 2011. Impact of neonicotinoid insecticides on natural enemies in greenhouse and interiorscape environments. Pest Manag. Sci. 67, 3e9. Cui, F., Chai, T., Qian, L., Wang, C., 2016. Effects of three diamides (chlorantraniliprole, cyantraniliprole and flubendiamide) on life history, embryonic development and oxidative stress biomarkers of Daphnia magna. Chemosphere 169, 107e116. Desneux, N., Decourtye, A., Delpuech, J.M., 2007. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52, 81e106. Fernandes, M.E.S., Alves, F.M., Pereira, R.C., Aquino, L.A., Fernandes, F.L., Zanuncio, J.C., 2016. Lethal and sublethal effects of seven insecticides on three beneficial insects in laboratory assays and field trials. Chemosphere 156, 45e55. lez, B., Ronco, A.E., 2013. Impact of Fogel, M.N., Schneider, M.I., Desneux, N., Gonza the neonicotinoid acetamiprid on immature stages of the predator Eriopis connexa (Coleoptera: Coccinellidae). Ecotoxicology 22, 1063e1071. Fogel, M.N., Schneider, M.I., Rimoldi, F., Ladux, L.S., Desneux, N., Ronco, A.E., 2016. Toxicity assessment of four insecticides with different modes of action on pupae and adults of Eriopis connexa (Coleoptera: Coccinellidae), a relevant predator of the neotropical region. Environ. Sci. Pollut. Res. 23, 14918e14926. Galvan, T.L., Koch, R.L., Hutchison, W.D., 2005a. Effects of spinosad and indoxacarb on survival, development, and reproduction of the multicolored asian lady beetle (Coleoptera: Coccinellidae). Biol. Control 34, 108e114.

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