Invasive species are major environmental and economic threats to agroecosystems in the United States (Pimentel 2005). Recently, the invasive brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), has become a serious nuisance and agricultural pest in the mid-Atlantic region of the United States, particularly in tree fruit, vegetables, and row crops (Leskey et al. 2012c). Halyomorpha halys was accidently introduced from Beijing, China in the mid-1990s (Hoebeke & Carter 2003; Xu et al. 2013) and as of 2013 has been officially detected in 40 states and the District of Columbia based on state records and BMSB Working Group assessments (Leskey & Hamilton 2013). Halyomorpha halys is a very mobile and polyphagous pest with >100 host plants identified in Asia (Lee et al. 2013a) and the U.S. (Bernon 2004).

When Halyomorpha halys populations increased dramatically in the mid-Atlantic region, the use of insecticides by growers rapidly changed in response to the immediate threat posed by this new stink bug species. Halyomorpha halys adults and nymphs feed on numerous crops causing direct feeding injury on fruit (Leskey et al. 2012c). Following the devastating crop losses in 2010 in this region due to H. halys, growers were forced to rely on broad-spectrum chemistries (e.g., pyrethroids and carbamates) thereby deviating from sustainable IPM programs. Some tree fruit growers in the region increased the number of insecticide applications nearly four-fold in 2011 (Leskey et al. 2012a). Natural enemy abundance has plummeted, leading to frequent secondary pest outbreaks (e.g., mites and aphids). This type of management program is not financially or ecologically sustainable for growers and does not meet the needs for organic growers.

Organic production utilizes a diverse array of cultural and biological control tactics as alternatives to synthetic insecticides to reduce the level of crop injury by arthropod pests (Zehnder et al. 2007). Few alternatives to synthetic insecticides are available to organic growers for management of H. halys (Lee et al. 2013a) and therefore, organic insecticides may play a key role until cultural and biological control tactics are developed and adopted. Organic insecticides may also continue being used in conjunction with other management tactics. To date, very little is known regarding the efficacy of insecticidal materials approved for use in organic farming against H. halys and fewer organic insecticides are available compared with conventional insecticides that have proven effective against other pentatomids (Durmusoglu et al. 2003; Trdan et al. 2006; Mahdian et al. 2007; Kamminga et al. 2009).

Along with the lethal effects of insecticides, conventional and organic materials may also affect fecundity, feeding, and dispersal of target or non-target insects (Haynes 1988; Desneux et al. 2007). Laboratory bioassays have documented changes in H. halys motor skills (e.g., climbing and walking) after exposure to synthetic insecticides (e.g., pyrethroids) (Leskey et al. 2012b; Lee et al. 2013b). Given that H. halys is considered a highly mobile pest, adults could disperse within and among plots and farms even after exposure to insecticide residues. Therefore, the impact of insecticides on H. halys mobility should be considered when developing management programs.

In the study reported here, we evaluated the lethality of organically-approved insecticides and experimental biopesticides against adult H. halys in laboratory bioassays. Organically-approved insecticides are natural or synthetic products that have been produced through approved methods that have met specific requirements and are generally regarded as safe and “do not contribute to the contamination of crops, soil or water” as specified by USD A National Organic Program Rule 7 under section 205.600. Other products evaluated included: biopesticides, which refer to certain types of pesticides derived from such natural materials as animals, plants, bacteria, and certain minerals (EPA 2013) and kaolin clay which forms a dry particulate film and is known to discourage insect foraging and oviposition (Leskey et al. 2010). In addition to lethal toxicity, we also determined whether insecticide exposure affected walking mobility of adults on horizontal and vertical surfaces. This information will ultimately assist in development of effective management programs for this invasive species in organic agricultural production.

Materials and Methods

Lethality Test

Insecticide lethality was evaluated based on guidelines published by the International Organization of Biological Control (Candolfi et al. 2000) and general methods described in detail in Leskey et al. (2012b). Wild overwintering H. halys adults were collected from man-made structures in Jefferson and Berkeley County, WV. The insects were maintained with food including potted soybean plants, peanuts, carrots and sunflower seeds, and water in a laboratory colony at ∼25 °C, ∼60% RH and 16:8 h L:D for ≥2 wk to break diapause.

Organically-approved insecticides were mixed in accordance with the label recommendations for tree fruit at a rate of 935 L of water per ha. In addition to registered materials, three experimental biopesticides, MBI-203 (Chromobacterium subtsugae Martin et al. strain PRAA4-V^T) (Martin et al. 2007), MBI-205 (extract of Eucalyptus sp.) and MBI-206 (Burkholderia sp.) (Marrone BioInnovations, Davis, California), were tested (Table 1). At the completion of this study, MBI-203 (trade name: Grandevo) and MBI-206 (trade name: Venerate) have been approved by the National Organic Program. With the exception of kaolin clay and the experimental biopesticides, all materials were tested at the highest recommended rate. For each bioassay arena, 505 µl of formulated material was atomized onto glass Petri dishes and lids (100 × 15 mm; Kimble Chase, Vineland, New Jersey) and then dried under the fume hood for 18 h prior to the start of the bioassays. A total of eight insecticide treatments were evaluated in this study and water alone was used as an untreated control.

Thirty H. halys adults (sex ratio = 1:1) were evaluated individually for response to each insecticide within a treated Petri dish arena. Dishes for the untreated controls were atomized with water. Two untreated control treatments were included over the course of the bioassays for a total of 60 individuals. Adults were exposed individually to the dried residues for 4.5 h in the arena. After the 4.5-h exposure period, H. halys were transferred individually into clean 30-ml plastic cups (Jetware, Hatfield, Pennsylvania) with peanuts, sun-dried tomatoes, and water. Thereafter, adults were monitored daily over 7 d for survivorship and assigned a physical condition (alive, affected, moribund or dead). Each individual represented a replicate. H. halys rated as ‘alive’ showed no signs of intoxication, could move horizontally and vertically, and appeared to feed normally. An ‘affected’ bug was capable of moving, but with irregular, lethargic motions. A ‘moribund’ bug was nearly immobilized, typically lying on its dorsum and only capable of slight movements of a leg or antenna. A ‘dead’ bug no longer exhibited any movement, even in response to probing. The insecticide lethality was calculated as the percentage of ‘moribund’ plus ‘dead’ individuals for each daily observation period, and this mortality rate of H. halys was used to compare insecticide efficacy with the untreated control. The data were analyzed using a generalized linear model with binomial distribution for each daily observation period (JMP Genomics 5.0, SAS Institute Inc., Cary, North Carolina). P-values were adjusted using the Bonferroni correction for multiple comparisons. Each individual H. halys was evaluated in the following mobility tests over the course of the 7-d experiment period.

Table 1.

Insecticides tested against adult Halyomorpha halys in the laboratory bioassays.

Results

Insecticidal Efficacy

Overall, there was a significant difference in the lethality of H. halys adults (i.e., the percentage of ‘moribund’ plus ‘dead’ individuals) between the untreated control and insecticide treatments over a 7-d experiment period (P < 0.001) (Fig. 1). In general, the insecticide lethality increased over time, suggesting there was no significant recovery of H. halys from the moribund state after exposure to the insecticide residues evaluated in this study. Pyrethrins and pyrethrins + kaolin resulted in significantly higher lethality rates compared with the untreated control immediately after 4.5-h insecticide exposure (pyrethrins: χ ² = 29.520, df = 1, P < 0.001; pyrethrins + kaolin: y = 18.499, df = 1, P < 0.001). Other materials, except for azadirachtin, began to yield significantly higher lethality 3 d after the 4.5-h exposure to insecticide residues (P < 0.05). All materials, except for azadirachtin (y = 4.575, df = 1, P = 0.260), resulted in significantly higher rates of lethality of adults after 7 d, compared with the untreated control (P lt; 0.05) (Fig. 1). Among insecticide treatments, exposure to MBI-203 residues resulted in the highest lethality rate after 7 d.

Fig. 1.

Percentage of adult Halyomorpha halys by physical condition over 7 d following 4.5-h exposure period on insecticide-treated and untreated surfaces in the Petri dish arenas. Asterisk indicates that insecticide lethality (the percentage of ‘moribund’ plus ‘dead’ individuals) was significantly different from the untreated control (P < 0.05).

Insect Mobility

In the Petri dish arenas treated with insecticides, H. halys adults exposed to pyrethrins moved significantly greater horizontal distances compared with the untreated control, during the first 10 min of insecticide exposure (P < 0.05) (Table 2). However, this elevated walking distance by pyrethrins was not observed during the first 10-min period when the material was applied with kaolin. At 1.5 h, horizontal distance moved by adults exposed to pyrethrins + kaolin was significantly less than the untreated control (P < 0.05). At 3.0 and 4.5 h, H. halys adults moved significantly longer distances and for longer periods of time compared with the untreated control when exposed to MBI-203 (P < 0.05).

Table 2.

Mean horizontal movement distance (cm) and duration (s) of adult Halyomorpha halys over a 10-min period at 0.0, 1.5, 3.0, and 4.5 h after introduction into the petri dish arenas.

For H. halys exposed to potassium salts, pyrethrins, and pyrethrins + kaolin, vertical distance climbed by surviving (i.e., ‘alive’ or ‘affected’) adults was significantly lower compared with the untreated control immediately after the 4.5-h exposure period (P < 0.05) (Table 3). Conversely, adults exposed to MBI-203 moved significantly greater distances compared with the control (P < 0.05) after the 4.5-h exposure period. At 7 d, there was no significant difference in the vertical distance moved by surviving H. halys compared with the untreated control for any of the treatments.

Discussion

Limited information is available for insecticidal efficacy of organically-approved materials against H. halys. Organically-approved materials and experimental biopesticides tested in this study had lethal effects on adult H. halys within the laboratory setting. With the exception of azadirachtin, exposure to insecticides resulted in significantly greater mortality of H. halys over a 7-d period compared with the untreated control. Pyrethrins and pyrethrins + kaolin resulted in knockdown effects on H. halys yielding significantly higher lethality immediately after 4.5-h exposure to dried residues. Other materials generally resulted in significant insecticidal effects three or four days after the 4.5-h exposure period. There was virtually no recovery of H. halys from a moribund state after exposure to the organic compounds tested in this study. H. halys adults used in this study were older, overwintered bugs. Based on season-long trials examining the effect of residual activity of synthetic insecticides against H. halys, overwintered adults were much easier to kill with insecticides than new generation adults later in the season (Leskey et al. 2013). Thus, organic materials evaluated here may be more effective against overwintered adults, but less so against younger, new generation adults later in the season.

Table 3.

Mean vertical movement distance (cm) of adult Halyomorpha halys over a 15-min period at 4.5 h and 7.0 d after exposure to treatments.

Other researchers have reported varying levels of efficacy of organic materials against other pentatomids. Pyrethrins, an organic insecticide group derived from Chrysanthemum spp. (Casida 1980), were effective against the green stink bug, Chinavia hilaris (Say), but not the brown stink bug, Euschistus servus (Say), in laboratory bioassays (Kamminga et al. 2009). We found that H. halys was susceptible to pyrethrins with 73% lethality after 7 d following 4.5-h exposure to dried residues. Trdan et al. (2006) recommended the use of potassium salts against cabbage stink bugs (Eurydema spp.) as a reduced toxicity insecticide, although its effectiveness was inferior to that of a synthetic insecticide such as malathion (organophosphate). A product containing fatty acid of the neem seeds and 25% potassium salt was effective on the southern green stink bug Nezara viridula (L.) nymphs but not adults (Durmusoglu et al. 2003). Here, we found that H. halys was susceptible to potassium salts but not to azadirachtin, a neem-based product. Spinosad has been tested and used for management of many insect pests (Sparks et al. 2012), such as Diptera (Burns et al. 2001), Lepidoptera (Zhao et al. 2002), and Thysanoptera (Eger et al. 1998). Kamminga et al. (2009) reported that spinosad was as effective as lambda-cyhalothrin in laboratory bioassays against C. hilaris and E. servus. Spinosad was also promising against H. halys in our studies, and this material has demonstrated selectivity against the predatory stink bug, Picromerus bidens (L.) (Mahdian et al. 2007).

Experimental biopesticides tested in this study exhibited insecticidal activity against H. halys at levels comparable with other organically-approved compounds (Fig. 1). MBI-203 is formulated from a strain of Chromobacterium subtsugae that has shown activity against Colorado potato beetle (Leptinotarsa decemlineata Say), yellowmargined leaf beetle (Microtheca ochroloma Stål), and southern green stink bug (N. viridula) (Martin et al. 2007; Balusu & Fadamiro 2012). MBI-205 is based on the extract of Eucalyptus sp. Eucalyptus essential oil has been demonstrated to possess a wide spectrum of biological activity including insecticidal and repellency effects on mosquitoes and flour beetles (Batish et al. 2008). MBI-206 consists of a new bacterial species of the genus Burkholderia isolated from soil with reputed broad insecticidal effects on chewing and sucking insects (Asolkar et al. 2013).

In addition to the lethal impact of insecticides, the tested materials were also evaluated for their effects on mobility of adult H. halys. Exposure to pyrethrins resulted in an immediate elevation in horizontal movement of H. halys compared with the untreated control. This activity waned after 1.5 h to levels observed in the untreated control. Pyrethroids, synthetic versions of pyrethrins, have been shown to cause similar immediate locomotive stimulation of H. halys, although synthetic pyrethroids typically yielded greater toxicity thereby leaving most individuals moribund within a 4.5-h exposure period (Leskey et al. 2012b; Lee et al. 2013b). There was also a significant increase in horizontal mobility in both distance and duration of H. halys movement after 3 h of exposure when exposed to MBI-203 indicating that the onset of insecticide effects was not as immediate as pyrethrins.

For vertical mobility, distances climbed by surviving H. halys after the 4.5-h exposure period was significantly less than the untreated control for potassium salts, pyrethrins, and pyrethrins + kaolin; however, the climbed distance was significantly greater for MBI-203. Changes in H. halys mobility are an important consideration in management programs in conjunction with insecticidal efficacy. For example, low initial knockdown but increased mobility of H. halys adults exposed to MBI-203 needs to be considered because the majority of surviving H. halys are likely to maintain the capacity to disperse from insecticide-treated areas. This may facilitate pest dispersals within/among crops. Alternatively, although speculative, MBI-203 could work as a repellent on crops. In contrast, pyrethrins + kaolin showed relatively rapid knockdown effects compared with other test materials and decreased the mobility of surviving H. halys, indicating that this treatment not only could result in high mortality, but also, perhaps, reduce the likelihood of surviving adults to escape from the treated area. Further studies are warranted to evaluate how these non-lethal effects would affect the overall management efficacy at larger scales in time and space.

Currently, organic growers have few options to effectively and sustainably manage H. halys. The results reported here indicate that some organically-approved insecticides and experimental biopesticides hold promise for management of H. halys. In general, the materials tested in this study yielded significantly higher mortality of H. halys and affected the insect mobility to varying degrees in the laboratory bioassays. The changes in mobility may have different implications for pest management depending on crop systems and pest pressure. This baseline information should be further validated in the field in order to develop appropriate treatment recommendations for organic growers.