Biopesticide and Parasitoid Effects on Megacopta cribraria (Hemiptera: Plataspidae) Life Stage Density and Egg Parasitism in Soybean

Abstract

Since its invasion of the southeastern United States in 2009, the bean plataspid or kudzu bug, Megacopta cribraria (F.) (Hemiptera: Plataspidae), has become an agricultural pest of soybean, Glycine max (L.) Merrill (Gardner et al. 2013, J. Entomol. Sci. 48: 355–359; Lahiri and Reisig 2016, J. Integrated Pest Manage. 7: 1–6; Ruberson et al. 2013, J. Appl. Zool. Entomol. 48: 3–13). The use of chemical-based arthropod control is the dominate means of controlling this pest (Lahiri and Reisig 2016). However, this practice can harm nontarget species including Paratelenomous saccharalis (Dodd) (Hymenoptera: Platygastridae), an egg parasitoid of M. cribraria in the kudzu bugs' native range. Paratelenomous saccharalis was first discovered in the southeastern United States in 2013, but only populations in southern Georgia and Florida have established (Gardner and Olson 2016, J. Entomol. Sci. 51: 325–328; Gardner et al. 2013; Medal et al. 2015, Florida Entomol. 98: 1250–1251). Therefore, alternative less toxic control methods are needed. One method of control is the use of biopesticides in an integrated pest management (IPM) strategy (Lahiri and Reisig 2016). Biopesticides are derived from natural materials and are less toxic than conventional pesticides; they are more pest specific, and smaller quantities are needed for control. Our objectives were to (a) determine the influence of the biopesticides Azera, Neem, and Pyganic on all life stages of M. cribraria in soybean and (b) determine the influence of these biopesticides on P. saccharalis sampled from naturally occurring M. cribraria egg masses in soybean.The study was conducted on the University of Georgia Lang experimental farm in Tifton, GA. Soybean (variety AG 6931) was planted 7 May 2014 in an area 13.7 m by 16 rows. Four treatments were randomly assigned in plots of 3.4 m by eight rows with four replications. Biopesticides were applied to the plots on 23 July at 4.10 L/ha for Azera (MGK, Minneapolis, MN) and Pyganic (MGK, Minneapolis, MN) and 2.34 L/ha for Neem (Certis, Columbia, MD). GOS (Georgia Organic Solutions, LLC) spray clean (0.95 L) was also applied to the biopesticide plots. No biopesticides were applied to the control plots. Megacopta cribraria adults and nymphs were sampled from the four middle rows, two rows alternated per sampling date, with a sweep net 38 cm in diameter for 7.31 m of rows. Egg masses were sampled by collecting a single egg mass from each sample location. Weekly sampling began on 8 July and was every 3 days after the pesticides were applied for a total of seven sampling dates. Kudzu bug developmental stages were identified and recorded in the laboratory. Egg masses were held in an environmental chamber (12:12 h [L:D]; 25 ± 2.0°C; 50 ± 10% relative humidity) for emergence of kudzu bugs or parasitoids.All data were analyzed using SAS statistical software (SAS Institute Inc., Cary, NC). The effect of date, treatment, and their interactions on the density of eggs, nymphs, and adults was tested with analysis of variance using Tukey's honestly significant difference (HSD) to separate significantly different means. Chi-square analyses were used to compare percentage of eggs and egg masses parasitized and those not parasitized by P. saccharalis among treatments.There were significant interactions between date and treatment on the density of M. cribraria third instars (Table 1). The density of third instars was higher in Pyganic than in the other treatments but only on 31 July. No interactions between date and treatment were found for the density of adults, egg masses, and second, fourth, and fifth instars (Table 1). There was a significant effect of date on the density of adults, egg masses, and first, second and fourth instars, but not fifth instars (Table 1). The density of adults was higher on 16 July than on all other sampling dates (Fig. 1). Egg mass density increased over the first three sampling dates, peaking on 22 July and remaining at this density over the later sampling dates (Fig. 1). The density of first instars was higher on 25 July than on all other sampling dates (Fig. 2). The density of second instars was higher on 23 July than on 8 and 15 July (Fig. 2). The density of fourth instars was higher on 31 July than on any other sampling date (Fig. 2). Treatment had a significant effect on the density of second instars and egg masses (Table 1). The density of second instars was significantly lower in the Azera and Neem treatments than in the control and the Pyganic treatments (Fig. 3). The density of egg masses was significantly lower in the Azera treatment than in the control, Neem, and Pyganic treatments (Fig. 3).There was a significant influence of treatment on the percentage parasitism of M. cribraria eggs (χ2 = 36.94, df = 3, P < 0.001) and egg masses (χ2 = 40.04, df = 3, P < 0.001). Parasitism was highest in the control, intermediate in the Neem, lower in the Azera, and lowest in the Pyganic treatment (Fig. 4). There was no significant influence of treatment on the percentage of eggs of M. cribraria not parasitized (χ2 = 6.38, df = 3, P = 0.095; Fig. 4). There was a significant influence of treatment on the percentage of M. cribraria total eggs (χ2 = 10.49, df = 3, P = 0.015), those hatched (χ2 = 8.80, df = 3, P = 0.032), and those not hatched (χ2 = 12.62, df = 3, P = 0.006). A higher percentage of eggs was found in the control than in the biopesticide treatments (Fig. 5). A lower percentage of eggs hatched, and a higher percentage of eggs did not hatch in the Azera treatment (Fig. 5). The least percentage of eggs not hatched was found in the Pyganic treatment (Fig. 5).We found that Neem and especially Azera had a negative effect on the density of second instars of M. cribraria in soybean, with almost 100% fewer numbers of these instars compared with the control. Neem treatments showed a 50% reduction in the density of second instars in soybean compared with the control. The number of M. cribraria egg masses was also lowest in the Azera treated soybean, and the number of M. cribraria eggs that did not hatch was highest in the Azera-treated soybean compared with the control and other biopesticide treatments. This suggests that Azera may be effective in reducing M. cribraria eggs and second-instar nymphs in soybean. However, Azera-treated soybean had fewer parasitized M. cribraria eggs and egg masses than the control and Neem treatment. Given the reduction in second instars treated with Neem and Neem's lower negative effect on egg and egg mass parasitism, Neem may be the most suitable alternative control method for M. cribraria in an IPM management strategy. The benefits of Neem as a biopesticide have been reviewed in Unsal (2019, Turkish J. Agric. Food Sci. Tech. 7: 1415–1423). Laboratory assays of Azera show high mortality of brown marmorated, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), and other stink bug adults and nymphs, but field studies in pepper and tomato indicated no effect on these pests (Morehead and Kuhar 2017, J. Pest Sci. 90: 1277–1285). To the best of our knowledge, this is the first report of Azera as a biopesticide of kudzu bugs. The Pyganic biopesticide had the lowest parasitized M. cribraria eggs and egg masses and had no effect on any M. cribraria life stage, suggesting the use of Pyganic may not be a suitable strategy for M. cribraria control in soybean. No control of the crucifer flea beetle, Phyllotreta cruciferae (Goeze) (Coleoptera: Chrysomelidae), on canola and brown marmorated and other stink bugs on pepper and tomato has been found (Briar et al. 2018, Phytoparasitica 46: 247–254; Morehead and Kuhar 2017), but the compound has been effective against whiteflies, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), in squash (Razze et al. 2016, J. Econ. Entomol. 109: 1766–1771) and had no effect on the whitefly predator Delphastus catalinae (Horn) (Coleoptera: Coccinellidae) when the predator was released 5 days after pesticide application.