FIELD AND FORAGE CROPS Efficacy of Selected Insecticides Against Eggs of Euschistus servus and Acrosternum hilare (: ) and the Egg Parasitoid Telenomus podisi (Hymenoptera: Scelionidae)

1 2 3 2 2 A. L. KOPPEL, D. A. HERBERT, JR., T. P. KUHAR, S. MALONE, AND M. ARRINGTON

J. Econ. Entomol. 104(1): 137Ð142 (2011); DOI: 10.1603/EC10222 ABSTRACT Brown stink bug, Euschistus servus (Say), and , Acrosternum hilare (Say) (Hemiptera: Pentatomidae), are major agricultural pests. Although various insecticides are used to control nymphs and adults, little is known about how they affect eggs. Laboratory bioassays and Þeld trials were conducted to determine the efÞcacy of common Þeld rates of acephate, ␭-cyhalothrin, spinosad, and thiamethoxam on developing E. servus and A. hilare eggs, as well as Telenomus podisi Downloaded from Ashmead (Hymenoptera: Scelionidae) parasitoids developing in E. servus eggs. In laboratory bioas- says, egg masses were dipped into insecticide and water solutions and assessed for mortality after 2 wk. In the Þeld trials, egg masses on a cloth section were pinned to leaves in each plot of a randomized complete block and returned to the laboratory 24 h after exposure to insecticide sprays. Mortality was assessed after 2 wk. In dip bioassays, there was a signiÞcant effect of insecticide treatment on A. hilare

eggs with all insecticides resulting in greater mortality than the water control. However, no effect of http://jee.oxfordjournals.org/ treatment occurred in the Þeld with A. hilare or for E. servus eggs in both the laboratory bioassays and the Þeld trials. In contrast, developing T. podisi parasitoids showed signiÞcant mortality when exposed to all insecticide treatments, when dipped or Þeld-treated. Spinosad and ␭-cyhalothrin treatments resulted in 100% mortality of T. podisi, and acephate resulted in greater mortality than thiamethoxam. Our results suggest that there is relatively little efÞcacy from insecticide sprays on stink bugs developing in eggs but that mortality of egg parasitoids may be signiÞcant.

KEY WORDS Pentatomidae, Scelionidae, egg efÞcacy, chemical control by guest on November 17, 2016

In Virginia, brown stink bug, Euschistus servus (Say), to pesticide sprays, either as adults or while develop- and the green stink bug, Acrosternum hilare (Say), are ing in stink bug eggs. major agricultural pests. They are polyphagous, feed- The efÞcacy of insecticides on parasitoids has been ing on the fruiting bodies of shrubs, trees, grasses, row explored in other studies. Waddill (1978) subjected crops, fruiting vegetables, and fruit and can survive on several adult parasitoids, including Telenomus remus weedy hosts (McPherson and McPherson 2000). Py- (Nixon) (Hymenoptera: Scelionidae), to treatment rethroid or organophosphate insecticides are typically with pyrethroids, including permethrin, resulting in used for control in most crops (Herbert 2008), but high mortality. A high mortality also was recorded other control options, such as organic pesticides and within6hofexposure to methyl parathion, which also biological control, also are being investigated (Kam- caused high mortality in other hymenopteran parasi- minga et al. 2008). Pesticide sprays are timed to target toids, including members of the families Chalcididae, stink bug nymphal and adult stages, but little research Braconidae, and Ichneumonidae (Wilkinson et al. 1975). has been done to determine how these insecticides However, another study found that almost all adult Tris- affect the stink bug eggs or the natural enemies asso- solcus basalis (Wollaston), in two repetitions, survived ciated with them. exposure to permethrin (Orr et al. 1989). Stink bug egg parasitoids such as Telenomus podisi An important consideration in the study of insec- Ashmead (Hymenoptera: Scelionidae) are present ticide efÞcacy on embryonic Euschistus servus (Say) throughout the stink bug Þeld season, parasitizing up and Telenomus podisi Ashmead (Hymenoptera: Sce- to 50% of stink bug egg masses (Koppel et al. 2009) in lionidae) is that of the structure and physiology of host southeastern Virginia, and they are probably subject eggs, which serve to protect developing embryos. Bea- ment (1948) studied the properties of Rhodnius pro- 1 Corresponding author: Department of Entomology, Virginia lixus Stål (Hemiptera: Reduviidae) eggs, stating that it Tech, Blacksburg, VA 24061 (e-mail: [email protected]). could serve as a “type specimen” for hemipterous 2 Department of Entomology, Tidewater AREC, Virginia Tech, pest-speciesÕ eggs. He proposed that micropyles, Suffolk, VA 23437. 3 Department of Entomology, Eastern Shore AREC, Virginia Tech, which penetrate some eggshell layers, are crucial to Painter, VA 23420. the transport of insecticides into eggs because chorion

0022-0493/11/0137Ð0142$04.00/0 ᭧ 2011 Entomological Society of America 138 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 104, no. 1

Table 1. Insecticides evaluated for efficacy in laboratory bioassays and field trials

Bioassay Material Product Manufacturer Class Field rate formulation Acephate Orthene 97 SPa Amvac Chemical Corp. Organophosphate 5.28 g (AI)/liters 0.82 kg (AI)/ha ␭-Cyhalothrin Warrior ZT Syngenta Crop Protection, Inc. Pyrethroid 0.22 g (AI)/liter 0.03 kg (AI)/ha Spinosad Entrust 80 Wb Dow AgroSciences LLC Spinosyn 1.09 g (AI)/liters 0.18 kg (AI)/ha Thiamethoxam Centric 40 WGc Syngenta Crop Protection, Inc. Neonicotinoid 0.36 g (AI)/liter 0.06 kg (AI)/ha

a Soluble pellet. b Wettable powder. c Water-dispersible granules. is impermeable to ovicidal or toxic substances, even if transferred adults died, they were replaced with there are smaller molecules of methyl alcohol or acetic newly emergent adults. When the fresh egg masses dark- acid present (Beament 1952). ened, T. podisi were transferred to a new E. servus egg The uptake of speciÞc classes of insecticides into mass. All eggs used for laboratory bioassays and Þeld eggs also has been studied. Organophosphates trials were 3 d old or younger from the time they were have been used as ovicides, but eggs of some insect laid or parasitized. Parasitized eggs used for the efÞcacy Downloaded from species have developed resistance to this insecticide study were stored in a 5ЊC refrigerator for no Ͼ3d. group due to biochemical differences in the esterase Laboratory Bioassay. Individual parasitized and complex of resistant strain embryos (Smith and nonparasitized egg masses were gathered for the bio- Salkeld 1966). Furthermore, parathion does not act as assay. Acephate, ␭-cyhalothrin, spinosad, and thiame- a true ovicide on the eggs of large milkweed bug, thoxam were each mixed with 2,500 ml of water, to Oncopeltus fasciatus (Dallas), because the penetration match a typical spray tank concentration based on barrier of eggs does not allow enough insecticide to currently labeled (Amvac Chemical Corp. 2009; Dow http://jee.oxfordjournals.org/ ßow into the eggs to kill the embryo (Zschintzsch et AgroSciences LLC 2009; Syngenta Crop Protection, al. 1965). However, it has been demonstrated that Inc. 2009a,b) and recommended Þeld rates (Herbert symptoms of organophosphate toxicity coincide very 2008; Table 1), with water as a control. Rates were closely with cholinesterase inhibition in O. fasciatus determined from stink bug control recommendations eggs (Smith and Salkeld 1966). Both cholinesterase on pesticide labels. After formulation, 500 ml of each and acetylcholine occur in these eggs at4dofdevel- insecticide solution was poured into separate mason opment (Mehrotra 1960). jars. Egg masses in eight repetitions were randomly The objective of this study was to assess insecticide assigned treatment levels, in a randomized complete efÞcacy on developing stink bugs and parasitoids in block experimental design, and were dipped for 1 s. by guest on November 17, 2016 pentatomid eggs by using insecticides in four classes: Each mass was placed into a labeled 47-mm Millipore neonicotinoids, organophosphates, pyrethroids, and dish and returned to the growth chamber. After 2 wk, spinosyns. mortality of developing was assessed based on the number of individual eggs within each mass that hatched or had an adult emerge. Materials and Methods In total, 770 E. servus eggs, 471 parasitized E. servus Rearing. E. servus eggs, either nonparasitized or eggs, and 1,428 A. hilare eggs were dipped in insecti- parasitized by T. podisi, and nonparasitized A. hilare cides in the laboratory bioassay. Each treatment rep- eggs, were used in this study. Host eggs were obtained etition consisted of one stink bug egg mass, and there from a laboratory-reared colony of stink bugs as per were eight repetitions per treatment group. previously described methods (Koppel et al. 2009). To Field Trials. Plots of Asgrow brand ÔAG 5905 RRÕ obtain parasitized eggs, T. podisi founders were Þeld- soybean, Glycine max (L.) Merr. at the Virginia Tech collected. Fresh E. servus egg masses were pinned to Tidewater Agricultural Research and Extension Cen- the undersides of leaves or on stems of host plants that ter near Suffolk, VA, were planted on 30 June 2009. were located on the margins of Þelds, on sunny days When plants reached the full pod stage of develop- with light wind. After 48 h, the egg masses were col- ment, the experiment was conducted. Soybean plots lected and returned to a growth chamber (24.4ЊC, 85% were divided into four, 4.6-m rows per treatment, with RH, and a photoperiod of 14:10 [L:D] h). four replicates, arranged in a randomized complete When the eggs turned black, it signaled that they block experimental design. Each of the plots within a had been parasitized. These parasitized eggs were block was randomly assigned a treatment. A stink bug placed into 47-mm Millipore dishes (Millipore, Bil- egg mass on a strip of substrate (Kleenex Viva scrub lerica, MA), with a few drops of honey on the lid, and cloths, Kimberly-Clark, Neenah, WI) was pinned to returned to the growth chamber. the midvein on the underside of a soybean leaf, lo- The eggs were observed daily, and emergent adults cated near the middle of the row, no more than three were transferred to a new 47-mm Millipore dish, con- leaves from the top of the canopy. Insecticide treat- taining a newly laid (Ͻ3-d-old) E. servus egg mass. ments were formulated in the same manner as the dip Each dish had a 3:2 female-to-male ratio per egg mass, tests (Table 1). Treatments were broadcast with a and a few drops of honey on the lid. If any of the spider Þeld sprayer calibrated to deliver 154.05 liters/ha February 2011 KOPPEL ET AL.: EFFICACY OF INSECTICIDES AGAINST STINK BUGS AND PARASITOIDS 139

Fig. 1. Mortality of the parasitoid T. podisi, developing in E. servus egg masses, when dipped into Þeld-formulated insecticide solutions. N, number of eggs, markers indicate SE. Untransformed hatch proportion data were analyzed. *, mortality of T. podisi in eggs dipped in water (dark bar) was signiÞcantly lower (F ϭ 11.96; df ϭ 4, 35; P Ͻ 0.0001) than the mortality of those dipped in insecticide treatments. Downloaded from at 2.04 atmospheres through 8002VS spray nozzles partial insect emergence from eggs. All insects that (TeeJet Technologies, Wheaton, IL) spaced 45.7 cm hatched from eggs did so completely. apart on the spray boom. There were no signiÞcant differences in mortality of After 24 h, egg masses were retrieved, placed into a developing E. servus among treatments in both the labeled 47-mm Millipore dish, and returned to the laboratory (F ϭ 1.44; df ϭ 4, 35; P ϭ 0.24) and Þeld http://jee.oxfordjournals.org/ growth chamber. After 2 wk, mortality of developing trials (F ϭ 0.08; df ϭ 11, 4; P ϭ 0.99). Mortality of insects was assessed based on individual egg hatch or developing stink bugs ranged from 15 to 40% in the parasitoid emergence. laboratory studies and from 40 to 54% in the Þeld. There were 648 E. servus eggs, 612 parasitized E. Mortality values had a standard error of approximately servus eggs, and 1,114 A. hilare eggs analyzed in the Ϯ10%. However, there was a signiÞcant effect of treat- Þeld trials. Each treatment repetition consisted of one ment on T. podisi mortality when parasitized eggs stink bug egg mass, and there were eight repetitions were treated with insecticides in laboratory bioassays per treatment group. (F ϭ 11.96; df ϭ 4, 35; P Ͻ 0.0001) and Þeld trials (F ϭ Statistical Analysis. Individual eggs from the eight 19.93; df ϭ 11, 4; P Ͻ 0.0001). In the lab, T. podisi by guest on November 17, 2016 egg masses per treatment group were pooled for sta- experienced greater mortality with all insecticide tistical analysis. Masses were not analyzed because of treatments than when treated with water (Fig. 1), but the difÞculty in assigning quantitative hatch values to there were no differences in mortality among the a mass where only some individuals emerged. Both insecticide treatments. In the Þeld experiments, T. one-way analysis of variance (ANOVA) and Fisher podisi mortality averaged 100% in the spinosad and least signiÞcant difference tests were performed for ␭-cyhalothrin treatments (Fig. 2), which was signiÞ- each data set (PROC GLM, SAS Institute 2002-2005). cantly greater than in the other treatments (P Ͻ 0.05). An arcsine square-root transformation was performed When the data were analyzed without these two in- on proportion mortality data before analysis, and both secticides, there was signiÞcantly greater T. podisi transformed and untransformed data were analyzed. mortality in eggs treated with acephate than with Two-way ANOVA, also testing for an interaction ef- thiamethoxam or water (F ϭ 18.24; df ϭ 9, 2; P ϭ fect between treatment and insect type, was used to 0.0001). analyze combined E. servus and T. podisi bioassay In addition, there was a signiÞcant effect of insec- results. This test also was used for combined Þeld trial ticide treatment on A. hilare mortality when eggs were results for all developing insect species. Due to highly treated with insecticides in laboratory bioassays (F ϭ variable error variance in the A. hilare egg laboratory 71.6; df ϭ 4, 35; P Ͻ 0.0001), but not in Þeld trials (F ϭ data, both a one-way ANOVA and Fisher exact tests 1.04; df ϭ 11, 4; P ϭ 0.40). In the laboratory dip also were performed on that data set using PROC bioassays, all insecticides had signiÞcantly higher mor- FREQ (SAS Institute 2002Ð2005) on individual treat- tality than the water control (Fig. 3), and there were ment comparisons. Statistical analysis of transformed no differences among the insecticides. The mortality and untransformed data yielded similar results; un- of A. hilare in the Þeld trials ranged from 20 to 50%, transformed numbers and statistics are reported un- with a standard error of ϷϮ10%. less otherwise noted. When laboratory bioassay arcsine-transformed data from developing insects in nonparasitized and para- sitized E. servus eggs were analyzed together, statistics Results indicated that insecticide treatments resulted in an When eggs were returned to the laboratory for overall greater mortality to developing T. podisi than observation, we noted that there was no evidence of to developing E. servus (F ϭ 84.63; df ϭ 9, 1; P Ͻ 140 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 104, no. 1

Fig. 2. Mortality of the parasitoid T. podisi, developing in E. servus egg masses, when placed into a soybean plot and sprayed with Þeld-formulated insecticides at the standard rate. N, number of eggs, markers indicate SE. Untransformed hatch Downloaded from proportion data were analyzed. *, mortality of T. podisi in eggs dipped in spinosad and ␭-cyhalothrin was signiÞcantly greater (F ϭ 19.93; df ϭ 11, 4; P Ͻ 0.0001) than in the other treatments. **, when the treatments were analyzed with spinosad and ␭-cyhalothrin (100% mortality) omitted, there was signiÞcantly greater mortality in T. podisi developing in eggs treated with acephate (F ϭ 18.24; df ϭ 9, 2; P ϭ 0.0001).

0.0001). Furthermore, there was signiÞcantly less mor- analysis suggested that thiamethoxam treatments re- http://jee.oxfordjournals.org/ tality of developing insects when exposed to water and sulted in signiÞcantly lower mortality to developing ␭-cyhalothrin (F ϭ 3.42; df ϭ 4, 4; P ϭ 0.0013) than the insects than the other three insecticides (F ϭ 4.97; other three treatments. Due to the error variances of df ϭ 32, 3; P ϭ 0.0037) and that there was signiÞcantly the A. hilare bioassay data, they were not included in higher mortality, overall, to developing T. podisi (F ϭ this analysis. 37.95; df ϭ 32, 2; P Ͻ 0.0001) than to stink bugs. It is difÞcult to draw deÞnite conclusions from the combined analysis of Þeld trial data for insects in Discussion nonparasitized A. hilare, and all E. servus eggs. Both

the untransformed and arcsine-transformed data con- When nonparasitized and parasitized stink bug eggs by guest on November 17, 2016 tained a signiÞcant interaction effect between egg were treated with water, there was 20Ð60% control status and treatment. Water seemed to account for mortality in developing insects. These levels were too this, and was removed from the analysis such that only high for AbbottÕs formula to be used for adjustment, the four insecticide treatments were analyzed. In this and it is unknown why high percentage of mortality case, the arcsine-transformed data still indicated that occurred. However, past stink bug parasitoid survey there was an interaction between egg status and treat- data (Koppel et al. 2009) shows that T. podisi in Þeld- ment, but the untransformed data did not. The latter collected parasitized eggs have naturally occurring

Fig. 3. Mortality of developing A. hilare in eggs when dipped into Þeld-formulated insecticide solutions. N, number of eggs, markers indicate SE. Hatch proportion data were normalized with an arcsine transformation. *, mortality of A. hilare in eggs dipped in water (dark bar) was signiÞcantly lower (F ϭ 71.6; df ϭ 4, 35; P Ͻ 0.0001) than all insecticide treatments. February 2011 KOPPEL ET AL.: EFFICACY OF INSECTICIDES AGAINST STINK BUGS AND PARASITOIDS 141 levels of mortality ranging from 0 to 50% and that dae) eggs when they have been treated with insecti- developing A. hilare in nonparasitized Þeld-collected cides (Varma and Singh 1987). eggs had 20.6% mortality. Mortality ranged from 5 to Because developing stink bugs in the next genera- 80% for E. servus in Þeld-collected and lab-reared eggs tion will hatch from eggs in greater numbers than egg (A.L.K., unpublished data). Thus, the levels of control parasitoids, it is important for growers to use insecti- mortality observed in this study are comparable to that cides only as needed. Excessive applications of insec- of developing insects in eggs observed in past studies. ticide could decrease the population of T. podisi In general, this study showed that the selected in- enough to reduce naturally occurring parasitization to secticides were more toxic to developing parasitoids unnoticeable levels. Field data from Louisiana indi- and A. hilare than to developing E. servus. Further- cated that nymphal populations of stink bugs rapidly more, A. hilare in bioassays experienced greater mor- increased after applications of methyl parathion and tality when treated with insecticides than those in the permethrin (Orr et al. 1989), which Orr interprets as Þeld trials, which may be attributed to wind conditions a possible reßection of stink bug predator mortality. when the insecticides were sprayed, decreasing foliar Given the results of this efÞcacy study, a similar effect coverage. Developing A. hilare were completely sub- is possible as a result of parasitoid mortality. merged in insecticide solutions in the laboratory bio- Perhaps growers could limit their chemical appli- assay. The bioassay results suggest that developing A. cations to key times in the summer Þeld season when stink bug populations have reached economic thresh- hilare experienced greater mortality than developing Downloaded from E. servus, which is consistent with reports in the lit- old. Leaving more time between sprays would allow erature of A. hilare being more susceptible to insec- natural enemies a recovery period to rebuild their ticide exposure. populations in surrounding refugia. EfÞcacy studies The organophosphate dicrotophos has been cited as using a wider variety of insecticides are still needed to having a high toxicity to various stink bug species see if there are less toxic options within classes that may allow for more selective mortality of insects at the (Tillman and Mullinix 2004, Snodgrass et al. 2005), and http://jee.oxfordjournals.org/ it is suggested that insecticides provide more consis- time of application. tent control for A. hilare and Nezara viridula L., the southern green stink bug (Willrich et al. 2003, Snodgrass et al. 2005, Kamminga et al. 2008) than for Acknowledgments E. servus. Kamminga et al. (2008) performed a number We thank our colleagues D. G. Pfeiffer and S. M. Salom of efÞcacy trials on E. servus and A. hilare nymphs and (Department of Entomology, Virginia Tech), K. A. Hoelmer adults and found that A. hilare was especially suscep- (USDAÐARS BeneÞcial Introductory Research Laboratory), tible to all of the pyrethroids that were tested. and R. Arrington and A. Aston (Tidewater Agricultural Re- search and Extension Center, Virginia Tech,) for research

The high mortality of developing parasitoids in this by guest on November 17, 2016 study contrasts with previous research. Novozhilov et and writing support. Thanks also to C. Brownie (North Carolina State University) for valuable help with statistical al. (1973) found that when chlorophos, an organo- analyses. phosphate also known as trichlorfon, penetrated stink bug eggs, most of it was absorbed by the chorion and never entered the egg interior. Furthermore, several References Cited studies, including many listed by Orr (1988), and a more recent one by Sudarsono et al. (1992), have Amvac Chemical Corp. 2009. Orthene 97 specimen label. shown that preimaginal parasitoids experienced low (http://www.amvac-chemical.com/media/pdf/products/ specimen_labels/Orthene%2097%20Specimen%20(12642-3) mortality when treated with insecticides. Developing %20-%20CPS%20-%2010-12-09.pdf). parasitoids even experienced less mortality than Beament, J.W.L. 1948. The penetration of insect egg-shells. developing rice stink bugs [Oebalus pugnax (F.) I.ÑPenetration of the chorion of Rhodnius prolixus, Stål. (Hemiptera: Pentatomidae)] in a study by Sudarsono Bull. Entomol. Res. 39: 359Ð383. et al. (1992). Beament, J.W.L. 1952. The role of cuticle and egg-shell However, further studies (A.L.K., unpublished membranes in the penetration of insecticides. Ann. Appl. data) on the chorion permeability of nonparasitized Biol. 39: 142Ð143. Dow AgroSciences LLC. 2009. Entrust 80 W label. (http:// and parasitized E. servus egg masses showed that ϭ ␭ www.dowagro.com/webapps/lit/litorder.asp?Þlepath ca/ acephate, -cyhalothrin, and thiamethoxam are in fact pdfs/noreg/010-21150.pdf&pdfϭtrue). absorbed into the interior of E. servus eggs. Sales Garjan, A. S., K. Talebi, and A. A. Pourmirza. 2005. Effect of (1978) found that exposure to insecticides led to high some pyrethroid and organphosphorous insecticides on mortality of T. basalis. Studies from Iran on Trissolcus developmental stages of Trissolcus grandis (Thom.) (Hy- grandis Thompson (Hymenoptera: Scelionidae) have menoptera: Scelionidae). J. Sci. Technol. Agric. Nat. Re- indicated that insecticide treatments have signiÞ- sour. Isf. Univ. Technol. Isf. Iran 8: 165. cantly decreased the emergence of this parasitoid, Herbert, Jr., D. A. 2008. Insects: soybeans, pp. 61Ð74. In S. E. especially when applied to recently parasitized eggs Hagood and D. A. Herbert [eds.], Pest management Þeld guide Þeld crops. Virginia Cooperative Extension Publi- (Garjan et al. 2005, Saber et al. 2005). Similarly, there cation 456-420. are low rates of Trichogramma brasiliensis Ashmead Kamminga, K. L., D. A. Herbert, Jr., T. P. Kuhar, S. Malone, (Hymenoptera: Trichogrammatidae) emergence in and A. Koppel. 2008. EfÞcacy of insecticides against Corcyra cephalonica (Stainton) (Lepidoptera: Pyrali- Acrosternum hilare and Euschistus servus (Hemiptera: 142 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 104, no. 1

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