Translator Disclaimer
10 July 2020 Susceptibility of First Instar Hippodamia convergens (Coleoptera: Coccinellidae) and Chrysoperla rufilabris (Neuroptera: Chrysopidae) to the Insecticide Sulfoxaflor
Author Affiliations +
Abstract

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), continues to be the most economically important arthropod pest of soybean in the Midwest. Currently, management tactics for A. glycines rely on scouting and application of broad-spectrum insecticides. However, broad-spectrum insecticides are toxic to most natural enemies of this aphid. Selective insecticides may provide an alternative strategy for suppressing A. glycines populations while conserving populations of its natural enemies. Therefore, the aim of this study was to evaluate the potential lethal and sublethal effects of sulfoxaflor (a relatively new selective insecticide), to 2 of this pest's natural enemies, Chrysoperla rufilabris (Burmeister) (Neuroptera: Chrysopidae) and Hippodamia convergens Guérin-Méneville (Coleoptera: Coccinellidae). Laboratory bioassays were performed on first instars of both predators with residual toxicity evaluated over time until adult emergence. Parameters evaluated were mortality and developmental time for larvae and pupae, and adult body size. Fecundity also was determined for C. rufilabris. We found that sulfoxaflor was not toxic to first instar C. rufilabris. However, developmental time to adult was significantly delayed after exposure to this insecticide, but fecundity and body size were not negatively affected. For H. convergens, sulfoxaflor at 25% of the field rate was toxic to first instars. No significant differences were found with regard to developmental time and body size. It is important to note that sulfoxaflor, though relatively less toxic than some insecticides, is not entirely without consequence if natural enemies are exposed. The present study emphasizes the importance of examining earlier life stages and potential sublethal effects when evaluating the toxicity of insecticides in the presence of natural enemies.

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), first detected in North America in 2000, continues to be the most economically important arthropod pest of soybean, Glycine max (L.) Merrill (Fabaceae), in the Midwest (Ragsdale et al. 2011; Hurley & Mitchell 2017). Large infestations of A. glycines can significantly reduce photosynthetic rates of infested soybean leaflets by 50% (Macedo et al. 2003), and negatively impact yield components (i.e., seed size, seeds per pod, and pods per plant) (Beckendorf et al. 2008) that cause up to 40% yield loss (Ragsdale et al. 2007). Currently, management tactics for A. glycines rely on scouting and application of broad-spectrum insecticides based on an established economic threshold and economic injury level (Ragsdale et al. 2007; Hodgson et al. 2012; Koch et al. 2016). Since the introduction of A. glycines in North America, the amount of soybean acreage treated with insecticides in the Midwest increased from < 0.1% in 2000 to > 13% in 2006 (Ragsdale et al. 2011). Non-chemical tactics for managing A. glycines, such as host plant resistance (Hill et al. 2004; Hesler et al. 2013; Hanson & Koch 2018) and biological control (Heimpel et al. 2004), are promising complementary tactics for improving current integrated pest management (IPM) programs for this pest.

Natural enemies have been shown to play a role in suppressing and preventing outbreaks of A. glycines (Costamagna et al. 2008; Ragsdale et al. 2011; Koch & Costamagna 2017). In North America, there are over 40 species of predators and parasitoids associated with this pest (Rutledge et al. 2004). Costamagna and Landis (2006) showed that natural enemies significantly reduced population growth and establishment of A. glycines in several production systems. Additionally, Fox et al. (2005) found that generalist predators reduced overall survival of this aphid during a 24-h period in 50% of field cage trials performed. Insecticides commonly used for A. glycines management (i.e., organophosphates and pyrethroids) (Hodgson et al. 2012) may have lethal and sublethal impacts on beneficial arthropods (Desneux et al. 2007; Seagraves & Lundgren 2012; Guedes et al. 2016). Selective insecticides may provide an alternative for suppressing A. glycines populations, while conserving populations of natural enemies (Weinzierl 2009). Integrated pest management programs can be improved with the combination of selective insecticides and biological control agents (Garzón et al. 2015). Previous studies have evaluated the potential role of selective insecticides in A. glycines management programs (Ohnesorg et al. 2009; Bahlai et al. 2010; Frewin et al. 2012; Varenhorst & O'Neal 2012; Pezzini & Koch 2015; Tran et al. 2016; Koch et al. 2019). However, it has been shown that some selective insecticides may not be entirely benign to natural enemies (Bahlai et al. 2010; Gentz et al. 2010; Biondi et al. 2012a). Understanding the impacts of insecticides, including sublethal effects, to beneficial arthropods is essential for an integrated pest management program. Sublethal effects are defined as deleterious physiological or behavioral effects on individuals that survive an exposure to a pesticide (Desneux et al. 2007). Previous authors have reported that population dynamics and other reproductive and behavioral traits (e.g., developmental rate, fecundity, fertility, longevity, sex ratio, feeding, and oviposition) of beneficial arthropods may be adversely affected by sublethal concentrations of pesticides (Stark & Banks 2003; Desneux et al. 2007; Biondi et al. 2012b; Cloyd 2012; Moscardini et al. 2013; Guedes et al. 2016).

Sulfoxaflor is in the sulfoximine class of insecticides and is a potential selective chemical tool for management of A. glycines (Knodel et al. 2016; Tran et al. 2016). The specific activity of sulfoxaflor on the insect nicotinic acetylcholine receptor (nAChR) is novel and structurally different from neonicotinoids (Babcock et al. 2011; Zhu et al. 2011; Sparks et al. 2013). This factor has resulted in sulfoxamines being classified as Group 4C by the Insecticide Resistance Action Committee (IRAC 2018). Sulfoxaflor is effective against a wide range of sap-feeding insects, such as the rice brown planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae) (Ghosh et al. 2013); plant bugs, Lygus hesperus Knight (Joseph & Bolda 2016) and Lygus lineolaris (Palisot de Beauvois) (Hemiptera: Miridae) (Siebert et al. 2012); whiteflies, Bemisia tabaci (Gennadius) and Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) (Longhurst et al. 2013); and aphids, Myzus persicae (Sulzer) (Hemiptera: Aphididae) (Zhu et al. 2011); as well as A. glycines (Hemiptera: Aphididae) (Tran et al. 2016). The high efficacy of this insecticide to control sap-feeding insect pests, reduced toxicity to natural enemies, and the lack of cross-resistance with some insecticides (Babcock et al. 2011; Longhurst et al. 2013, Sparks et al. 2013; Tran et al. 2016; Liao et al. 2019), suggests that sulfoxaflor may provide an effective alternative for integrated pest management and insecticide resistance management programs for pests such as A. glycines.

However, the lethal and sublethal impacts of sulfoxaflor on natural enemies are not fully understood. Potential impacts of sulfoxaflor on natural enemies appear to depend on the concentration of the insecticide and the species of natural enemy used in the study. For example, Pan et al. (2017) reported that sulfoxaflor had a negative impact on the growth, feeding, and behavior of the red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae). In addition, Garzón et al. (2015) showed that sulfoxaflor was highly toxic to the late instar larvae of Adalia bipunctata (L.) (Coleoptera: Coccinellidae). However, when compared with broad-spectrum insecticides, sulfoxaflor was less impactful to key predators of A. glycines (Tran et al. 2016). These studies generally have not examined impacts of sulfoxaflor to first instars of natural enemies, which are often the most susceptible life stage (Kraiss & Cullen 2008; Pezzini & Koch 2015; Prabhaker et al. 2017).

Therefore, to improve the integration of chemical and biological control for A. glycines, further understanding is needed of the potential lethal and sublethal effects of sulfoxaflor on natural enemies. The objective of this study was to investigate the potential lethal and sublethal effects of sulfoxaflor after exposure of early instars of 2 representative natural enemies, Chrysoperla rufilabris (Burmeister) (Neuroptera: Chrysopidae) and Hippodamia convergens Guérin-Méneville (Coleoptera: Coccinellidae), under laboratory conditions.

Materials and Methods

CHRYSOPERLA RUFILABRIS

Laboratory bioassays were performed on first instar C. rufilabris and H. convergens at the University of Minnesota, St. Paul, Minnesota, USA. Chrysoperla rufilabris eggs were purchased from Beneficial Insectary (Redding, California, USA) and shipped overnight. Upon arrival, eggs were removed from the original packaging and transferred into individual 60 × 15-mm plastic Petri dishes. Chrysoperla rufilabris eggs were allowed to develop into 2- to 3-d-old larvae in a growth chamber at 25 °C, 75% RH, and a photoperiod of 16:8 h (L:D).

To evaluate insecticide residual toxicity to first instar C. rufilabris, a randomized complete block design experiment was used with 3 treatments and 4 replications, with 15 individuals per replication. Treatments consisted of sulfoxaflor (34.8 g a.i. per ha, Transform, Corteva Agriscience, Wilmington, Delaware, USA) (i.e., high end of range of labeled field rates); λ-cyhalothrin (29.1 g a.i. per ha, Warrior II, Syngenta Crop Protection Inc., Basel, Switzerland); and an untreated check. The bioassay methodology was similar to the laboratory bioassay performed by Tran et al. (2016). Treatments were applied to the interior of 60 × 15-mm plastic Petri dishes. After application, dishes were allowed to dry for 1 h and the 2- to 3-d-old first instars of C. rufilabris were transferred to treated Petri dishes. Larvae were maintained in the treated dishes for 24 h. After 24 h, C. rufilabris larvae were transferred to untreated Petri dishes. Larvae were maintained in a growth chamber under the conditions previously described, and provided with water-moistened florist foam and Ephestia kuehniella (Zeller) (Lepidoptera: Pyralidae) eggs ad libitum as food source until larvae reached the pupal stage. Prior to transferring the larvae into untreated Petri dishes, the exterior surfaces of the dishes were wiped with a cloth sprayed with Static Guard (B&G Foods Inc., Parsippany, New Jersey, USA) to prevent static electricity from interfering with larval transfer and food placement (Amarasekare & Shearer 2013). Chrysoperla rufilabris larval mortality was monitored daily and defined as the immobility of the larvae upon stimulation with a fine camel-hair brush. For pupae, mortality was defined as the inability to molt to the next life stage. Developmental time for each life stage was recorded.

Adult C. rufilabris that emerged successfully from the pupal stage were transferred to clean Petri dishes, and provisioned with honey and water-moistened floral foam. Honey was used to provision adult C. rufilabris, because artificial diets can affect female fecundity (Hagen 1950; Sundby 1967). Petri dishes were cleaned every other d to prevent mold growth. After 10 d, surviving adults were placed into the freezer at approximately –20 °C. Adult wing lengths were recorded from the base axillary sclerite to the apex of the wing using a dissecting scope and Leica Application Suite software (Version 4.0.0, Leica Microsystems Inc., Buffalo Grove, Illinois, USA). The adults were sexed and dissected in Dulbecco's Phosphate Buffered Saline 1X (DPBS) with calcium and magnesium solution (Meditech Inc., Manassas, Virginia, USA) to record sex and fecundity (i.e., number of eggs in ovaries) of females.

HIPPODAMIA CONVERGENS

Hippodamia convergens adults were purchased from Arbico Organics (Oro Valley, Arizona, USA) and shipped overnight. Upon arrival, approximately 20 pairs of adults were separated into individual 60 × 15-mm Petri dishes for mating, and were maintained in a growth chamber at 25 °C, 55% RH, and a photoperiod of 16:8 h (L:D). Live A. glycines on soybean leaves were provisioned ad libitum as a food source, and water was provisioned through moistened florist foam. Aphis glycines and water were replenished every 48 h or as needed. A filter paper disc also was placed inside each Petri dish to absorb excess humidity, and was replaced if mold was present. After a 7-d mating period, 20 female adult H. convergens were separated into individual 60 × 15-mm plastic Petri dishes with food and water as described above. Eggs deposited by females were collected by transferring the females to clean Petri dishes and maintaining the eggs in the previous dishes. Eggs remained in the dishes under conditions described above, and were reared to 2- to 3-d-old first instars.

To evaluate insecticide residual toxicity to first instar H. convergens, a randomized complete block design experiment was performed with 3 treatments and 3 replications with 10 individuals per replication. Preliminary experiments conducted with a field rate (i.e., low end of range of labeled field rates) and 50% field rate of sulfoxaflor (Transform, 25.8 g a.i. per ha and 12.9 g a.i per ha, respectively) resulted in high rates of mortality of first instar H. convergens. Therefore, sulfoxaflor concentrations were reduced for this experiment. Treatments were 10% field rate of sulfoxaflor (2.6 g a.i. per ha); 25% field rate of sulfoxaflor (6.4 g a.i. per ha); and an untreated check. Methodology for treating dishes and performing the bioassays was the same as described for C. rufilabris experiment. However, during the 24-h exposure period to treatments, approximately 0.2 to 0.3 g of frozen E. kuehniella eggs were placed inside each treated dish to reduce mortality due to starvation.

Hippodamia convergens larvae were maintained in a growth chamber under the conditions described earlier, and provided with water-moistened florist foam and E. kuehniella eggs ad libitum as a food source until larvae reached the adult stage. Hippodamia convergens larval mortality was monitored daily, and developmental time for each life stage was recorded as described above. Newly emerged adults (1-d-old) were placed in a freezer at a temperature of –20 °C for future measurements. Individuals were sexed based on the shape of the terminal abdominal segment (Heimpel & Lundgren 2000), and body weight was measured using an analytical balance (Sartorius Entris® 224, Sartorius AG, Göttingen, Germany). Elytral lengths and pronotal widths were measured using a dissecting scope and Leica Application Suite software (Version 4.0.0, Leica Microsystems Inc., Buffalo Grove, Illinois, USA).

STATISTICAL ANALYSES

Data were analyzed using R version 3.5.2 (R Core Team 2018) and RStudio Desktop version 1.1.463 (RStudio Team 2018). The effect of treatments on mortality of H. convergens and C. rufilabris were subjected to a bias-reduced generalized linear model (package: ‘brglm2') (Kosmidis 2018) with a binomial response variable (i.e., 1 = alive, 0 = dead). Separate linear mixed-effect models (package: ‘lme4') (Bates et al. 2015) were used to test the fixed effect of pesticide treatment on developmental time and fecundity with a random effect for replication. Separate linear mixed-effect models were used to test the fixed effects of pesticide treatment, sex, and their interaction on body weight, pronotal width, elytral length, and wing length, with a random effect for replication. Random effects accounted for location differences in blocking of treatments within growth chambers. Non-significant (P > 0.05) interactions were removed from the models. Responses were analyzed on non-transformed scales, except development times for C. rufilabris were square-root transformed for analyses. Means were separated using Tukey's honestly significant difference (HSD) test at α = 0.05.

Results

CHRYSOPERLA RUFILABRIS

Proportion mortality of C. rufilabris was significantly affected after individuals were treated in the first instar. In particular, treatment with λ-cyhalothrin significantly increased mortality during the first instar compared with the control and sulfoxaflor (χ2 = 54.33; df = 2; P < 0.001) (Fig. 1A). In addition, total proportion mortality (i.e., from first instar to adult) was significantly increased by λ-cyhalothrin compared to the control and sulfoxaflor (χ2 = 33.56; df = 2; P < 0.001) (Fig. 1A). No significant differences in mortality were found among treatments for the remaining life stages (second instar: χ2 = 9.11; df = 2; P = 0.01; third instar: χ2 = 0.19; df = 2; P = 0.91; and pupa: χ2 = 1.52; df = 2; P = 0.46) (Fig. 1A).

Development time of C. rufilabris was significantly affected after individuals were treated in the first instar. In particular, λ-cyhalothrin and sulfoxaflor increased development time of the first instar (χ2 = 72.51; df = 2; P < 0.001) and total (i.e., first instar to adult) (χ2 = 112.92; df = 2; P < 0.001) (Fig. 1B). In addition, λ-cyhalothrin increased development time of the second instar (χ2 = 13.54; df = 2; P = 0.001) (Fig. 1B). No significant differences were found for development times of the third instar (χ2 = 4.36; df = 2; P = 0.11) or pupa (χ2 = 0.78; df = 2; P = 0.67) (Fig. 1B).

Mean (± SEM) fecundity (i.e., number of eggs in ovaries) of C. rufilabris females ranged from 2.92 ± 1.26 to 4.38 ± 1.25 among treatments, but did not differ significantly (χ2 = 0.9; df = 2; P = 0.63). Mean wing length of females (12.65 ± 0.16 mm) was greater than that of males (11.72 ± 0.17 mm) (χ2 = 35.49; df = 1; P < 0.001). However, the effect of treatment on adult wing length was not significant (χ2 = 4.80; df = 2; P = 0.9).

HIPPODAMIA CONVERGENS

The 25% field rate of sulfoxaflor significantly increased H. convergens mortality during the first instar (χ2 = 24.29; df = 2; P < 0.001) and total mortality from first instar to adult (χ2 = 20.34; df = 2; P < 0.001) compared with the control and 10% sulfoxaflor field rate (Fig. 2A). No significant differences were found for the remaining life stages where mortality occurred (second instar: χ2 = 0.33; df = 2; P = 0.84; pupa: χ2 = 0.10; df = 2; P = 0.94) (Fig. 2A).

No significant differences were found among treatments for developmental time of H. convergens for all life stages (first instar: χ2 = 1.05; df = 2; P = 0.58; second instar: χ2 = 1.45; df = 2; P = 1.48; third instar: χ2 = 1.10; df = 2; P = 0.57; fourth instar: χ2 = 0.01; df = 2; P = 0.99; pupa: χ2 = 0.99; df = 2; P = 0.6; and total: χ2 = 0.95; df = 2; P = 0.62) (Fig. 2B). Mean body weight of females (15.10 ± 0.36 mg) was greater than males (13.25 ± 0.37 mg) (χ2 = 25.52; df = 1; P < 0.001). However, the effects of treatment on body weight were not significant (χ2 = 0.90; df = 2; P = 0.63). Mean pronotum width and elytra length of females (2.36 ± 0.02 mm and 4.49 ± 0.05 mm, respectively) were greater than males (2.25 ± 0.02 mm and 4.17 ± 0.05 mm, respectively) (pronotum width: χ2 = 26.20; df = 1; P < 0.001; elytra length: χ2 = 37.30; df = 1; P < 0.001). But the effect of treatment on body size was not significant (pronotum width: χ2 = 1.20; df = 2; P = 0.54; elytra length: χ2 = 0.47; df = 2; P = 0.78).

Fig. 1.

Proportion of mortality (A) and developmental time (B) of Chrysoperla rufilabris life stages after exposure of first instars to dried insecticide residues. After exposure, individuals were reared to adults (L1, L2, and L3 represent first, second, and third instars, respectively, and total represents first instar to adult). Within life stages, treatment means with the same letter are not significantly different (Tukey HSD, P > 0.05). Asterisks (*) indicate zeros.

img-z4-1_191.jpg

Discussion

Our study provides the first examination of the potential lethal and sublethal effects of sulfoxaflor to first instars of C. rufilibris and H. convergens. Sulfoxaflor had distinct effects to both predators. Although mortality was increased by reduced rates of sulfoxaflor applied to H. convergens, a field rate of this insecticide proved to be non-toxic to C. rufilabris. Our results for H. convergens are in contrast to those of Tran et al. (2016), Colares et al. (2017), and Prabhaker et al. (2017). However, these authors used later life stages than those used in our study, which may have contributed to the higher rates of mortality reported in the present study. The greater susceptibility of larvae in early instars could be partially explained by their smaller size, presence of a more permeable cuticle, or lower enzymatic detoxifying processes (Stark et al. 2004; Fogel et al. 2013). In addition, under field conditions, the lower mobility of immatures compared to adults, which can fly and potentially avoid insecticidal contact, could further contribute to differences in pesticide susceptibility among life stages (Medina et al. 2004; Garzón et al. 2015). However, when C. rufilabris and H. convergens were exposed to the insecticide treatments as first instars, lethal and sublethal effects were generally limited to that stage and their total development from first instar to adult.

Fig. 2.

Proportion of mortality (A) and developmental time (B) of Hippodamia convergens life stages after exposure of first instars to dried insecticide residues. After exposure, individuals were reared to adults (L1, L2, L3, and L4 represent first, second, third, and fourth instars, respectively, and total represents first instar to adult). Within life stages, treatment means with the same letter are not significantly different (Tukey HSD, P > 0.05). FR = field rate of insecticide. Asterisks (*) indicate zeros.

img-z4-6_191.jpg

As stated earlier, exposure of C. rufilabris to a field rate of sulfoxaflor in the first instar did not affect mortality but did cause an intermediate increase in developmental time compared with the control and λ-cyhalothrin. In a residual toxicity experiment, Tran et al. (2016) found that sulfoxaflor was harmless to third instars of C. rufilabris. Similar results were found by Garzón et al. (2015), where sulfoxaflor was found to be harmless to the third instars of Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). Additionally, sulfoxaflor had no toxicity when first instars of C. carnea were exposed via residues on treated leaves (Barbosa et al. 2017). However, larvae of C. carnea had slower developmental time compared with the control when ingesting food contaminated with sulfoxaflor (Barbosa et al. 2017). The generally lower susceptibility of C. rufilabris to these insecticides compared with H. convergens may have been due to generally higher esterase activity in Chrysopidae (Ishaayn & Casida 1981).

Moreover, exposure of H. convergens to reduced rates of sulfoxaflor in the first instar affected mortality at the 25% field rate, but not the 10% field rate. In addition, these rates did not affect development time at any life stage or total development time. Lower rates of sulfoxaflor were used in this study because of the high mortality found for first instars at a full field rate. Similarly, a field rate of sulfoxaflor was highly toxic to second instar H. convergens exposed to residues on treated leaves (Colares et al. 2017). In addition, sulfoxaflor was highly toxic to fourth instars of A. bipunctata (Garzón et al. 2015). The greater insecticide tolerance of H. convergens adults compared to larvae is consistent with results for other coccinellids (Galvan et al. 2005; Jalali et al. 2009; Fogel et al. 2013), and may be due to some of the factors described above.

Sulfoxaflor holds promise for improved integration of chemical and biological controls of A. glycines and other piercing-sucking pests. Consistent with other studies, some sublethal effects on development time for both predators were found, but none on size or reproductive potential (Garzón et al. 2015; Colares et al. 2017). Therefore, when developing integrated pest management programs it is important to note that the use of sulfoxaflor is not entirely without consequence to natural enemies. The present study emphasizes the importance of examining earlier life stages and potential sublethal effects when evaluating compatibility of insecticides with natural enemies. Additional research should examine the potential consequences of these lethal and sublethal effects on the effectiveness of biological control offered by these predators.

Acknowledgments

Funding was provided by the Minnesota Soybean Research & Promotion Council. We are thankful for assistance provided by laboratory staff.

References Cited

1.

Amarasekare KG, Shearer PW. 2013. Comparing effects of insecticides on two green lacewings species, Chrysoperla johnsoni and Chrysoperla carnea (Neuroptera: Chrysopidae). Journal of Economic Entomology 106: 1126–1133. Google Scholar

2.

Babcock JM, Gerwick CB, Huang JX, Loso MR, Nakamura G, Nolting SP, Rogers RB, Sparks TC, Thomas J, Watson GB, Zhu Y. 2011. Biological characterization of sulfoxaflor, a novel insecticide. Pest Management Science 67: 328–334. Google Scholar

3.

Bahlai CA, Xue Y, McCreary CM, Schaafsma AW, Hallett RH. 2010. Choosing organic pesticides over synthetic pesticides may not effectively mitigate environmental risk in soybeans. PLoS ONE 5: e11250. https://doi.org/10.1371/journal.pone.0011250 Google Scholar

4.

Barbosa PRR, Michaud JP, Bain CL, Torres JB. 2017. Toxicity of three aphicides to the generalist predators Chrysoperla carnea (Neuroptera: Chrysopidae) and Orius insidiosus (Hemiptera: Anthocoridae). Ecotoxicology 26: 589–599. Google Scholar

5.

Bates D, Mäechler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistics Software 67: 1–48. Google Scholar

6.

Beckendorf EA, Catangui MA, Riedell WE. 2008. Soybean aphid feeding injury and soybean yield, yield components, and seed composition. Agronomy Journal 100: 237–246. Google Scholar

7.

Biondi A, Desneux N, Siscaro G, Zappalà L. 2012a. Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere 87: 803–812. Google Scholar

8.

Biondi A, Mommaerts V, Smagghe G, Viñuela E, Zappalà L, Desneux N. 2012b. The non-target impact of spinosyns on beneficial arthropods. Pest Management Science 68: 1523–1536. Google Scholar

9.

Cloyd R. 2012. Indirect effects of pesticides on natural enemies, pp. 127–150 In Soundararajan RP [ed.], Pesticides - Advances in Chemical and Botanical Pesticides. Intech, Rijeka, Croatia. Google Scholar

10.

Colares F, Michaud JP, Bain CL, Torres JB. 2017. Relative toxicity of two aphicides to Hippodamia convergens (Coleoptera: Coccinellidae): implications for integrated management of sugarcane aphid, Melanaphis sacchari (Hemiptera: Aphididae). Journal of Economic Entomology 110: 52–58. Google Scholar

11.

Costamagna AC, Landis DA. 2006. Predators exert top-down control of soybean aphid across a gradient of agricultural management systems. Ecological Applications 16: 1619–1628. Google Scholar

12.

Costamagna AC, Landis DA, Brewer MJ. 2008. The role of natural enemy guilds in Aphis glycines suppression. Biological Control 45: 368–379. Google Scholar

13.

Desneux N, Decourtye A, Delpuech JM. 2007. The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology 52: 81–106. Google Scholar

14.

Fogel MN, Schneider MI, Desneux N, González B, Ronco AE. 2013. Impact of the neonicotinoid acetamiprid on immature stages of the predator Eriopis connexa (Coleoptera: Coccinellidae). Ecotoxicology 22: 1063–1071. Google Scholar

15.

Fox TB, Landis DA, Cardoso FF, Difonzo CD. 2005. Impact of predation on establishment of the soybean aphid, Aphis glycines in soybean, Glycine max. BioControl 50: 545–563. Google Scholar

16.

Frewin AJ, Schaafsma AW, Hallett RH. 2012. Susceptibility of Aphelinus certus to foliar-applied insecticides currently or potentially registered for soybean aphid control. Pest Management Science 68: 202–208. Google Scholar

17.

Galvan TL, Koch RL, Hutchison WD. 2005. Toxicity of commonly used insecticides in sweet corn and soybean to multicolored Asian lady beetle (Coleoptera: Coccinellidae). Journal of Economic Entomology 98: 780–789. Google Scholar

18.

Garzón A, Medina P, Amor F, Viñuela E, Budia F. 2015. Toxicity and sublethal effects of six insecticides to last instar larvae and adults of the biocontrol agents Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) and Adalia bipunctata (L.) (Coleoptera: Coccinellidae). Chemosphere 132: 87–93. Google Scholar

19.

Gentz MC, Murdoch G, King GF. 2010. Tandem use of selective insecticides and natural enemies for effective, reduced-risk pest management. Biological Control 52: 208–215. Google Scholar

20.

Ghosh A, Das A, Samanta A, Chatterjee ML, Roy A. 2013. Sulfoximine: a novel insecticide for management of rice brown planthopper in India. African Journal of Agricultural Research 8: 4798–4803. Google Scholar

21.

Guedes RNC, Smagghe G, Stark JD, Desneux N. 2016. Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annual Review of Entomology 61: 43–62. Google Scholar

22.

Hagen KS. 1950. Fecundity of Chrysopa californica as affected by synthetic food. Journal of Economic Entomology 43: 101–104. Google Scholar

23.

Hanson AA, Koch RL. 2018. Interactions of host-plant resistance and foliar insecticides for soybean aphid management. Crop Protection 112: 232–238. Google Scholar

24.

Heimpel GE, Lundgren JG. 2000. Sex ratios of commercially reared biological control agents. Biological Control 19: 77–93. Google Scholar

25.

Heimpel GE, Ragsdale DW, Venette R, Hopper KR, O'Neil RJ, Rutledge CE, Wu Z. 2004. Prospects for importation biological control of the soybean aphid: anticipating potential costs and benefits. Annals of the Entomological Society of America 97: 249–258. Google Scholar

26.

Hesler LS, Chiozza MV, O'Neal ME, MacIntosh GC, Tilmon KJ, Chandrasena DI, Tinsley NA, Cianzio SR, Costamagna AC, Cullen EM, DiFonzo CD, Potter BD, Ragsdale DW, Steffey K, Koehler KJ. 2013. Performance and prospects of Rag genes for management of soybean aphid. Entomologia Experimentalis et Applicata 147: 201–216. Google Scholar

27.

Hill CB, Li Y, Hartman GL. 2004. Resistance to the soybean aphid in soybean germplasm. Crop Science 44: 98–106. Google Scholar

28.

Hodgson EW, McCornack BP, Tilmon K, Knodel JJ. 2012. Management recommendations for soybean aphid (Hemiptera: Aphididae) in the United States. Journal of Integrated Pest Management 3: E1–E10. Google Scholar

29.

Hurley T, Mitchell P. 2017. Value of neonicotinoid seed treatments to US soybean farmers. Pest Management Science 73: 102–112. Google Scholar

30.

IRAC – Insecticide Resistance Action Committee. 2018. IRAC Mode of Action Classification Scheme.  http://www.irac-online.org/documents/moa-classification/ (last accessed 20 Jan 2020). Google Scholar

31.

Ishaaya I, Casida JE. 1981. Pyrethroid esterase(s) may contribute to natural pyrethroid tolerance of larvae of the common green lacewing. Environmental Entomology 10: 681–684. Google Scholar

32.

Jalali MA, Van Leeuwen T, Tirry L, De Clercq P. 2009. Toxicity of selected insecticides to the two-spot ladybird Adalia bipunctata. Phytoparasitica 37: 323–326. Google Scholar

33.

Joseph SV, Bolda M. 2016. Efficacy of insecticides against Lygus hesperus Knight (Hemiptera: Miridae) in the California's central coast strawberry. International Journal of Fruit Science 16: 178–187. Google Scholar

34.

Knodel JJ, Beauzay PB, Prasifka P. 2016. Efficacy of foliar-applied sulfoxaflor for control of soybean aphid and impact on lady beetles, 2015. Arthropod Management Tests 41: 1.  https://doi.org/10.1093/amt/tsw060 Google Scholar

35.

Koch RL, Costamagna AC. 2017. Reaping benefits from an invasive species: role of Harmonia axyridis in natural biological control of Aphis glycines in North America. BioControl 62: 331–340. Google Scholar

36.

Koch RL, da Silva Queiroz O, Aita RC, Hodgson EW, Potter BD, Nyoike T, Ellers-Kirk CD. 2019. Efficacy of afidopyropen against soybean aphid (Hemiptera: Aphididae) and toxicity to natural enemies. Pest Management Science 76: 375–383. Google Scholar

37.

Koch RL, Potter BD, Glogoza PA, Hodgson EW, Krupke CH, Tooker JF, DiFonzo CD, Michel AP, Tilmon KJ, Prochaska TJ, Knodel JJ, Wright RJ, Hunt TE, Jensen B, Varenhorst AJ, McCornack BP, Estes KA, Spencer JL. 2016. Biology and economics of recommendations for insecticide-based management of soybean aphid. Plant Health Progress 17: 265–269. Google Scholar

38.

Kosmidis I. 2018. Brglm2: Bias reduction in generalized linear models. R package version 0.1.6.  https://github.com/ikosmidis/brglm2  Google Scholar

39.

Kraiss H, Cullen EM. 2008. Efficacy and nontarget effects of reduced-risk insecticides on Aphis glycines (Hemiptera: Aphididae) and its biological control agent Harmonia axyridis (Coleoptera: Coccinellidae). Journal of Economic Entomology 101: 391–398. Google Scholar

40.

Liao X, Jin R, Zhang X, Ali E, Mao K, Xu P, Li J, Wan H. 2019. Characterization of sulfoxaflor resistance in the brown planthopper, Nilaparvata lugens (Stål). Pest Management Science 75: 1646–1654. Google Scholar

41.

Longhurst C, Babcock JM, Denholm I, Gorman K, Thomas JD, Sparks TC. 2013. Cross-resistance relationships of the sulfoximine insecticide sulfoxaflor with neonicotinoids and other insecticides in the whiteflies Bemisia tabaci and Trialeurodes vaporariorum. Pest Management Science 69: 809–813. Google Scholar

42.

Macedo TB, Bastos CS, Higley LG, Ostlie KR, Madhavan S. 2003. Photosynthetic responses of soybean to soybean aphid (Homoptera: Aphididae) injury. Journal of Economic Entomology 96: 188–193. Google Scholar

43.

Medina P, Budia F, Estal PD, Adán A, Viñuela E. 2004. Toxicity of fipronil to the predatory lacewing Chrysoperla carnea (Neuroptera: Chrysopidae). Biocontrol Science and Technology 14: 261–268. Google Scholar

44.

Moscardini VF, da Costa Gontijo P, Carvalho GA, Oliveira RL, Maia JB, Silva FF. 2013. Toxicity and sublethal effects of seven insecticides to eggs of the flower bug Orius insidiosus (Say) (Hemiptera: Anthocoridae). Chemosphere 92: 490–496. Google Scholar

45.

Ohnesorg WJ, Johnson KD, O'Neal ME. 2009. Impact of reduced-risk insecticides on soybean aphid and associated natural enemies. Journal of Economic Entomology 102: 1816–1826. Google Scholar

46.

Pan F, Lu Y, Wang L. 2017. Toxicity and sublethal effects of sulfoxaflor on the red imported fire ant, Solenopsis invicta. Ecotoxicology and Environmental Safety 139: 377–383. Google Scholar

47.

Pezzini DT, Koch RL. 2015. Compatibility of flonicamid and a formulated mixture of pyrethrins and azadirachtin with predators for soybean aphid (Hemiptera: Aphididae) management. Biocontrol Science and Technology 25: 1024–1035. Google Scholar

48.

Prabhaker N, Naranjo S, Perring T, Castle S. 2017. Comparative toxicities of newer and conventional insecticides: against four generalist predator species. Journal of Economic Entomology 110: 2630–2636. Google Scholar

49.

Ragsdale DW, Landis DA, Brodeur J, Heimpel GE, Desneux N. 2011. Ecology and management of the soybean aphid in North America. Annual Review of Entomology 56: 375–399. Google Scholar

50.

Ragsdale DW, McCornack BP, Venette RC, Potter BD, Macrae IV, Hodgson EW, O'Neal ME, Johnson KD, O'Neil RJ, Difonzo CD, Hunt TE, Glogoza PA, Cullen EM. 2007. Economic threshold for soybean aphid (Hemiptera: Aphididae). Journal of Economic Entomology 100: 1258–1267. Google Scholar

51.

R Core Team. 2018. R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria.  https://www.Rproject.org/ (last accessed 20 Jan 2020). Google Scholar

52.

RStudio Team. 2018. RStudio: integrated development for R. RStudio, Inc., Boston, Massachusetts, USA.  http://www.rstudio.com/ (last accessed 20 Jan 2020). Google Scholar

53.

Rutledge CE, O'Neil RJ, Fox TB, Landis DA. 2004. Soybean aphid predators and their use in integrated pest management. Annals of the Entomological Society of America 97: 240–248. Google Scholar

54.

Seagraves MP, Lundgren JG. 2012. Effects of neonicotinoid seed treatments on soybean aphid and its natural enemies. Journal of Pest Science 85: 125–132. Google Scholar

55.

Siebert MW, Thomas JD, Nolting SP, Leonard BR, Gore J, Catchot A, Lorenz GM, Stewart SD, Cook DR, Walton LC, Lassiter RB, Haygood RA, Siebert JD. 2012. Field evaluations of sulfoxaflor, a novel insecticide, against tarnished plant bug (Hemiptera: Miridae) in cotton. The Journal of Cotton Science 16: 129–143. Google Scholar

56.

Sparks TC, Watson GB, Loso MR, Geng C, Babcock JM, Thomas JD. 2013. Sulfoxaflor and the sulfoximine insecticides: chemistry, mode of action and basis for efficacy on resistant insects. Pesticide Biochemistry and Physiology 107: 1–7. Google Scholar

57.

Stark JD, Banks JE. 2003. Population-level effects of pesticides and their toxicants on arthropods. Annual Review of Entomology 48: 505–519. Google Scholar

58.

Stark JD, Banks JE, Acheampong S. 2004. Estimating susceptibility of biological control agents to pesticides: influence of life history strategies and population structure. Biological Control 29: 392–398. Google Scholar

59.

Sundby RA. 1967. Influence of food on the fecundity of Chrysopa carnea Stephens (Neuroptera, Chrysopidae). Entomophaga 12: 475–479. Google Scholar

60.

Tran AK, Alves TM, Koch RL. 2016. Potential for sulfoxaflor to improve conservation biological control of Aphis glycines (Hemiptera: Aphididae) in soybean. Journal of Economic Entomology 109: 2105–2114. Google Scholar

61.

Varenhorst AJ, O'Neal ME. 2012. The response of natural enemies to selective insecticides applied to soybean. Environmental Entomology 41: 1565–1574. Google Scholar

62.

Weinzierl RA. 2009. Integrating pesticides with biotic and biological control for arthropod pest management, pp. 179–191 In Radcliffe EB, Hutchison WD, Cancelado RE [eds.], Integrated Pest Management: Concepts, Tactics, Strategies and Case Studies. Cambridge University Press, Cambridge, Massachusetts, USA. Google Scholar

63.

Zhu Y, Loso MR, Watson GB, Sparks TC, Rogers RB, Huang JX, Gerwick BC, Babcock JM, Kelley D, Hegde VB, Nugent BM, Renga JM, Denholm I, Gorman K, DeBoer GJ, Hasler J, Meade T, Thomas JD. 2011. Discovery and characterization of sulfoxaflor, a novel insecticide targeting sap-feeding pests. Journal of Agricultural and Food Chemistry 59: 2950–2957. Google Scholar
Rafael Carlesso Aita, Anh K. Tran, and Robert L. Koch "Susceptibility of First Instar Hippodamia convergens (Coleoptera: Coccinellidae) and Chrysoperla rufilabris (Neuroptera: Chrysopidae) to the Insecticide Sulfoxaflor," Florida Entomologist 103(2), 191-196, (10 July 2020). https://doi.org/10.1653/024.103.0206
Published: 10 July 2020
JOURNAL ARTICLE
6 PAGES


SHARE
ARTICLE IMPACT
Back to Top